2025
Coban, Abdulbaki; Bornberg-Bauer, Erich; Kemena, Carsten
Tracing the Paths of Modular Evolution by Quantifying Rearrangement Events of Protein Domains Journal Article
In: BMC Ecology and Evolution, vol. 25, iss. 1, pp. 6, 2025.
@article{nokey,
title = {Tracing the Paths of Modular Evolution by Quantifying Rearrangement Events of Protein Domains},
author = {Abdulbaki Coban and Erich Bornberg-Bauer and Carsten Kemena},
url = {https://bornberglab.org/wp-content/uploads/2025/01/Baki2025-DomRatesSeq.pdf},
doi = {10.1186/s12862-024-02347-7},
year = {2025},
date = {2025-09-08},
urldate = {2025-09-08},
journal = {BMC Ecology and Evolution},
volume = {25},
issue = {1},
pages = {6},
abstract = {Background Protein evolution is central to molecular adaptation and largely characterized by modular rearrange‐
ments of domains, the evolutionary and structural building blocks of proteins. Genetic events underlying protein
rearrangements are relatively rare compared to changes of amino-acids. Therefore, these events can be used to char‐
acterize and reconstruct major events of molecular adaptation by comparing large data sets of proteomes.
Results Here we determine, at unprecedented completeness, the rates of fusion, fission, emergence and loss
of domains in five eukaryotic clades (monocots, eudicots, fungi, insects, vertebrates). By characterizing rearrange‐
ments that were previously considered “ambiguous” or “complex” we raise the fraction of resolved rearrangement
events from previously ca. 60% to around 92%. We exemplify our method by analyzing the evolutionary histories
of protein rearrangements in (i) the extracellular matrix, (ii) innate immunity across Eukaryota, Metazoa, and Verte‐
brata, and (iii) Toll-Like-Receptors in the innate immune system of Eukaryota. In all three cases we can find hot-spots
of rearrangement events in their phylogeny which (i) can be related with major events of adaptation and (ii) which
follow the emergence of new domains which become integrated into existing arrangements.
Conclusion Our results demonstrate that, akin to the change at the level of amino acids, domain rearrangements
follow a clock-like dynamic which can be well quantified and supports the concept of evolutionary tinkering. While
many novel domain emergence events are ancient, emerged domains are quickly incorporated into a great number
of proteins. In parallel, the observed rates of emergence of new domains are becoming smaller over time.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background Protein evolution is central to molecular adaptation and largely characterized by modular rearrange‐
ments of domains, the evolutionary and structural building blocks of proteins. Genetic events underlying protein
rearrangements are relatively rare compared to changes of amino-acids. Therefore, these events can be used to char‐
acterize and reconstruct major events of molecular adaptation by comparing large data sets of proteomes.
Results Here we determine, at unprecedented completeness, the rates of fusion, fission, emergence and loss
of domains in five eukaryotic clades (monocots, eudicots, fungi, insects, vertebrates). By characterizing rearrange‐
ments that were previously considered “ambiguous” or “complex” we raise the fraction of resolved rearrangement
events from previously ca. 60% to around 92%. We exemplify our method by analyzing the evolutionary histories
of protein rearrangements in (i) the extracellular matrix, (ii) innate immunity across Eukaryota, Metazoa, and Verte‐
brata, and (iii) Toll-Like-Receptors in the innate immune system of Eukaryota. In all three cases we can find hot-spots
of rearrangement events in their phylogeny which (i) can be related with major events of adaptation and (ii) which
follow the emergence of new domains which become integrated into existing arrangements.
Conclusion Our results demonstrate that, akin to the change at the level of amino acids, domain rearrangements
follow a clock-like dynamic which can be well quantified and supports the concept of evolutionary tinkering. While
many novel domain emergence events are ancient, emerged domains are quickly incorporated into a great number
of proteins. In parallel, the observed rates of emergence of new domains are becoming smaller over time.
ments of domains, the evolutionary and structural building blocks of proteins. Genetic events underlying protein
rearrangements are relatively rare compared to changes of amino-acids. Therefore, these events can be used to char‐
acterize and reconstruct major events of molecular adaptation by comparing large data sets of proteomes.
Results Here we determine, at unprecedented completeness, the rates of fusion, fission, emergence and loss
of domains in five eukaryotic clades (monocots, eudicots, fungi, insects, vertebrates). By characterizing rearrange‐
ments that were previously considered “ambiguous” or “complex” we raise the fraction of resolved rearrangement
events from previously ca. 60% to around 92%. We exemplify our method by analyzing the evolutionary histories
of protein rearrangements in (i) the extracellular matrix, (ii) innate immunity across Eukaryota, Metazoa, and Verte‐
brata, and (iii) Toll-Like-Receptors in the innate immune system of Eukaryota. In all three cases we can find hot-spots
of rearrangement events in their phylogeny which (i) can be related with major events of adaptation and (ii) which
follow the emergence of new domains which become integrated into existing arrangements.
Conclusion Our results demonstrate that, akin to the change at the level of amino acids, domain rearrangements
follow a clock-like dynamic which can be well quantified and supports the concept of evolutionary tinkering. While
many novel domain emergence events are ancient, emerged domains are quickly incorporated into a great number
of proteins. In parallel, the observed rates of emergence of new domains are becoming smaller over time.
Harrison, Mark C.; Séguret, Alice; Finke, Christopher; Jongepier, Evelien; Grandchamp, Anna; Stoldtd, Marah; Heinze, Jürgen; Foitzik, Susanne; Bornberg-Bauer, Erich; Feldmeyer, Barbara
Convergent Evolutionary Traces of Genomic Innovations and Depletions in Socially Parasitic Ants Journal Article Forthcoming
In: Forthcoming.
@article{nokey,
title = {Convergent Evolutionary Traces of Genomic Innovations and Depletions in Socially Parasitic Ants},
author = {Mark C. Harrison and Alice Séguret and Christopher Finke and Evelien Jongepier and
Anna Grandchamp and Marah Stoldtd and Jürgen Heinze and Susanne Foitzik and Erich
Bornberg-Bauer and Barbara Feldmeyer},
url = {https://bornberglab.org/wp-content/uploads/2024/12/vw_prag_24_group-scaled.jpeg},
doi = {https://doi.org/10.1101/2024.12.31.630940 },
year = {2025},
date = {2025-01-18},
urldate = {2025-01-18},
keywords = {},
pubstate = {forthcoming},
tppubtype = {article}
}
2024
Jones, Alun; Dohmen, Elias; Berger, Juliette; Legendre, Frederic; Harrison, Mark; Bornberg-Bauer, Erich
Reduced regulatory complexity associated with the evolutionary transition to sociality from cockroaches to termites despite evolutionary parallels with Hymenoptera Unpublished Forthcoming
Forthcoming.
@unpublished{nokey,
title = {Reduced regulatory complexity associated with the evolutionary transition to sociality from cockroaches to termites despite evolutionary parallels with Hymenoptera},
author = {Alun Jones and Elias Dohmen and Juliette Berger and Frederic Legendre and Mark Harrison and Erich Bornberg-Bauer},
doi = {https://www.biorxiv.org/content/biorxiv/early/2024/11/26/2024.11.25.625201.full.pdf},
year = {2024},
date = {2024-12-17},
urldate = {2024-12-17},
abstract = {In social species, the phenotypic diversity within a single species has often been associated with more complex genetic regulation. Transcription factors (TFs) being key to genetic regulation, have been studied in the origins of eusociality in Hymenoptera (Bees, Ants and Wasps) but less so in Blattodea (Cockroaches and Termites). Here we show that the social transition in Blattodea, from cockroaches to termites, displays similar patterns of regulatory change to those found in Hymenoptera. Specifically, by analysing 3 cockroach and 5 termite genomes, we find more TF families with relaxed selection compared to intensified selection and lineage-specific gene family expansions in termites. We also find that genes under selection support neotenic caste determination. There are key differences in TF regulation in comparison with Hymenoptera with contractions in TF gene families and reduced diversity in enriched DNA binding motifs of TFs. Furthermore, we show that with increased social complexity TF activating domain diversity, one of the evolutionary and structural building blocks of TFs, decreases with gene family size while DNA binding domain diversity and number increases. This study highlights similarities in social transitions between Hymenoptera and Blattodea, with evidence of large changes in transcriptional regulation followed by lineage specific adaptations. We also show that phenotypic diversity in termites does not necessitate greater transcriptional complexity.},
keywords = {},
pubstate = {forthcoming},
tppubtype = {unpublished}
}
In social species, the phenotypic diversity within a single species has often been associated with more complex genetic regulation. Transcription factors (TFs) being key to genetic regulation, have been studied in the origins of eusociality in Hymenoptera (Bees, Ants and Wasps) but less so in Blattodea (Cockroaches and Termites). Here we show that the social transition in Blattodea, from cockroaches to termites, displays similar patterns of regulatory change to those found in Hymenoptera. Specifically, by analysing 3 cockroach and 5 termite genomes, we find more TF families with relaxed selection compared to intensified selection and lineage-specific gene family expansions in termites. We also find that genes under selection support neotenic caste determination. There are key differences in TF regulation in comparison with Hymenoptera with contractions in TF gene families and reduced diversity in enriched DNA binding motifs of TFs. Furthermore, we show that with increased social complexity TF activating domain diversity, one of the evolutionary and structural building blocks of TFs, decreases with gene family size while DNA binding domain diversity and number increases. This study highlights similarities in social transitions between Hymenoptera and Blattodea, with evidence of large changes in transcriptional regulation followed by lineage specific adaptations. We also show that phenotypic diversity in termites does not necessitate greater transcriptional complexity.
Eenink, Bernard D. G.; Heberlein, Magdalena; Holstein, Josephin M.; Lange, Andreas; Dilkaute, Carina; Kaminski, Tomasz S.; Bornberg-Bauer, Erich; Jose, Joachim; Hollfelder, Florian; van Loo, Bert
Ancestral aryl sulfatases in the alkaline phosphatase family allow for greater increases in catalytic efficiency than extant variants Journal Article Forthcoming
In: Forthcoming.
@article{nokey,
title = {Ancestral aryl sulfatases in the alkaline phosphatase family allow for greater increases in catalytic efficiency than extant variants},
author = {Bernard D. G. Eenink and Magdalena Heberlein and Josephin M. Holstein and Andreas Lange and Carina Dilkaute and Tomasz S. Kaminski and Erich Bornberg-Bauer and Joachim Jose and Florian Hollfelder and Bert van Loo},
url = {https://bornberglab.org/wp-content/uploads/2024/12/Eeninketal-s-MBE-2024.pdf},
year = {2024},
date = {2024-12-10},
urldate = {2024-12-10},
keywords = {},
pubstate = {forthcoming},
tppubtype = {article}
}
Glaser-Schmitt, Amanda; Lebherz, Marie; Sayda, Ezgi; Bornberg-Bauer, Erich; Parsch, John
Expression of de novo open reading frames in natural populations of Drosophila melanogaster Journal Article Forthcoming
In: Forthcoming.
@article{nokey,
title = {Expression of de novo open reading frames in natural populations of Drosophila melanogaster},
author = {Amanda Glaser-Schmitt and Marie Lebherz and Ezgi Sayda and Erich Bornberg-Bauer and John
Parsch},
url = {https://bornberglab.org/wp-content/uploads/2024/10/Parsch-Lebherz-JEZB_paper_2024.pdf},
year = {2024},
date = {2024-10-30},
urldate = {2024-10-30},
keywords = {},
pubstate = {forthcoming},
tppubtype = {article}
}
Iyengar, Bharat R.; Grandchamp, Anna; Bornberg-Bauer, Erich
How antisense transcripts can evolve to encode novel proteins Journal Article
In: Nature Communications, vol. 15, no. 6187, 2024.
@article{nokey,
title = {How antisense transcripts can evolve to encode novel proteins},
author = {Bharat R. Iyengar and Anna Grandchamp and Erich Bornberg-Bauer},
url = {https://doi.org/10.1038/s41467-024-50550-3},
year = {2024},
date = {2024-07-23},
urldate = {2024-07-23},
journal = {Nature Communications},
volume = {15},
number = {6187},
abstract = {Protein coding features can emerge de novo in non coding transcripts, resulting in emergence of new protein coding genes. Studies across many species show that a large fraction of evolutionarily novel non-coding RNAs have an antisense overlap with protein coding genes. The open reading frames (ORFs) in these antisense RNAs could also overlap with existing ORFs. In this study, we investigate how the evolution an ORF could be constrained by its overlap with an existing ORF in three different reading frames. Using a combination of mathematical modeling and genome/transcriptome data analysis in two different model organisms, we show that antisense overlap can increase the likelihood of ORF emergence and reduce the likelihood of ORF loss, especially in one of the three reading frames. In addition to rationalising the repeatedly reported prevalence of de novo emerged genes in antisense transcripts, our work also provides a generic modeling and an analytical framework that can be used to understand evolution of antisense genes.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Protein coding features can emerge de novo in non coding transcripts, resulting in emergence of new protein coding genes. Studies across many species show that a large fraction of evolutionarily novel non-coding RNAs have an antisense overlap with protein coding genes. The open reading frames (ORFs) in these antisense RNAs could also overlap with existing ORFs. In this study, we investigate how the evolution an ORF could be constrained by its overlap with an existing ORF in three different reading frames. Using a combination of mathematical modeling and genome/transcriptome data analysis in two different model organisms, we show that antisense overlap can increase the likelihood of ORF emergence and reduce the likelihood of ORF loss, especially in one of the three reading frames. In addition to rationalising the repeatedly reported prevalence of de novo emerged genes in antisense transcripts, our work also provides a generic modeling and an analytical framework that can be used to understand evolution of antisense genes.
Iyengar, Bharat R.
In search for multifunctional lncRNAs Journal Article Forthcoming
In: Forthcoming.
@article{nokey,
title = {In search for multifunctional lncRNAs},
author = {Bharat R. Iyengar},
url = {https://doi.org/10.1101/2024.07.11.603032},
year = {2024},
date = {2024-07-11},
urldate = {2024-07-11},
abstract = {Long non-coding RNAs (lncRNAs) were so named because at the time of their discovery, no corresponding protein products were known. Despite the lack of evidence for translation, many lncRNAs perform essential cellular functions such as regulation of gene expression. Recent studies show that many lncRNAs, including those with known regulatory functions, bind to ribosomes and are translated, suggesting that RNAs can perform two different kinds of functions (a phenomenon known in proteins, called moonlighting). Using a formal mathematical model, I show that execution of one function limits that of the other. However, an RNA can transition from one function to the other, simply by a spatiotemporal regulation of its interacting partners. I further studied the properties of proteins encoded in functional human lncRNAs and found that many of them have complex sequences, and some of them can even adopt stable 3D structures. These findings may encourage further exploration of moonlighting lncRNAs, their regulation, and their role in the evolution of new protein coding genes.},
keywords = {},
pubstate = {forthcoming},
tppubtype = {article}
}
Long non-coding RNAs (lncRNAs) were so named because at the time of their discovery, no corresponding protein products were known. Despite the lack of evidence for translation, many lncRNAs perform essential cellular functions such as regulation of gene expression. Recent studies show that many lncRNAs, including those with known regulatory functions, bind to ribosomes and are translated, suggesting that RNAs can perform two different kinds of functions (a phenomenon known in proteins, called moonlighting). Using a formal mathematical model, I show that execution of one function limits that of the other. However, an RNA can transition from one function to the other, simply by a spatiotemporal regulation of its interacting partners. I further studied the properties of proteins encoded in functional human lncRNAs and found that many of them have complex sequences, and some of them can even adopt stable 3D structures. These findings may encourage further exploration of moonlighting lncRNAs, their regulation, and their role in the evolution of new protein coding genes.
Lebherz, Marie K.; Fouks, Bertrand; Schmidt, Julian; Bornberg-Bauer, Erich; Grandchamp, Anna
DNA Transposons favour de novo transcript emergence through enrichment of transcription factor binding motifs Journal Article
In: Genome Biology and Evolution, vol. 16, iss. 7, no. evae134, 2024.
@article{nokey,
title = {DNA Transposons favour de novo transcript emergence through enrichment of transcription factor binding motifs},
author = {Marie K. Lebherz and Bertrand Fouks and Julian Schmidt and Erich Bornberg-Bauer and Anna Grandchamp},
url = {https://bornberglab.org/lebherzgrandchamp/},
doi = {https://doi.org/10.1093/gbe/evae134},
year = {2024},
date = {2024-06-27},
urldate = {2024-06-27},
journal = {Genome Biology and Evolution},
volume = {16},
number = {evae134},
issue = {7},
abstract = {De novo genes emerge from noncoding regions of genomes via succession of mutations. Among others, such mutations activate transcription and create a new open reading frame (ORF). Although the mechanisms underlying ORF emergence are well documented, relatively little is known about the mechanisms enabling new transcription events. Yet, in many species a continuum between absent and very prominent transcription has been reported for essentially all regions of the genome. In this study, we searched for de novo transcripts by using newly assembled genomes and transcriptomes of seven inbred lines of Drosophila melanogaster, originating from six European and one African population. This setup allowed us to detect sample specific de novo transcripts, and compare them to their homologous nontranscribed regions in other samples, as well as genic and intergenic control sequences. We studied the association with transposable elements (TEs) and the enrichment of transcription factor motifs upstream of de novo emerged transcripts and compared them with regulatory elements. We found that de novo transcripts overlap with TEs more often than expected by chance. The emergence of new transcripts correlates with regions of high guanine-cytosine content and TE expression. Moreover, upstream regions of de novo transcripts are highly enriched with regulatory motifs. Such motifs are more enriched in new transcripts overlapping with TEs, particularly DNA TEs, and are more conserved upstream de novo transcripts than upstream their ‘nontranscribed homologs’. Overall, our study demonstrates that TE insertion is important for transcript emergence, partly by introducing new regulatory motifs from DNA TE families.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
De novo genes emerge from noncoding regions of genomes via succession of mutations. Among others, such mutations activate transcription and create a new open reading frame (ORF). Although the mechanisms underlying ORF emergence are well documented, relatively little is known about the mechanisms enabling new transcription events. Yet, in many species a continuum between absent and very prominent transcription has been reported for essentially all regions of the genome. In this study, we searched for de novo transcripts by using newly assembled genomes and transcriptomes of seven inbred lines of Drosophila melanogaster, originating from six European and one African population. This setup allowed us to detect sample specific de novo transcripts, and compare them to their homologous nontranscribed regions in other samples, as well as genic and intergenic control sequences. We studied the association with transposable elements (TEs) and the enrichment of transcription factor motifs upstream of de novo emerged transcripts and compared them with regulatory elements. We found that de novo transcripts overlap with TEs more often than expected by chance. The emergence of new transcripts correlates with regions of high guanine-cytosine content and TE expression. Moreover, upstream regions of de novo transcripts are highly enriched with regulatory motifs. Such motifs are more enriched in new transcripts overlapping with TEs, particularly DNA TEs, and are more conserved upstream de novo transcripts than upstream their ‘nontranscribed homologs’. Overall, our study demonstrates that TE insertion is important for transcript emergence, partly by introducing new regulatory motifs from DNA TE families.
Lebherz, Marie K.; Iyengar, Bharat R.; Bornberg-Bauer, Erich
Modeling Length Changes in De Novo Open Reading Frames during Neutral Evolution Journal Article
In: Genome Biology and Evolution, vol. 16, iss. 7, no. evae129, 2024.
@article{nokey,
title = { Modeling Length Changes in \textit{De Novo} Open Reading Frames during Neutral Evolution },
author = {Marie K. Lebherz and Bharat R. Iyengar and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2024/07/LebherzRavi2024-2.pdf},
doi = {https://doi.org/10.1093/gbe/evae129},
year = {2024},
date = {2024-06-16},
urldate = {2024-06-16},
journal = {Genome Biology and Evolution},
volume = {16},
number = {evae129},
issue = {7},
abstract = {For protein coding genes to emerge de novo from a non-genic DNA, the DNA sequence must gain an open reading frame (ORF) and the ability to be transcribed. The newborn de novo gene can further evolve to accumulate changes in its sequence. Consequently, it can also elongate or shrink with time. Existing literature shows that older de novo genes have longer ORF, but it is not clear if they elongated with time or remained of the same length since their inception. To address this question we developed a mathematical model of ORF elongation as a Markov-jump process, and show that ORFs tend to keep their length in short evolutionary timescales. We also show that if change occurs it is likely to be a truncation. Our genomics and transcriptomics data analyses of seven Drosophila melanogaster populations are also in agreement with the model’s prediction. We conclude that selection could facilitate ORF length extension that may explain why longer ORFs were observed in old de novo genes in studies analysing longer evolutionary time scales. Alternatively, shorter ORFs may be purged because they may be less likely to yield functional proteins.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
For protein coding genes to emerge de novo from a non-genic DNA, the DNA sequence must gain an open reading frame (ORF) and the ability to be transcribed. The newborn de novo gene can further evolve to accumulate changes in its sequence. Consequently, it can also elongate or shrink with time. Existing literature shows that older de novo genes have longer ORF, but it is not clear if they elongated with time or remained of the same length since their inception. To address this question we developed a mathematical model of ORF elongation as a Markov-jump process, and show that ORFs tend to keep their length in short evolutionary timescales. We also show that if change occurs it is likely to be a truncation. Our genomics and transcriptomics data analyses of seven Drosophila melanogaster populations are also in agreement with the model’s prediction. We conclude that selection could facilitate ORF length extension that may explain why longer ORFs were observed in old de novo genes in studies analysing longer evolutionary time scales. Alternatively, shorter ORFs may be purged because they may be less likely to yield functional proteins.
Feldmeyer, Barbara; Bornberg-Bauer, Erich; Dohmen, Elias; Fouks, Bertrand; Heckenhauer, Jaqueline; Huylmans, Ann Kathrin; Jones, Alun; Stolle, Eckart; Harrison, Mark C.
Comparative Evolutionary Genomics in Insects Journal Article
In: Methods in Molecular Biology, vol. 2802, pp. 473-514, 2024.
@article{nokey,
title = {Comparative Evolutionary Genomics in Insects},
author = {Barbara Feldmeyer and Erich Bornberg-Bauer and Elias Dohmen and Bertrand Fouks and Jaqueline Heckenhauer and Ann Kathrin Huylmans and Alun Jones and Eckart Stolle and Mark C. Harrison },
doi = {10.1007/978-1-0716-3838-5_16},
year = {2024},
date = {2024-06-01},
urldate = {2024-06-01},
journal = {Methods in Molecular Biology},
volume = {2802},
pages = {473-514},
abstract = {Genome sequencing quality, in terms of both read length and accuracy, is constantly improving. By combining long-read sequencing technologies with various scaffolding techniques, chromosome-level genome assemblies are now achievable at an affordable price for non-model organisms. Insects represent an exciting taxon for studying the genomic underpinnings of evolutionary innovations, due to ancient origins, immense species-richness, and broad phenotypic diversity. Here we summarize some of the most important methods for carrying out a comparative genomics study on insects. We describe available tools and offer concrete tips on all stages of such an endeavor from DNA extraction through genome sequencing, annotation, and several evolutionary analyses. Along the way we describe important insect-specific aspects, such as DNA extraction difficulties or gene families that are particularly difficult to annotate, and offer solutions. We describe results from several examples of comparative genomics analyses on insects to illustrate the fascinating questions that can now be addressed in this new age of genomics research.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Genome sequencing quality, in terms of both read length and accuracy, is constantly improving. By combining long-read sequencing technologies with various scaffolding techniques, chromosome-level genome assemblies are now achievable at an affordable price for non-model organisms. Insects represent an exciting taxon for studying the genomic underpinnings of evolutionary innovations, due to ancient origins, immense species-richness, and broad phenotypic diversity. Here we summarize some of the most important methods for carrying out a comparative genomics study on insects. We describe available tools and offer concrete tips on all stages of such an endeavor from DNA extraction through genome sequencing, annotation, and several evolutionary analyses. Along the way we describe important insect-specific aspects, such as DNA extraction difficulties or gene families that are particularly difficult to annotate, and offer solutions. We describe results from several examples of comparative genomics analyses on insects to illustrate the fascinating questions that can now be addressed in this new age of genomics research.
Makova, Kateryna D.; Pickett, Brandon D.; Harris, Robert S.; Hartley, Gabrielle A.; Cechova, Monika; Pal, Karol; Nurk, Sergey; Yoo, DongAhn; Li, Qiuhui; Hebbar, Prajna; McGrath, Barbara C.; Antonacci, Francesca; Aubel, Margaux; Biddanda, Arjun; Borchers, Matthew; Bornberg-Bauer, Erich; Bouffard, Gerard G.; Brooks, Shelise Y.; Carbone, Lucia; Carrel, Laura; Carroll, Andrew; Chang, Pi-Chuan; Chin, Chen-Shan; Cook, Daniel E.; Craig, Sarah J. C.; de Gennaro, Luciana; Diekhans, Mark; Dutra, Amalia; Garcia, Gage H.; Grady, Patrick G. S.; Green, Richard E.; Haddad, Diana; Hallast, Pille; Harvey, William T.; Hickey, Glenn; Hillis, David A.; Hoyt, Savannah J.; Jeong, Hyeonsoo; Kamali, Kaivan; Pond, Sergei L. Kosakovsky; LaPolice, Troy M.; Lee, Charles; Lewis, Alexandra P.; Loh, Yong-Hwee E.; Masterson, Patrick; McGarvey, Kelly M.; McCoy, Rajiv C.; Medvedev, Paul; Miga, Karen H.; Munson, Katherine M.; Pak, Evgenia; Paten, Benedict; Pinto, Brendan J.; Potapova, Tamara; Rhie, Arang; Rocha, Joana L.; Ryabov, Fedor; Ryder, Oliver A.; Sacco, Samuel; Shafin, Kishwar; Shepelev, Valery A.; Slon, Viviane; Solar, Steven J.; Storer, Jessica M.; Sudmant, Peter H.; Sweetalana,; Sweeten, Alex; Tassia, Michael G.; Thibaud-Nissen, Françoise; Ventura, Mario; Wilson, Melissa A.; Young, Alice C.; Zeng, Huiqing; Zhang, Xinru; Szpiech, Zachary A.; Huber, Christian D.; Gerton, Jennifer L.; Yi, Soojin V.; Schatz, Michael C.; Alexandrov, Ivan A.; Koren, Sergey; O’Neill, Rachel J.; Eichler, Evan E.; Phillippy, Adam M.
The complete sequence and comparative analysis of ape sex chromosomes Journal Article
In: Nature, 2024.
@article{nokey,
title = {The complete sequence and comparative analysis of ape sex chromosomes},
author = {Kateryna D. Makova and Brandon D. Pickett and Robert S. Harris and Gabrielle A. Hartley and Monika Cechova and Karol Pal and Sergey Nurk and DongAhn Yoo and Qiuhui Li and Prajna Hebbar and Barbara C. McGrath and Francesca Antonacci and Margaux Aubel and Arjun Biddanda and Matthew Borchers and Erich Bornberg-Bauer and Gerard G. Bouffard and Shelise Y. Brooks and Lucia Carbone and Laura Carrel and Andrew Carroll and Pi-Chuan Chang and Chen-Shan Chin and Daniel E. Cook and Sarah J. C. Craig and Luciana de Gennaro and Mark Diekhans and Amalia Dutra and Gage H. Garcia and Patrick G. S. Grady and Richard E. Green and Diana Haddad and Pille Hallast and William T. Harvey and Glenn Hickey and David A. Hillis and Savannah J. Hoyt and Hyeonsoo Jeong and Kaivan Kamali and Sergei L. Kosakovsky Pond and Troy M. LaPolice and Charles Lee and Alexandra P. Lewis and Yong-Hwee E. Loh and Patrick Masterson and Kelly M. McGarvey and Rajiv C. McCoy and Paul Medvedev and Karen H. Miga and Katherine M. Munson and Evgenia Pak and Benedict Paten and Brendan J. Pinto and Tamara Potapova and Arang Rhie and Joana L. Rocha and Fedor Ryabov and Oliver A. Ryder and Samuel Sacco and Kishwar Shafin and Valery A. Shepelev and Viviane Slon and Steven J. Solar and Jessica M. Storer and Peter H. Sudmant and Sweetalana and Alex Sweeten and Michael G. Tassia and Françoise Thibaud-Nissen and Mario Ventura and Melissa A. Wilson and Alice C. Young and Huiqing Zeng and Xinru Zhang and Zachary A. Szpiech and Christian D. Huber and Jennifer L. Gerton and Soojin V. Yi and Michael C. Schatz and Ivan A. Alexandrov and Sergey Koren and Rachel J. O’Neill and Evan E. Eichler and Adam M. Phillippy },
url = {https://bornberglab.org/wp-content/uploads/2024/05/Makova2024.pdf},
doi = {10.1038/s41586-024-07473-2},
year = {2024},
date = {2024-05-29},
urldate = {2024-05-29},
journal = {Nature},
abstract = {Apes possess two sex chromosomes—the male-specific Y chromosome and the X chromosome, which is present in both males and females. The Y chromosome is crucial for male reproduction, with deletions being linked to infertility. The X chromosome is vital for reproduction and cognition. Variation in mating patterns and brain function among apes suggests corresponding differences in their sex chromosomes. However, owing to their repetitive nature and incomplete reference assemblies, ape sex chromosomes have been challenging to study. Here, using the methodology developed for the telomere-to-telomere (T2T) human genome, we produced gapless assemblies of the X and Y chromosomes for five great apes (bonobo (Pan paniscus), chimpanzee (Pan troglodytes), western lowland gorilla (Gorilla gorilla gorilla), Bornean orangutan (Pongo pygmaeus) and Sumatran orangutan (Pongo abelii)) and a lesser ape (the siamang gibbon (Symphalangus syndactylus)), and untangled the intricacies of their evolution. Compared with the X chromosomes, the ape Y chromosomes vary greatly in size and have low alignability and high levels of structural rearrangements—owing to the accumulation of lineage-specific ampliconic regions, palindromes, transposable elements and satellites. Many Y chromosome genes expand in multi-copy families and some evolve under purifying selection. Thus, the Y chromosome exhibits dynamic evolution, whereas the X chromosome is more stable. Mapping short-read sequencing data to these assemblies revealed diversity and selection patterns on sex chromosomes of more than 100 individual great apes. These reference assemblies are expected to inform human evolution and conservation genetics of non-human apes, all of which are endangered species.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Apes possess two sex chromosomes—the male-specific Y chromosome and the X chromosome, which is present in both males and females. The Y chromosome is crucial for male reproduction, with deletions being linked to infertility. The X chromosome is vital for reproduction and cognition. Variation in mating patterns and brain function among apes suggests corresponding differences in their sex chromosomes. However, owing to their repetitive nature and incomplete reference assemblies, ape sex chromosomes have been challenging to study. Here, using the methodology developed for the telomere-to-telomere (T2T) human genome, we produced gapless assemblies of the X and Y chromosomes for five great apes (bonobo (Pan paniscus), chimpanzee (Pan troglodytes), western lowland gorilla (Gorilla gorilla gorilla), Bornean orangutan (Pongo pygmaeus) and Sumatran orangutan (Pongo abelii)) and a lesser ape (the siamang gibbon (Symphalangus syndactylus)), and untangled the intricacies of their evolution. Compared with the X chromosomes, the ape Y chromosomes vary greatly in size and have low alignability and high levels of structural rearrangements—owing to the accumulation of lineage-specific ampliconic regions, palindromes, transposable elements and satellites. Many Y chromosome genes expand in multi-copy families and some evolve under purifying selection. Thus, the Y chromosome exhibits dynamic evolution, whereas the X chromosome is more stable. Mapping short-read sequencing data to these assemblies revealed diversity and selection patterns on sex chromosomes of more than 100 individual great apes. These reference assemblies are expected to inform human evolution and conservation genetics of non-human apes, all of which are endangered species.
Mikhailova, Alina; Dohmen, Elias; Harrison, Mark C.
Major changes in domain arrangements are associated with the evolution of termite castes Journal Article
In: Journal of Evolutionary Biology, 2024.
@article{nokey,
title = {Major changes in domain arrangements are associated with the evolution of termite castes},
author = {Alina Mikhailova and Elias Dohmen and Mark C. Harrison},
url = {https://bornberglab.org/wp-content/uploads/2024/06/voae047-1.pdf},
doi = {https://doi.org/10.1093/jeb/voae047},
year = {2024},
date = {2024-04-17},
urldate = {2024-04-17},
journal = {Journal of Evolutionary Biology},
abstract = {Domains as functional protein units and their rearrangements along the phylogeny can shed light on the functional changes of proteomes associated with the evolution of complex traits like eusociality. This complex trait is associated with sterile soldiers and workers, and long-lived, highly fecund reproductives. Unlike in Hymenoptera (ants, bees, and wasps), the evolution of eusociality within Blattodea, where termites evolved from within cockroaches, was accompanied by a reduction in proteome size, raising the question of whether functional novelty was achieved with existing rather than novel proteins. To address this, we investigated the role of domain rearrangements during the evolution of termite eusociality. Analysing domain rearrangements in the proteomes of three solitary cockroaches and five eusocial termites, we inferred more than 5,000 rearrangements over the phylogeny of Blattodea. The 90 novel domain arrangements that emerged at the origin of termites were enriched for several functions related to longevity, such as protein homeostasis, DNA repair, mitochondrial activity, and nutrient sensing. Many domain rearrangements were related to changes in developmental pathways, important for the emergence of novel castes. Along with the elaboration of social complexity, including permanently sterile workers and larger, foraging colonies, we found 110 further domain arrangements with functions related to protein glycosylation and ion transport. We found an enrichment of caste-biased expression and splicing within rearranged genes, highlighting their importance for the evolution of castes. Furthermore, we found increased levels of DNA methylation among rearranged compared to non-rearranged genes suggesting fundamental differences in their regulation. Our findings indicate the importance of domain rearrangements in the generation of functional novelty necessary for termite eusociality to evolve.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Domains as functional protein units and their rearrangements along the phylogeny can shed light on the functional changes of proteomes associated with the evolution of complex traits like eusociality. This complex trait is associated with sterile soldiers and workers, and long-lived, highly fecund reproductives. Unlike in Hymenoptera (ants, bees, and wasps), the evolution of eusociality within Blattodea, where termites evolved from within cockroaches, was accompanied by a reduction in proteome size, raising the question of whether functional novelty was achieved with existing rather than novel proteins. To address this, we investigated the role of domain rearrangements during the evolution of termite eusociality. Analysing domain rearrangements in the proteomes of three solitary cockroaches and five eusocial termites, we inferred more than 5,000 rearrangements over the phylogeny of Blattodea. The 90 novel domain arrangements that emerged at the origin of termites were enriched for several functions related to longevity, such as protein homeostasis, DNA repair, mitochondrial activity, and nutrient sensing. Many domain rearrangements were related to changes in developmental pathways, important for the emergence of novel castes. Along with the elaboration of social complexity, including permanently sterile workers and larger, foraging colonies, we found 110 further domain arrangements with functions related to protein glycosylation and ion transport. We found an enrichment of caste-biased expression and splicing within rearranged genes, highlighting their importance for the evolution of castes. Furthermore, we found increased levels of DNA methylation among rearranged compared to non-rearranged genes suggesting fundamental differences in their regulation. Our findings indicate the importance of domain rearrangements in the generation of functional novelty necessary for termite eusociality to evolve.
Aubel, Margaux; Buchel, Filip; Heames, Brennen; Jones, Alun; Honc, Ondrej; Bornberg-Bauer, Erich; Hlouchova, Klara
High-throughput selection of human de novo-emerged sORFs with high folding potential Journal Article
In: Genome Biology and Evolution, vol. 16, iss. 4, no. evae069, 2024.
@article{Aubel2024,
title = {High-throughput selection of human de novo-emerged sORFs with high folding potential},
author = {Margaux Aubel and Filip Buchel and Brennen Heames and Alun Jones and Ondrej Honc and Erich Bornberg-Bauer and Klara Hlouchova},
url = {https://bornberglab.org/wp-content/uploads/2024/04/GBE_aubel_2024-3.pdf},
doi = { https://doi.org/10.1093/gbe/evae069},
year = {2024},
date = {2024-04-10},
urldate = {2024-04-10},
journal = {Genome Biology and Evolution},
volume = {16},
number = {evae069},
issue = {4},
abstract = {De novo genes emerge from previously non-coding stretches of the genome. Their encoded de novo proteins are generally expected to be similar to random sequences and, accordingly, with no stable tertiary fold and high predicted disorder. However, structural properties of de novo proteins and whether they differ during the stages of emergence and fixation have not been studied in depth and rely heavily on predictions. Here we generated a library of short human putative de novo proteins of varying lengths and ages and sorted the candidates according to their structural compactness and disorder propensity. Using F ̈orster resonance energy transfer (FRET) combined with Fluorescence-activated cell sorting (FACS) we were able to screen the library for most compact protein structures, as well as most elongated and flexible structures. Compact de novo proteins are on average slightly shorter and contain lower predicted disorder than less compact ones. The predicted structures for most and least compact de novo proteins correspond to expectations in that they contain more secondary structure content or higher disorder content, respectively. Our experiments indicate that older de novo proteins have higher compactness and structural propensity compared to young ones. We discuss possible evolutionary scenarios and their implications underlying the age-dependencies of compactness and structural content of putative de novo proteins.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
De novo genes emerge from previously non-coding stretches of the genome. Their encoded de novo proteins are generally expected to be similar to random sequences and, accordingly, with no stable tertiary fold and high predicted disorder. However, structural properties of de novo proteins and whether they differ during the stages of emergence and fixation have not been studied in depth and rely heavily on predictions. Here we generated a library of short human putative de novo proteins of varying lengths and ages and sorted the candidates according to their structural compactness and disorder propensity. Using F ̈orster resonance energy transfer (FRET) combined with Fluorescence-activated cell sorting (FACS) we were able to screen the library for most compact protein structures, as well as most elongated and flexible structures. Compact de novo proteins are on average slightly shorter and contain lower predicted disorder than less compact ones. The predicted structures for most and least compact de novo proteins correspond to expectations in that they contain more secondary structure content or higher disorder content, respectively. Our experiments indicate that older de novo proteins have higher compactness and structural propensity compared to young ones. We discuss possible evolutionary scenarios and their implications underlying the age-dependencies of compactness and structural content of putative de novo proteins.
Brink, Kristiana; Thomas, Christian; W., Chan T.; Jones, Alun; Mallon, Eamonn
Exploring the ageing methylome in the model insect, Nasonia vitripennis Journal Article
In: BMC Genomics volume, vol. 25, no. 305, 2024.
@article{nokey,
title = {Exploring the ageing methylome in the model insect, Nasonia vitripennis},
author = {Kristiana Brink and Christian Thomas and Chan T. W. and Alun Jones and Eamonn Mallon},
url = {https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-024-10211-7},
doi = {https://doi.org/10.1186/s12864-024-10211-7},
year = {2024},
date = {2024-03-22},
urldate = {2024-03-22},
journal = {BMC Genomics volume},
volume = {25},
number = {305},
abstract = {The ageing process is a multifaceted phenomenon marked by the gradual deterioration of cellular and organismal functions, accompanied by an elevated susceptibility to diseases. The intricate interplay between genetic and environmental factors complicates research, particularly in complex mammalian models. In this context, simple invertebrate organisms have been pivotal, but the current models lack detectable DNA methylation limiting the exploration of this critical epigenetic ageing mechanism.
This study introduces Nasonia vitripennis, the jewel wasp, as an innovative invertebrate model for investigating the epigenetics of ageing. Leveraging its advantages as a model organism and possessing a functional DNA methylation system, Nasonia emerges as a valuable addition to ageing research.
Results
Whole-genome bisulfite sequencing unveiled dynamic alterations in DNA methylation, with differentially methylated CpGs between distinct time points in both male and female wasps. These changes were associated with numerous genes, enriching for functions related to telomere maintenance, histone methylation, and mRNA catabolic processes. Additionally, other CpGs were found to be variably methylated at each timepoint. Sex-specific effects on epigenetic entropy were observed, indicating differential patterns in the loss of epigenetic stability over time. Constructing an epigenetic clock containing 19 CpGs revealed a robust correlation between epigenetic age and chronological age.
Conclusions
Nasonia vitripennis emerges as a promising model for investigating the epigenetics of ageing, shedding light on the intricate dynamics of DNA methylation and their implications for age-related processes. This research not only expands the repertoire of ageing models but also opens avenues for deeper exploration of epigenetic mechanisms in the context of ageing.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The ageing process is a multifaceted phenomenon marked by the gradual deterioration of cellular and organismal functions, accompanied by an elevated susceptibility to diseases. The intricate interplay between genetic and environmental factors complicates research, particularly in complex mammalian models. In this context, simple invertebrate organisms have been pivotal, but the current models lack detectable DNA methylation limiting the exploration of this critical epigenetic ageing mechanism.
This study introduces Nasonia vitripennis, the jewel wasp, as an innovative invertebrate model for investigating the epigenetics of ageing. Leveraging its advantages as a model organism and possessing a functional DNA methylation system, Nasonia emerges as a valuable addition to ageing research.
Results
Whole-genome bisulfite sequencing unveiled dynamic alterations in DNA methylation, with differentially methylated CpGs between distinct time points in both male and female wasps. These changes were associated with numerous genes, enriching for functions related to telomere maintenance, histone methylation, and mRNA catabolic processes. Additionally, other CpGs were found to be variably methylated at each timepoint. Sex-specific effects on epigenetic entropy were observed, indicating differential patterns in the loss of epigenetic stability over time. Constructing an epigenetic clock containing 19 CpGs revealed a robust correlation between epigenetic age and chronological age.
Conclusions
Nasonia vitripennis emerges as a promising model for investigating the epigenetics of ageing, shedding light on the intricate dynamics of DNA methylation and their implications for age-related processes. This research not only expands the repertoire of ageing models but also opens avenues for deeper exploration of epigenetic mechanisms in the context of ageing.
This study introduces Nasonia vitripennis, the jewel wasp, as an innovative invertebrate model for investigating the epigenetics of ageing. Leveraging its advantages as a model organism and possessing a functional DNA methylation system, Nasonia emerges as a valuable addition to ageing research.
Results
Whole-genome bisulfite sequencing unveiled dynamic alterations in DNA methylation, with differentially methylated CpGs between distinct time points in both male and female wasps. These changes were associated with numerous genes, enriching for functions related to telomere maintenance, histone methylation, and mRNA catabolic processes. Additionally, other CpGs were found to be variably methylated at each timepoint. Sex-specific effects on epigenetic entropy were observed, indicating differential patterns in the loss of epigenetic stability over time. Constructing an epigenetic clock containing 19 CpGs revealed a robust correlation between epigenetic age and chronological age.
Conclusions
Nasonia vitripennis emerges as a promising model for investigating the epigenetics of ageing, shedding light on the intricate dynamics of DNA methylation and their implications for age-related processes. This research not only expands the repertoire of ageing models but also opens avenues for deeper exploration of epigenetic mechanisms in the context of ageing.
Middendorf, Lasse; Iyengar, Bharat R.; Eicholt, Lars A.
Sequence, Structure and Functional space of Drosophila de novo proteins Journal Article
In: Genome Biology and Evolution, vol. 16, iss. 8, no. evae176, 2024.
@article{nokey,
title = {Sequence, Structure and Functional space of Drosophila de novo proteins},
author = {Lasse Middendorf and Bharat R. Iyengar and Lars A. Eicholt},
url = {https://bornberglab.org/wp-content/uploads/2024/07/Middendorf_Iyengar_Eicholt_revised1_2024.pdf},
doi = {https://doi.org/10.1093/gbe/evae176},
year = {2024},
date = {2024-01-30},
urldate = {2024-01-30},
journal = {Genome Biology and Evolution},
volume = {16},
number = {evae176},
issue = {8},
abstract = {During de novo emergence, new protein coding genes emerge from previously non-genic sequences. The de novo proteins they encode are dissimilar in composition and predicted biochemical properties to conserved proteins. However, many functional de novo proteins indeed exist. Both identification of functional de novo proteins and their structural characterisation are experimentally laborious. To identify functional and structured de novo proteins in silico, we applied recently developed machine learning based tools and refined the results for de novo proteins. We found that most de novo proteins are indeed different from conserved proteins both in their structure and sequence. However, some de novo proteins are predicted to adopt known protein folds, participate in cellular reactions, and to form biomolecular condensates. Apart from broadening our understanding of de novo protein evolution, our study also provides a large set of testable hypotheses for focused experimental studies on structure and function of de novo proteins in Drosophila.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
During de novo emergence, new protein coding genes emerge from previously non-genic sequences. The de novo proteins they encode are dissimilar in composition and predicted biochemical properties to conserved proteins. However, many functional de novo proteins indeed exist. Both identification of functional de novo proteins and their structural characterisation are experimentally laborious. To identify functional and structured de novo proteins in silico, we applied recently developed machine learning based tools and refined the results for de novo proteins. We found that most de novo proteins are indeed different from conserved proteins both in their structure and sequence. However, some de novo proteins are predicted to adopt known protein folds, participate in cellular reactions, and to form biomolecular condensates. Apart from broadening our understanding of de novo protein evolution, our study also provides a large set of testable hypotheses for focused experimental studies on structure and function of de novo proteins in Drosophila.
Middendorf, Lasse; Eicholt, Lars A.
Random, de novo and conserved proteins: How structure and disorder predictors perform differently Journal Article
In: Proteins: Structure, Function and Bioinformatics, iss. 1‐11, 2024.
@article{middendorf2023,
title = {Random, de novo and conserved proteins: How structure and disorder predictors perform differently},
author = {Lasse Middendorf and Lars A. Eicholt},
url = {https://bornberglab.org/wp-content/uploads/2024/01/middendorf_2024.pdf},
doi = {10.1002/prot.26652},
year = {2024},
date = {2024-01-16},
urldate = {2024-01-16},
journal = {Proteins: Structure, Function and Bioinformatics},
issue = {1‐11},
abstract = {Understanding the emergence and structural characteristics of de novo and random proteins is crucial for unraveling protein evolution and designing novel enzymes. However, experimental determination of their structures remains challenging. Recent advancements in protein structure prediction, particularly with AlphaFold2 (AF2), have expanded our knowledge of protein structures, but their applicability to de novo and random proteins is unclear. In this study, we investigate the structural predictions and confidence scores of AF2 and protein language model (pLM)-based predictor ESMFold for de novo, random, and conserved proteins. We find that the structural predictions for de novo and random proteins differ significantly from conserved proteins. Interestingly, a positive correlation between disorder and confidence scores (pLDDT) is observed for de novo and random proteins, in contrast to the negative correlation observed for conserved proteins. Furthermore, the performance of structure predictors for de novo and random proteins is hampered by the lack of sequence identity. We also observe varying predicted disorder among different sequence length quartiles for random proteins, suggesting an influence of sequence length on disorder predictions. In conclusion, while structure predictors provide initial insights into the structural composition of de novo and random proteins, their accuracy and applicability to such proteins remain limited. Experimental determination of their structures is necessary for a comprehensive understanding. The positive correlation between disorder and pLDDT could imply a potential for conditional folding and transient binding interactions of de novo and random proteins.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Understanding the emergence and structural characteristics of de novo and random proteins is crucial for unraveling protein evolution and designing novel enzymes. However, experimental determination of their structures remains challenging. Recent advancements in protein structure prediction, particularly with AlphaFold2 (AF2), have expanded our knowledge of protein structures, but their applicability to de novo and random proteins is unclear. In this study, we investigate the structural predictions and confidence scores of AF2 and protein language model (pLM)-based predictor ESMFold for de novo, random, and conserved proteins. We find that the structural predictions for de novo and random proteins differ significantly from conserved proteins. Interestingly, a positive correlation between disorder and confidence scores (pLDDT) is observed for de novo and random proteins, in contrast to the negative correlation observed for conserved proteins. Furthermore, the performance of structure predictors for de novo and random proteins is hampered by the lack of sequence identity. We also observe varying predicted disorder among different sequence length quartiles for random proteins, suggesting an influence of sequence length on disorder predictions. In conclusion, while structure predictors provide initial insights into the structural composition of de novo and random proteins, their accuracy and applicability to such proteins remain limited. Experimental determination of their structures is necessary for a comprehensive understanding. The positive correlation between disorder and pLDDT could imply a potential for conditional folding and transient binding interactions of de novo and random proteins.
Grandchamp, Anna; Czuppon, Peter; Bornberg-Bauer, Erich
Quantification and modeling of turnover dynamics of de novo transcripts in Drosophila melanogaster Journal Article
In: Nucleic Acids Research, vol. 52, iss. 1, pp. 274–287, 2024.
@article{nokey,
title = {Quantification and modeling of turnover dynamics of de novo transcripts in Drosophila melanogaster},
author = {Anna Grandchamp and Peter Czuppon and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2024/01/grandchamp_czuppon-2.pdf},
doi = {https://doi.org/10.1101/2023.02.13.528330},
year = {2024},
date = {2024-01-01},
urldate = {2024-01-01},
journal = {Nucleic Acids Research},
volume = {52},
issue = {1},
pages = {274–287},
abstract = {Most of the transcribed genome in eukaryotes does not code for proteins but produces non-genic transcripts. Among these non-genic transcripts, some are newly transcribed when compared to an evolutionary close outgroup, and are referred to as de novo transcript. Despite their creative role for genomic innovations as potential predecessors of de novo genes, little is known about the rates at which de novo transcripts emerge and disappear. Such a rate estimation requires a precise comparison of the absence and presence of de novo transcripts between phylogenetically close samples, and a mathematical model based on evolutionary processes. To detect newly emerged transcripts on short evolutionary distances, we use DNA long reads and RNA short reads from lines derived from seven populations of Drosophila melanogaster. Transcripts from the seven lines were distributed in orthogroups according to three newly proposed definitions. Overall, each line contains between 2,708 and 3,116 de novo transcripts with most of them being specific to a single line. Depending on the definition of transcript orthogroups, we estimate that between 0.13 and 0.34 transcripts are gained per year and that a transcript is lost at a rate between 6.6. × 10−5 and 2 × 10−4 per year. This suggests frequent exploration of new genomic sequences mediated through a high turnover of transcripts. Our study therefore provides novel insight on non-genic transcript dynamics on a very short evolutionary time-scale with implications for the process of de novo gene birth.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Most of the transcribed genome in eukaryotes does not code for proteins but produces non-genic transcripts. Among these non-genic transcripts, some are newly transcribed when compared to an evolutionary close outgroup, and are referred to as de novo transcript. Despite their creative role for genomic innovations as potential predecessors of de novo genes, little is known about the rates at which de novo transcripts emerge and disappear. Such a rate estimation requires a precise comparison of the absence and presence of de novo transcripts between phylogenetically close samples, and a mathematical model based on evolutionary processes. To detect newly emerged transcripts on short evolutionary distances, we use DNA long reads and RNA short reads from lines derived from seven populations of Drosophila melanogaster. Transcripts from the seven lines were distributed in orthogroups according to three newly proposed definitions. Overall, each line contains between 2,708 and 3,116 de novo transcripts with most of them being specific to a single line. Depending on the definition of transcript orthogroups, we estimate that between 0.13 and 0.34 transcripts are gained per year and that a transcript is lost at a rate between 6.6. × 10−5 and 2 × 10−4 per year. This suggests frequent exploration of new genomic sequences mediated through a high turnover of transcripts. Our study therefore provides novel insight on non-genic transcript dynamics on a very short evolutionary time-scale with implications for the process of de novo gene birth.
2023
Mikhailova, Alina; Rinke, Sarah; Harrison, Mark C.
Genomic signatures of eusocial evolution in insects. Journal Article
In: Current Opinion in Insect Science, 2023.
@article{MC2023,
title = {Genomic signatures of eusocial evolution in insects.},
author = {Alina Mikhailova and Sarah Rinke and Mark C. Harrison},
editor = {Kang Le},
url = {https://bornberglab.org/wp-content/uploads/2023/11/Mikhailova_Rinke_COIS_2023.pdf},
doi = {10.1016/j.cois.2023.101136},
year = {2023},
date = {2023-11-03},
urldate = {2023-11-03},
journal = {Current Opinion in Insect Science},
abstract = {The genomes of eusocial insects allow the production and regulation of highly distinct phenotypes, largely independent of genotype. Although rare, eusociality has evolved convergently in at least three insect orders (Hymenoptera, Blattodea and Coleoptera). Despite such disparate origins, eusocial phenotypes show remarkable similarity, exhibiting long-lived reproductives and short-lived sterile workers and soldiers. In this article, we review current knowledge on genomic signatures of eusocial evolution. We confirm that especially an increased regulatory complexity and the adaptive evolution of chemical communication are common to several origins of eusociality. Furthermore, colony life itself can shape genomes of divergent taxa in a similar manner. Future research should be geared towards generating more high-quality genomic resources, especially in hitherto understudied clades, such as ambrosia beetles and termites. The application of more sophisticated tools such as machine learning techniques may allow the detection of more subtle convergent genomic footprints of eusociality.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The genomes of eusocial insects allow the production and regulation of highly distinct phenotypes, largely independent of genotype. Although rare, eusociality has evolved convergently in at least three insect orders (Hymenoptera, Blattodea and Coleoptera). Despite such disparate origins, eusocial phenotypes show remarkable similarity, exhibiting long-lived reproductives and short-lived sterile workers and soldiers. In this article, we review current knowledge on genomic signatures of eusocial evolution. We confirm that especially an increased regulatory complexity and the adaptive evolution of chemical communication are common to several origins of eusociality. Furthermore, colony life itself can shape genomes of divergent taxa in a similar manner. Future research should be geared towards generating more high-quality genomic resources, especially in hitherto understudied clades, such as ambrosia beetles and termites. The application of more sophisticated tools such as machine learning techniques may allow the detection of more subtle convergent genomic footprints of eusociality.
Fouks, Bertrand; Harrison, Mark C.; Mikhailova, Alina A.; Marchal, Elisabeth; English, Sinead; Carruthers, Madeleine; Jennings, Emily C.; Chiamaka, Ezemuoka L.; Frigard, Ronja A.; Pippel, Martin; Attardo, Geoffrey M.; Benoit, Joshua B.; Bornberg-Bauer, Erich; Tobe, Stephen S.
Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond Journal Article
In: iScience, vol. 26, iss. 10, 2023.
@article{nokey,
title = {Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond},
author = {Bertrand Fouks and Mark C. Harrison and Alina A. Mikhailova and Elisabeth Marchal and Sinead English and Madeleine Carruthers and Emily C. Jennings and Ezemuoka L. Chiamaka and Ronja A. Frigard and Martin Pippel and Geoffrey M. Attardo and Joshua B. Benoit and Erich Bornberg-Bauer and Stephen S. Tobe},
doi = {https://doi.org/10.1016/j.isci.2023.107832},
year = {2023},
date = {2023-09-09},
urldate = {2023-09-09},
journal = { iScience},
volume = {26},
issue = {10},
abstract = {Live birth (viviparity) has arisen repeatedly and independently among animals. We sequenced the genome and transcriptome of the viviparous Pacific beetle-mimic cockroach and performed comparative analyses with two other viviparous insect lineages, tsetse flies and aphids, to unravel the basis underlying the transition to viviparity in insects. We identified pathways undergoing adaptive evolution for insects, involved in urogenital remodeling, tracheal system, heart development, and nutrient metabolism. Transcriptomic analysis of cockroach and tsetse flies revealed that uterine remodeling and nutrient production are increased and the immune response is altered during pregnancy, facilitating structural and physiological changes to accommodate and nourish the progeny. These patterns of convergent evolution of viviparity among insects, together with similar adaptive mechanisms identified among vertebrates, highlight that the transition to viviparity requires changes in urogenital remodeling, enhanced tracheal and heart development (corresponding to angiogenesis in vertebrates), altered nutrient metabolism, and shifted immunity in animal systems.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Live birth (viviparity) has arisen repeatedly and independently among animals. We sequenced the genome and transcriptome of the viviparous Pacific beetle-mimic cockroach and performed comparative analyses with two other viviparous insect lineages, tsetse flies and aphids, to unravel the basis underlying the transition to viviparity in insects. We identified pathways undergoing adaptive evolution for insects, involved in urogenital remodeling, tracheal system, heart development, and nutrient metabolism. Transcriptomic analysis of cockroach and tsetse flies revealed that uterine remodeling and nutrient production are increased and the immune response is altered during pregnancy, facilitating structural and physiological changes to accommodate and nourish the progeny. These patterns of convergent evolution of viviparity among insects, together with similar adaptive mechanisms identified among vertebrates, highlight that the transition to viviparity requires changes in urogenital remodeling, enhanced tracheal and heart development (corresponding to angiogenesis in vertebrates), altered nutrient metabolism, and shifted immunity in animal systems.
Thorburn, Doko-Miles J.; Sagonas, Kostas; Binzer-Panchal, Mahesh; Chain, Frédéric J. J.; Feulner, Philine G. D.; Bornberg-Bauer, Erich; Reusch, Thorsten BH; Samonte-Padilla, Irene E.; Milinski, Manfred; Lenz, Tobias L.; Eizaguirre, Christophe
Origin matters: Using a local reference genome improves measures in population genomics Journal Article
In: Molecular Ecology Resources, 2023.
@article{Thorburn2021,
title = {Origin matters: Using a local reference genome improves measures in population genomics},
author = {Doko-Miles J. Thorburn and Kostas Sagonas and Mahesh Binzer-Panchal and Frédéric J. J. Chain and Philine G. D. Feulner and Erich Bornberg-Bauer and Thorsten BH Reusch and Irene E. Samonte-Padilla and Manfred Milinski and Tobias L. Lenz and Christophe Eizaguirre},
url = {https://bornberglab.org/wp-content/uploads/2024/01/Thorburn2023.pdf},
doi = { https://doi.org/10.1111/1755-0998.13838},
year = {2023},
date = {2023-07-25},
urldate = {2023-07-25},
journal = {Molecular Ecology Resources},
abstract = {Balancing selection describes evolutionary processes that maintain genetic diversity. Despite pioneering genome scans, the number of impacted genes and underlying biological functions remain elusive. Using high-quality genome sequence data of 60 three-spined sticklebacks ( Gasterosteus aculeatus ) from five geographically distinct and recently diverged lake-river population pairs, we performed genome-wide scans across two levels of organization: parapatric population-pairs and populations. We overlapped Tajima’s D and Watterson’s estimator metrics and verified signals with additional summary statistics (NCD and π). We also evaluated alternative explanations such as the impact of neutral evolution, population structure, associated overdominance, or the effects of dramatic change in demography. We identified candidate windows exhibiting signals of balancing selection spanning 2.31% (population-pair) and 3.10% (population) of the autosomes. These candidate windows had extended linkage disequilibrium and were predominantly enriched in intergenic and nonsynonymous SNPs. We identified 715 (population-pair) and 1,010 (population) candidate genes under balancing selection, representing 3.44% and 4.85% of G. aculeatus coding genes. Importantly, using conservative thresholds, we found that a minor proportion of candidate genes overlapped with highly differentiated ( F ST ) genomic regions or regions of potential associated overdominance. We further found little evidence of confounding effects originating from dramatic demographic change. Overall, candidate genes under balancing selection were associated with functions directly related to an individual’s interaction with its environment such as olfaction and receptor signalling pathways. Our results demonstrate that selection that maintains standing genetic variation is common and evolves in response to local environmental pressures, playing an important role in adaptation to heterogeneous environments.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Balancing selection describes evolutionary processes that maintain genetic diversity. Despite pioneering genome scans, the number of impacted genes and underlying biological functions remain elusive. Using high-quality genome sequence data of 60 three-spined sticklebacks ( Gasterosteus aculeatus ) from five geographically distinct and recently diverged lake-river population pairs, we performed genome-wide scans across two levels of organization: parapatric population-pairs and populations. We overlapped Tajima’s D and Watterson’s estimator metrics and verified signals with additional summary statistics (NCD and π). We also evaluated alternative explanations such as the impact of neutral evolution, population structure, associated overdominance, or the effects of dramatic change in demography. We identified candidate windows exhibiting signals of balancing selection spanning 2.31% (population-pair) and 3.10% (population) of the autosomes. These candidate windows had extended linkage disequilibrium and were predominantly enriched in intergenic and nonsynonymous SNPs. We identified 715 (population-pair) and 1,010 (population) candidate genes under balancing selection, representing 3.44% and 4.85% of G. aculeatus coding genes. Importantly, using conservative thresholds, we found that a minor proportion of candidate genes overlapped with highly differentiated ( F ST ) genomic regions or regions of potential associated overdominance. We further found little evidence of confounding effects originating from dramatic demographic change. Overall, candidate genes under balancing selection were associated with functions directly related to an individual’s interaction with its environment such as olfaction and receptor signalling pathways. Our results demonstrate that selection that maintains standing genetic variation is common and evolves in response to local environmental pressures, playing an important role in adaptation to heterogeneous environments.
Grandchamp, Anna; Kühl, Lucas; Lebherz, Marie K.; Brüggemann, Kathrin; Parsch, John; Bornberg-Bauer, Erich
Population genomics reveals mechanisms and dynamics of de novo expressed open reading frame emergence in Drosophila melanogaster Journal Article
In: Genome Research, 2023.
@article{nokey,
title = {Population genomics reveals mechanisms and dynamics of de novo expressed open reading frame emergence in Drosophila melanogaster},
author = {Anna Grandchamp and Lucas Kühl and Marie K. Lebherz and Kathrin Brüggemann and John Parsch and Erich Bornberg-Bauer
},
url = {https://bornberglab.org/wp-content/uploads/2024/01/Grandchamp2023.pdf},
doi = {10.1101/gr.277482.122},
year = {2023},
date = {2023-07-23},
urldate = {2023-07-23},
journal = {Genome Research},
abstract = {Novel genes are essential for evolutionary innovations and differ substantially even between closely related species. Recently, multiple studies across many taxa showed that some novel genes arise de novo, that is, from previously noncoding DNA. To characterize the underlying mutations that allowed de novo gene emergence and their order of occurrence, homologous regions must be detected within noncoding sequences in closely related sister genomes. So far, most studies do not detect noncoding homologs of de novo genes because of incomplete assemblies and annotations, and long evolutionary distances separating genomes. Here, we overcome these issues by searching for de novo expressed open reading frames (neORFs), the not-yet fixed precursors of de novo genes that emerged within a single species. We sequenced and assembled genomes with long-read technology and the corresponding transcriptomes from inbred lines of Drosophila melanogaster, derived from seven geographically diverse populations. We found line-specific neORFs in abundance but few neORFs shared by lines, suggesting a rapid turnover. Gain and loss of transcription is more frequent than the creation of ORFs, for example, by forming new start and stop codons. Consequently, the gain of ORFs becomes rate limiting and is frequently the initial step in neORFs emergence. Furthermore, transposable elements (TEs) are major drivers for intragenomic duplications of neORFs, yet TE insertions are less important for the emergence of neORFs. However, highly mutable genomic regions around TEs provide new features that enable gene birth. In conclusion, neORFs have a high birth-death rate, are rapidly purged, but surviving neORFs spread neutrally through populations and within genomes. },
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Novel genes are essential for evolutionary innovations and differ substantially even between closely related species. Recently, multiple studies across many taxa showed that some novel genes arise de novo, that is, from previously noncoding DNA. To characterize the underlying mutations that allowed de novo gene emergence and their order of occurrence, homologous regions must be detected within noncoding sequences in closely related sister genomes. So far, most studies do not detect noncoding homologs of de novo genes because of incomplete assemblies and annotations, and long evolutionary distances separating genomes. Here, we overcome these issues by searching for de novo expressed open reading frames (neORFs), the not-yet fixed precursors of de novo genes that emerged within a single species. We sequenced and assembled genomes with long-read technology and the corresponding transcriptomes from inbred lines of Drosophila melanogaster, derived from seven geographically diverse populations. We found line-specific neORFs in abundance but few neORFs shared by lines, suggesting a rapid turnover. Gain and loss of transcription is more frequent than the creation of ORFs, for example, by forming new start and stop codons. Consequently, the gain of ORFs becomes rate limiting and is frequently the initial step in neORFs emergence. Furthermore, transposable elements (TEs) are major drivers for intragenomic duplications of neORFs, yet TE insertions are less important for the emergence of neORFs. However, highly mutable genomic regions around TEs provide new features that enable gene birth. In conclusion, neORFs have a high birth-death rate, are rapidly purged, but surviving neORFs spread neutrally through populations and within genomes.
Heames, Brennen; Buchel, Filip; Aubel, Margaux; Tretyachenko, Vyacheslav; Loginov, Dmitry; Novák, Petr; Lange, Andreas; Bornberg-Bauer, Erich; Hlouchová, Klára
Experimental characterization of de novo proteins and their unevolved random-sequence counterparts Journal Article
In: Nature Ecology and Evolution, 2023.
@article{heames2023b,
title = {Experimental characterization of de novo proteins and their unevolved random-sequence counterparts},
author = {Brennen Heames and Filip Buchel and Margaux Aubel and Vyacheslav Tretyachenko and Dmitry Loginov and Petr Novák and Andreas Lange and Erich Bornberg-Bauer and Klára Hlouchová},
url = {https://bornberglab.org/wp-content/uploads/2023/04/Heames2023.pdf},
doi = {https://doi.org/10.1038/s41559-023-02010-2},
year = {2023},
date = {2023-04-06},
journal = {Nature Ecology and Evolution},
abstract = {De novo gene emergence provides a route for new proteins to be formed from previously non-coding DNA. Proteins born in this way are considered random sequences and typically assumed to lack defined structure. While it remains unclear how likely a de novo protein is to assume a soluble and stable tertiary structure, intersecting evidence from random sequence and de novo-designed proteins suggests that native-like biophysical properties are abundant in sequence space. Taking putative de novo proteins identified in human and fly, we experimentally characterize a library of these sequences to assess their solubility and structure propensity. We compare this library to a set of synthetic random proteins with no evolutionary history. Bioinformatic prediction suggests that de novo proteins may have remarkably similar distributions of biophysical properties to unevolved random sequences of a given length and amino acid composition. However, upon expression in vitro, de novo proteins exhibit moderately higher solubility which is further induced by the DnaK chaperone system. We suggest that while synthetic random sequences are a useful proxy for de novo proteins in terms of structure propensity, de novo proteins may be better integrated in the cellular system than random expectation, given their higher solubility.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
De novo gene emergence provides a route for new proteins to be formed from previously non-coding DNA. Proteins born in this way are considered random sequences and typically assumed to lack defined structure. While it remains unclear how likely a de novo protein is to assume a soluble and stable tertiary structure, intersecting evidence from random sequence and de novo-designed proteins suggests that native-like biophysical properties are abundant in sequence space. Taking putative de novo proteins identified in human and fly, we experimentally characterize a library of these sequences to assess their solubility and structure propensity. We compare this library to a set of synthetic random proteins with no evolutionary history. Bioinformatic prediction suggests that de novo proteins may have remarkably similar distributions of biophysical properties to unevolved random sequences of a given length and amino acid composition. However, upon expression in vitro, de novo proteins exhibit moderately higher solubility which is further induced by the DnaK chaperone system. We suggest that while synthetic random sequences are a useful proxy for de novo proteins in terms of structure propensity, de novo proteins may be better integrated in the cellular system than random expectation, given their higher solubility.
Iyengar, Bharat R.; Bornberg-Bauer, Erich
Neutral models of de novo gene emergence suggest that gene evolution has a preferred trajectory Journal Article
In: Molecular Biology and Evolution, vol. 40, iss. 4, no. msad079, 2023.
@article{Ravi2023,
title = {Neutral models of de novo gene emergence suggest that gene evolution has a preferred trajectory},
author = {Bharat R. Iyengar and Erich Bornberg-Bauer},
url = {https://doi.org/10.1093/molbev/msad079},
year = {2023},
date = {2023-04-03},
urldate = {2023-04-03},
journal = {Molecular Biology and Evolution},
volume = {40},
number = {msad079},
issue = {4},
abstract = {New protein coding genes can emerge from genomic regions that previously did not contain any genes, via a process called de novo gene emergence. To synthesize a protein, DNA must be transcribed as well as translated. Both processes need certain DNA sequence features. Stable transcription requires promoters and a polyadenylation signal, while translation requires at least an open reading frame. We develop mathematical models based on mutation probabilities, and the assumption of neutral evolution, to find out how quickly genes emerge and are lost. We also investigate the effect of the order by which DNA features evolve, and if sequence composition is biased by mutation rate. We rationalize how genes are lost much more rapidly than they emerge, and how they preferentially arise in regions that are already transcribed. Our study not only answers some fundamental questions on the topic of de novo emergence but also provides a modeling framework for future studies.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
New protein coding genes can emerge from genomic regions that previously did not contain any genes, via a process called de novo gene emergence. To synthesize a protein, DNA must be transcribed as well as translated. Both processes need certain DNA sequence features. Stable transcription requires promoters and a polyadenylation signal, while translation requires at least an open reading frame. We develop mathematical models based on mutation probabilities, and the assumption of neutral evolution, to find out how quickly genes emerge and are lost. We also investigate the effect of the order by which DNA features evolve, and if sequence composition is biased by mutation rate. We rationalize how genes are lost much more rapidly than they emerge, and how they preferentially arise in regions that are already transcribed. Our study not only answers some fundamental questions on the topic of de novo emergence but also provides a modeling framework for future studies.
Aubel, Margaux; Eicholt, Lars A.; Bornberg-Bauer, Erich
Assessing structure and disorder prediction tools for de novo emerged proteins in the age of machine learning Journal Article
In: F1000 Research, 2023.
@article{nokey,
title = {Assessing structure and disorder prediction tools for de novo emerged proteins in the age of machine learning },
author = {Margaux Aubel and Lars A. Eicholt and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2023/07/AubelF2023-2.pdf},
doi = {https://doi.org/10.12688/f1000research.130443.1},
year = {2023},
date = {2023-03-29},
urldate = {2023-03-29},
journal = {F1000 Research},
abstract = {Background: De novo protein coding genes emerge from scratch in the non-coding regions of the genome and have, per definition, no homology to other genes. Therefore, their encoded de novo proteins belong to the so-called "dark protein space". So far, only four de novo protein structures have been experimentally approximated. Low homology, presumed high disorder and limited structures result in low confidence structural predictions for de novo proteins in most cases. Here, we look at the most widely used structure and disorder predictors and assess their applicability for de novo emerged proteins. Since AlphaFold2 is based on the generation of multiple sequence alignments and was trained on solved structures of largely conserved and globular proteins, its performance on de novo proteins remains unknown. More recently, natural language models of proteins have been used for alignment-free structure predictions, potentially making them more suitable for de novo proteins than AlphaFold2.
Methods: We applied different disorder predictors (IUPred3 short/long, flDPnn) and structure predictors, AlphaFold2 on the one hand and language-based models (Omegafold, ESMfold, RGN2) on the other hand, to four de novo proteins with experimental evidence on structure. We compared the resulting predictions between the different predictors as well as to the existing experimental evidence.
Results: Results from IUPred, the most widely used disorder predictor, depend heavily on the choice of parameters and differ significantly from flDPnn which has been found to outperform most other predictors in a comparative assessment study recently. Similarly, different structure predictors yielded varying results and confidence scores for de novo proteins.
Conclusions: We suggest that, while in some cases protein language model based approaches might be more accurate than AlphaFold2, the structure prediction of de novo emerged proteins remains a difficult task for any predictor, be it disorder or structure.
},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background: De novo protein coding genes emerge from scratch in the non-coding regions of the genome and have, per definition, no homology to other genes. Therefore, their encoded de novo proteins belong to the so-called "dark protein space". So far, only four de novo protein structures have been experimentally approximated. Low homology, presumed high disorder and limited structures result in low confidence structural predictions for de novo proteins in most cases. Here, we look at the most widely used structure and disorder predictors and assess their applicability for de novo emerged proteins. Since AlphaFold2 is based on the generation of multiple sequence alignments and was trained on solved structures of largely conserved and globular proteins, its performance on de novo proteins remains unknown. More recently, natural language models of proteins have been used for alignment-free structure predictions, potentially making them more suitable for de novo proteins than AlphaFold2.
Methods: We applied different disorder predictors (IUPred3 short/long, flDPnn) and structure predictors, AlphaFold2 on the one hand and language-based models (Omegafold, ESMfold, RGN2) on the other hand, to four de novo proteins with experimental evidence on structure. We compared the resulting predictions between the different predictors as well as to the existing experimental evidence.
Results: Results from IUPred, the most widely used disorder predictor, depend heavily on the choice of parameters and differ significantly from flDPnn which has been found to outperform most other predictors in a comparative assessment study recently. Similarly, different structure predictors yielded varying results and confidence scores for de novo proteins.
Conclusions: We suggest that, while in some cases protein language model based approaches might be more accurate than AlphaFold2, the structure prediction of de novo emerged proteins remains a difficult task for any predictor, be it disorder or structure.
Methods: We applied different disorder predictors (IUPred3 short/long, flDPnn) and structure predictors, AlphaFold2 on the one hand and language-based models (Omegafold, ESMfold, RGN2) on the other hand, to four de novo proteins with experimental evidence on structure. We compared the resulting predictions between the different predictors as well as to the existing experimental evidence.
Results: Results from IUPred, the most widely used disorder predictor, depend heavily on the choice of parameters and differ significantly from flDPnn which has been found to outperform most other predictors in a comparative assessment study recently. Similarly, different structure predictors yielded varying results and confidence scores for de novo proteins.
Conclusions: We suggest that, while in some cases protein language model based approaches might be more accurate than AlphaFold2, the structure prediction of de novo emerged proteins remains a difficult task for any predictor, be it disorder or structure.
Aubel, Margaux; Bornberg-Bauer, Erich
Introducing ’Creative Destruction’ as a Mechanism in Protein Evolution Journal Article
In: Proceedings of the National Academy of Sciences , vol. 120, no. 6, 2023.
@article{Aubel2023,
title = {Introducing ’Creative Destruction’ as a Mechanism in Protein Evolution},
author = {Margaux Aubel and Erich Bornberg-Bauer},
editor = {Josiah Armour},
url = {https://bornberglab.org/wp-content/uploads/2023/02/Aubelm2023.pdf},
doi = {https://doi.org/10.1073/pnas.2220460120},
year = {2023},
date = {2023-02-02},
urldate = {2023-02-02},
journal = {Proceedings of the National Academy of Sciences },
volume = {120},
number = {6},
type = {Commentary},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Thorburn, Doko-Miles J.; Sagonas, Kostas; Lenz, Tobias L.; Chain, Frédéric J. J.; Feulner, Philine G. D.; Bornberg-Bauer, Erich; Reusch, Thorsten BH; Milinski, Manfred; Eizaguirre, Christophe
Systematic genome scans reveal common population-specific signals of balancing selection Journal Article Forthcoming
In: Forthcoming.
@article{nokey,
title = {Systematic genome scans reveal common population-specific signals of balancing selection},
author = {Doko-Miles J. Thorburn and Kostas Sagonas and Tobias L. Lenz and Frédéric J. J. Chain and Philine G. D. Feulner and Erich Bornberg-Bauer and Thorsten BH Reusch and Manfred Milinski and Christophe Eizaguirre},
year = {2023},
date = {2023-01-09},
urldate = {2023-01-09},
keywords = {},
pubstate = {forthcoming},
tppubtype = {article}
}
2022
Post, Frederik; Bornberg-Bauer, Erich; Vasseur-Cognet, Mireille; Harrison, Mark C.
More effective transposon regulation in fertile, long-lived termite queens than in sterile workers Journal Article
In: Molecular Ecology, 2022.
@article{Post2022,
title = {More effective transposon regulation in fertile, long-lived termite queens than in sterile workers},
author = {Frederik Post and Erich Bornberg-Bauer and Mireille Vasseur-Cognet and Mark C. Harrison},
url = {https://bornberglab.org/wp-content/uploads/2022/11/Post22.pdf},
doi = {https://doi.org/10.1111/mec.16753},
year = {2022},
date = {2022-11-01},
urldate = {2022-11-01},
journal = {Molecular Ecology},
abstract = {Transposable elements (TEs) are mobile genetic sequences, which can cause the accumulation of genomic damage in the life time of an organism. The regulation of TEs, for instance via the piRNA-pathway, is an important mechanism to protect the integrity of genomes, especially in the germ-line where mutations can be transmitted to offspring. In eusocial insects soma and germ-line are divided among worker and reproductive castes, so one may expect caste-specific differences in TE regulation to exist. To test this, we compared whole-genome levels of repeat element transcription in the fat body of female workers, kings, and five different queen stages of the higher termite, Macrotermes natalensis. In this species, queens can live over 20 years, maintaining near maximum reproductive output, while sterile workers only live weeks. We found a strong, positive correlation between TE expression and the expression of neighbouring genes in all castes. However, we found substantially higher TE activity in workers than in reproductives. Furthermore, TE expression did not increase with age in queens, despite a seven-fold increase in gene expression, due to a significant upregulation of the piRNA-pathway in 20-year-old queens. Our results suggest a caste- and age-specific regulation of the piRNA-pathway has evolved in higher termites that is analogous to germ-line-specific activity in individual organisms. In the fat body of these termite queens, an important metabolic tissue for maintaining their extreme longevity and reproductive output, an efficient regulation of TEs likely protects genome integrity, thus further promoting reproductive fitness even at high age.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Transposable elements (TEs) are mobile genetic sequences, which can cause the accumulation of genomic damage in the life time of an organism. The regulation of TEs, for instance via the piRNA-pathway, is an important mechanism to protect the integrity of genomes, especially in the germ-line where mutations can be transmitted to offspring. In eusocial insects soma and germ-line are divided among worker and reproductive castes, so one may expect caste-specific differences in TE regulation to exist. To test this, we compared whole-genome levels of repeat element transcription in the fat body of female workers, kings, and five different queen stages of the higher termite, Macrotermes natalensis. In this species, queens can live over 20 years, maintaining near maximum reproductive output, while sterile workers only live weeks. We found a strong, positive correlation between TE expression and the expression of neighbouring genes in all castes. However, we found substantially higher TE activity in workers than in reproductives. Furthermore, TE expression did not increase with age in queens, despite a seven-fold increase in gene expression, due to a significant upregulation of the piRNA-pathway in 20-year-old queens. Our results suggest a caste- and age-specific regulation of the piRNA-pathway has evolved in higher termites that is analogous to germ-line-specific activity in individual organisms. In the fat body of these termite queens, an important metabolic tissue for maintaining their extreme longevity and reproductive output, an efficient regulation of TEs likely protects genome integrity, thus further promoting reproductive fitness even at high age.
Berger, Juliette; Legendre, Frédéric; Zelosko, Kevin-Markus; Harrison, Mark C.; Grandcolas, Philippe; Bornberg-Bauer, Erich; Fouks, Bertrand
Eusocial Transition in Blattodea: Transposable Elements and Shifts of Gene Expression Journal Article
In: Genes, 2022.
@article{nokey,
title = {Eusocial Transition in Blattodea: Transposable Elements and Shifts of Gene Expression},
author = {Juliette Berger and Frédéric Legendre and Kevin-Markus Zelosko and Mark C. Harrison and Philippe Grandcolas and Erich Bornberg-Bauer and Bertrand Fouks},
url = {https://bornberglab.org/wp-content/uploads/2022/11/Berger22.pdf},
doi = {https://doi.org/10.3390/genes13111948},
year = {2022},
date = {2022-10-26},
urldate = {2022-10-26},
journal = {Genes},
abstract = {1. Unravelling the molecular basis underlying major evolutionary transitions can shed light on how complex phenotypes arise. The evolution of eusociality, a major evolutionary transition, has been demonstrated to be accompanied by enhanced gene regulation. Numerous pieces of evidence suggest the major impact of transposon insertion on gene regulation and its role in adaptive evolution. Transposons have been shown to be play a role in gene duplication involved in the eusocial transition in termites. However, evidence of the molecular basis underlying the eusocial transition in Blattodea remains scarce. Could transposons have facilitated the eusocial transition in termites through shifts of gene expression? 2. Using available cockroach and termite genomes and transcriptomes, we investigated if transposons insert more frequently in genes with differential expression in queens and workers and if those genes could be linked to specific functions essential for eusocial transition. 3. The insertion rate of transposons differs among differentially expressed genes and displays opposite trends between termites and cockroaches. The functions of termite transposon-rich queen- and worker-biased genes are related to reproduction and ageing and behaviour and gene expression, respectively. 4. Our study provides further evidence on the role of transposons in the evolution of eusociality, potentially through shifts in gene expression.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
1. Unravelling the molecular basis underlying major evolutionary transitions can shed light on how complex phenotypes arise. The evolution of eusociality, a major evolutionary transition, has been demonstrated to be accompanied by enhanced gene regulation. Numerous pieces of evidence suggest the major impact of transposon insertion on gene regulation and its role in adaptive evolution. Transposons have been shown to be play a role in gene duplication involved in the eusocial transition in termites. However, evidence of the molecular basis underlying the eusocial transition in Blattodea remains scarce. Could transposons have facilitated the eusocial transition in termites through shifts of gene expression? 2. Using available cockroach and termite genomes and transcriptomes, we investigated if transposons insert more frequently in genes with differential expression in queens and workers and if those genes could be linked to specific functions essential for eusocial transition. 3. The insertion rate of transposons differs among differentially expressed genes and displays opposite trends between termites and cockroaches. The functions of termite transposon-rich queen- and worker-biased genes are related to reproduction and ageing and behaviour and gene expression, respectively. 4. Our study provides further evidence on the role of transposons in the evolution of eusociality, potentially through shifts in gene expression.
Coban, Abdulbaki; Bornberg-Bauer, Erich; Kemena, Carsten
Domain Evolution of Vertebrate Blood Coagulation Cascade Proteins Journal Article
In: Journal of Molecular Evolution, 2022.
@article{Coban2022,
title = {Domain Evolution of Vertebrate Blood Coagulation Cascade Proteins},
author = {Abdulbaki Coban and Erich Bornberg-Bauer and Carsten Kemena},
url = {https://bornberglab.org/wp-content/uploads/2022/11/coban2022.pdf, Download},
doi = {https://doi.org/10.1007/s00239-022-10071-3},
year = {2022},
date = {2022-10-01},
urldate = {2022-08-31},
journal = {Journal of Molecular Evolution},
abstract = {Vertebrate blood coagulation is controlled by a cascade containing more than 20 proteins. The cascade proteins are found in the blood in their zymogen forms and when the cascade is triggered by tissue damage, zymogens are activated and in turn activate their downstream proteins by serine protease activity. In this study, we examined proteomes of 21 chordates, of which 18 are vertebrates, to reveal the modular evolution of the blood coagulation cascade. Additionally, two Arthropoda species were used to compare domain arrangements of the proteins belonging to the hemolymph clotting and the blood coagulation cascades. Within the vertebrate coagulation protein set, almost half of the studied proteins are shared with jawless vertebrates. Domain similarity analyses revealed that there are multiple possible evolutionary trajectories for each coagulation protein. During the evolution of higher vertebrate clades, gene and genome duplications led to the formation of other coagulation cascade proteins.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Vertebrate blood coagulation is controlled by a cascade containing more than 20 proteins. The cascade proteins are found in the blood in their zymogen forms and when the cascade is triggered by tissue damage, zymogens are activated and in turn activate their downstream proteins by serine protease activity. In this study, we examined proteomes of 21 chordates, of which 18 are vertebrates, to reveal the modular evolution of the blood coagulation cascade. Additionally, two Arthropoda species were used to compare domain arrangements of the proteins belonging to the hemolymph clotting and the blood coagulation cascades. Within the vertebrate coagulation protein set, almost half of the studied proteins are shared with jawless vertebrates. Domain similarity analyses revealed that there are multiple possible evolutionary trajectories for each coagulation protein. During the evolution of higher vertebrate clades, gene and genome duplications led to the formation of other coagulation cascade proteins.
Feldmeyer, Barbara; Gstöttl, Claudia; Wallner, Jennifer; Jongepier, Evelien; Séguret, Alice; Grasso, Donato A; Bornberg-Bauer, Erich; Foitzik, Susanne; Heinze, Jürgen
Evidence for a conserved queen-worker genetic toolkit across slave-making ants and their ant hosts Journal Article
In: Molecular Ecology, 2022.
@article{Feldmeyer2022,
title = {Evidence for a conserved queen-worker genetic toolkit across slave-making ants and their ant hosts},
author = {Barbara Feldmeyer and Claudia Gstöttl and Jennifer Wallner and Evelien Jongepier and Alice Séguret and Donato A Grasso and Erich Bornberg-Bauer and Susanne Foitzik and Jürgen Heinze},
url = {https://bornberglab.org/wp-content/uploads/2022/08/Molecular-Ecology-2022-Feldmeyer-Evidence-for-a-conserved-queen‐worker-genetic-toolkit-across-slave‐making-ants-and.pdf, Download},
doi = {https://doi.org/10.1111/mec.16639},
year = {2022},
date = {2022-08-03},
urldate = {2022-08-03},
journal = {Molecular Ecology},
abstract = {The ecological success of social Hymenoptera (ants, bees, wasps) depends on the division of labour between the queen and workers. Each caste exhibits highly specialised morphology, behaviour, and life-history traits, such as lifespan and fecundity. Despite strong defences against alien intruders, insect societies are vulnerable to social parasites, such as workerless inquilines or slave-making ants. Here, we investigate whether gene expression varies in parallel ways between lifestyles (slave-making versus host ants) across five independent origins of ant slavery in the “Formicoxenus-group” of the ant tribe Crematogastrini. As caste differences are often less pronounced in slave-making ants than in non-parasitic ants, we also compare caste-specific gene expression patterns between lifestyles. We demonstrate a substantial overlap in expression differences between queens and workers across taxa, irrespective of lifestyle. Caste affects the transcriptomes much more profoundly than lifestyle, as indicated by 37 times more genes being linked to caste than to lifestyle and by multiple caste-associated modules of co-expressed genes with strong connectivity. However, several genes and one gene module are linked to slave-making across the independent origins of this parasitic lifestyle, pointing to some evolutionary convergence. Finally, we do not find evidence for an interaction between caste and lifestyle, indicating that caste differences in gene expression remain consistent even when species switch to a parasitic lifestyle. Our findings strongly support the existence of a core set of genes whose expression is linked to the queen and worker caste in this ant taxon, as proposed by the “genetic toolkit” hypothesis.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The ecological success of social Hymenoptera (ants, bees, wasps) depends on the division of labour between the queen and workers. Each caste exhibits highly specialised morphology, behaviour, and life-history traits, such as lifespan and fecundity. Despite strong defences against alien intruders, insect societies are vulnerable to social parasites, such as workerless inquilines or slave-making ants. Here, we investigate whether gene expression varies in parallel ways between lifestyles (slave-making versus host ants) across five independent origins of ant slavery in the “Formicoxenus-group” of the ant tribe Crematogastrini. As caste differences are often less pronounced in slave-making ants than in non-parasitic ants, we also compare caste-specific gene expression patterns between lifestyles. We demonstrate a substantial overlap in expression differences between queens and workers across taxa, irrespective of lifestyle. Caste affects the transcriptomes much more profoundly than lifestyle, as indicated by 37 times more genes being linked to caste than to lifestyle and by multiple caste-associated modules of co-expressed genes with strong connectivity. However, several genes and one gene module are linked to slave-making across the independent origins of this parasitic lifestyle, pointing to some evolutionary convergence. Finally, we do not find evidence for an interaction between caste and lifestyle, indicating that caste differences in gene expression remain consistent even when species switch to a parasitic lifestyle. Our findings strongly support the existence of a core set of genes whose expression is linked to the queen and worker caste in this ant taxon, as proposed by the “genetic toolkit” hypothesis.
Eicholt, Lars A.; Aubel, Margaux; Berk, Katrin; Bornberg-Bauer, Erich; Lange, Andreas
Heterologous expression of naturally evolved putative de novo proteins with chaperones Journal Article
In: Protein Science. 2022;31(8):e4371., 2022.
@article{https://doi.org/10.1002/pro.4371,
title = {Heterologous expression of naturally evolved putative de novo proteins with chaperones},
author = {Lars A. Eicholt and Margaux Aubel and Katrin Berk and Erich Bornberg-Bauer and Andreas Lange},
url = {https://bornberglab.org/wp-content/uploads/2022/07/Protein-Science-2022-Eicholt-Heterologous-expression-of-naturally-evolved-putative-de-novo-proteins-with-chaperones.pdf, Download},
doi = {https://doi.org/10.1002/pro.4371},
year = {2022},
date = {2022-07-13},
urldate = {2022-02-27},
journal = {Protein Science. 2022;31(8):e4371.},
abstract = {Over the past decade, evidence has accumulated that new protein coding genes can emerge de novo from previously non-coding DNA. Most studies have focused on large scale com- putational predictions of de novo protein coding genes across a wide range of organisms. In contrast, experimental data concerning the folding and function of de novo proteins is scarce. This might be due to difficulties in handling de novo proteins in vitro, as most are predicted to be short and disordered. Here we propose a guideline for the effective expres- sion of eukaryotic de novo proteins in Escherichia coli.
We used 11 sequences from Drosophila melanogaster and 10 from Homo sapiens, that are predicted de novo proteins from former studies, for heterologous expression. The candidate de novo proteins have varying secondary structure and disorder content. Using multiple combinations of purification tags, E. coli expression strains and chaperone systems, we were able to increase the number of solubly expressed putative de novo proteins from 30 % to 62 %. Our findings indicate that the best combination for expressing putative de novo proteins in E.coli is a GST-tag with T7 Express cells and co-expressed chaperones. We found that, overall, proteins with higher predicted disorder were easier to express.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Over the past decade, evidence has accumulated that new protein coding genes can emerge de novo from previously non-coding DNA. Most studies have focused on large scale com- putational predictions of de novo protein coding genes across a wide range of organisms. In contrast, experimental data concerning the folding and function of de novo proteins is scarce. This might be due to difficulties in handling de novo proteins in vitro, as most are predicted to be short and disordered. Here we propose a guideline for the effective expres- sion of eukaryotic de novo proteins in Escherichia coli.
We used 11 sequences from Drosophila melanogaster and 10 from Homo sapiens, that are predicted de novo proteins from former studies, for heterologous expression. The candidate de novo proteins have varying secondary structure and disorder content. Using multiple combinations of purification tags, E. coli expression strains and chaperone systems, we were able to increase the number of solubly expressed putative de novo proteins from 30 % to 62 %. Our findings indicate that the best combination for expressing putative de novo proteins in E.coli is a GST-tag with T7 Express cells and co-expressed chaperones. We found that, overall, proteins with higher predicted disorder were easier to express.
We used 11 sequences from Drosophila melanogaster and 10 from Homo sapiens, that are predicted de novo proteins from former studies, for heterologous expression. The candidate de novo proteins have varying secondary structure and disorder content. Using multiple combinations of purification tags, E. coli expression strains and chaperone systems, we were able to increase the number of solubly expressed putative de novo proteins from 30 % to 62 %. Our findings indicate that the best combination for expressing putative de novo proteins in E.coli is a GST-tag with T7 Express cells and co-expressed chaperones. We found that, overall, proteins with higher predicted disorder were easier to express.
Harrison, Mark C.; Dohmen, Elias; George, Simon; Sillam-Dussès, David; Séité, Sarah; Vasseur-Cognet, Mireille
Complex regulatory role of DNA methylation in caste- and age-specific expression of a termite Journal Article
In: Open Biology, vol. 12, no. 7, 2022, ISSN: 2046-2441.
@article{nokeyb,
title = {Complex regulatory role of DNA methylation in caste- and age-specific expression of a termite},
author = {Mark C. Harrison and Elias Dohmen and Simon George and David Sillam-Dussès and Sarah Séité and Mireille Vasseur-Cognet},
url = {https://bornberglab.org/wp-content/uploads/2022/07/rsob.220047.pdf, Download},
doi = {10.1098/rsob.220047},
issn = {2046-2441},
year = {2022},
date = {2022-07-06},
urldate = {2022-07-06},
journal = {Open Biology},
volume = {12},
number = {7},
abstract = {The reproductive castes of eusocial insects are often characterized by extreme lifespans and reproductive output, indicating an absence of the fecundity/longevity trade-off. The role of DNA methylation in the regulation of caste- and age-specific gene expression in eusocial insects is controversial. While some studies find a clear link to caste formation in honeybees and ants, others find no correlation when replication is increased across independent colonies. Although recent studies have identified transcription patterns involved in the maintenance of high reproduction throughout the long lives of queens, the role of DNA methylation in the regulation of these genes is unknown. We carried out a comparative analysis of DNA methylation in the regulation of caste-specific transcription and its importance for the regulation of fertility and longevity in queens of the higher termite Macrotermes natalensis. We found evidence for significant, well-regulated changes in DNA methylation in mature compared to young queens, especially in several genes related to ageing and fecundity in mature queens. We also found a strong link between methylation and caste-specific alternative splicing. This study reveals a complex regulatory role of fat body DNA methylation both in the division of labour in termites, and during the reproductive maturation of queens.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The reproductive castes of eusocial insects are often characterized by extreme lifespans and reproductive output, indicating an absence of the fecundity/longevity trade-off. The role of DNA methylation in the regulation of caste- and age-specific gene expression in eusocial insects is controversial. While some studies find a clear link to caste formation in honeybees and ants, others find no correlation when replication is increased across independent colonies. Although recent studies have identified transcription patterns involved in the maintenance of high reproduction throughout the long lives of queens, the role of DNA methylation in the regulation of these genes is unknown. We carried out a comparative analysis of DNA methylation in the regulation of caste-specific transcription and its importance for the regulation of fertility and longevity in queens of the higher termite Macrotermes natalensis. We found evidence for significant, well-regulated changes in DNA methylation in mature compared to young queens, especially in several genes related to ageing and fecundity in mature queens. We also found a strong link between methylation and caste-specific alternative splicing. This study reveals a complex regulatory role of fat body DNA methylation both in the division of labour in termites, and during the reproductive maturation of queens.
Eenink, Bernard D. G.; Kaminski, Thomasz S.; Bornberg-Bauer, Erich; Jose, Joachim; Hollfelder, Florian; Loo, Bert
Vector Redesign and In-Droplet Cell-Growth Improves Enrichment and Recovery in live Escherichia coli Journal Article
In: Microbial Biotechnoly, 2022.
@article{Eenink2022,
title = {Vector Redesign and In-Droplet Cell-Growth Improves Enrichment and Recovery in live Escherichia coli},
author = {Bernard D. G. Eenink and Thomasz S. Kaminski and Erich Bornberg-Bauer and Joachim Jose and Florian Hollfelder and Bert Loo},
url = {https://bornberglab.org/wp-content/uploads/2022/09/Microbial-Biotechnology-2022-Eenink-Vector-redesign-and-in‐droplet-cell‐growth-improves-enrichment-and-recovery-in.pdf, Download},
doi = {https://doi.org/10.1111/1751-7915.14144},
year = {2022},
date = {2022-05-13},
urldate = {2022-05-13},
journal = {Microbial Biotechnoly},
abstract = {Directed evolution (DE) is a widely used method for improving the function of bio-molecules via multiple rounds of mutation
and selection. Microfluidic droplets have emerged as an important means to screen the large libraries needed for DE, but
was so far limited by the need to lyse cells, amplify DNA using PCR, and re-transform into cells for the next round,
necessitating the use of high-copy number plasmids or oversampling. Recently developed live cell recovery avoids some of
these complications by directly re-growing selected cells after sorting. However, repeated sorting cycles used to further
enrich top variants ultimately resulted unfavorable recovery of empty plasmid vector-containing cells over those expressing
the protein of interest. Engineering of the original expression vector solved the problem of enrichment of false-positive empty
vector-containing cells. Subsequent comparison of the efficiency of several methods for live cell recovery, pre-induction cell
growth inside droplets and pico-injection of substrate and/or combinations thereof showed that i) substrate encapsulation
from the start, i.e. prior to expression of enzyme, showed no disadvantage to post-induction substrate addition by picoinjection
with respect to recovery of true positive variants and ii) in-droplet pre-induction cell growth improves recovery and
enrichment of true positive variants.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Directed evolution (DE) is a widely used method for improving the function of bio-molecules via multiple rounds of mutation
and selection. Microfluidic droplets have emerged as an important means to screen the large libraries needed for DE, but
was so far limited by the need to lyse cells, amplify DNA using PCR, and re-transform into cells for the next round,
necessitating the use of high-copy number plasmids or oversampling. Recently developed live cell recovery avoids some of
these complications by directly re-growing selected cells after sorting. However, repeated sorting cycles used to further
enrich top variants ultimately resulted unfavorable recovery of empty plasmid vector-containing cells over those expressing
the protein of interest. Engineering of the original expression vector solved the problem of enrichment of false-positive empty
vector-containing cells. Subsequent comparison of the efficiency of several methods for live cell recovery, pre-induction cell
growth inside droplets and pico-injection of substrate and/or combinations thereof showed that i) substrate encapsulation
from the start, i.e. prior to expression of enzyme, showed no disadvantage to post-induction substrate addition by picoinjection
with respect to recovery of true positive variants and ii) in-droplet pre-induction cell growth improves recovery and
enrichment of true positive variants.
and selection. Microfluidic droplets have emerged as an important means to screen the large libraries needed for DE, but
was so far limited by the need to lyse cells, amplify DNA using PCR, and re-transform into cells for the next round,
necessitating the use of high-copy number plasmids or oversampling. Recently developed live cell recovery avoids some of
these complications by directly re-growing selected cells after sorting. However, repeated sorting cycles used to further
enrich top variants ultimately resulted unfavorable recovery of empty plasmid vector-containing cells over those expressing
the protein of interest. Engineering of the original expression vector solved the problem of enrichment of false-positive empty
vector-containing cells. Subsequent comparison of the efficiency of several methods for live cell recovery, pre-induction cell
growth inside droplets and pico-injection of substrate and/or combinations thereof showed that i) substrate encapsulation
from the start, i.e. prior to expression of enzyme, showed no disadvantage to post-induction substrate addition by picoinjection
with respect to recovery of true positive variants and ii) in-droplet pre-induction cell growth improves recovery and
enrichment of true positive variants.
Ariza, María; Fouks, Bertrand; Mauvisseau, Quentin; Halvorsen, Rune; Alsos, Inger Greve; Boer, Hugo J.
Plant biodiversity assessment through soil eDNA reflects temporal and local diversity Journal Article
In: Methods in Ecology and Evolution, 2022.
@article{nokeyc,
title = {Plant biodiversity assessment through soil eDNA reflects temporal and local diversity},
author = {María Ariza and Bertrand Fouks and Quentin Mauvisseau and Rune Halvorsen and Inger Greve Alsos and Hugo J. Boer},
url = {https://bornberglab.org/wp-content/uploads/2022/11/Ariza22.pdf},
doi = {https://doi.org/10.1111/2041-210X.13865},
year = {2022},
date = {2022-04-12},
journal = {Methods in Ecology and Evolution},
abstract = {1. Several studies have shown the potential of eDNA-based proxies for plant identification, but little is known about their spatial and temporal resolution. This limits its use for plant biodiversity assessments and monitoring of vegetation responses to environmental changes. Here we calibrate the temporal and spatial plant signals detected with soil eDNA surveys by comparing with a standard visual above-ground vegetation survey.
2. Our approach compares vegetation in an old-growth boreal forest in southern Norway, surveyed in 100 permanent 1-m2 plots seven times over a 30-year period, with a single soil eDNA metabarcoding-based survey from soil samples collected at the same 100 plots in the year of the last vegetation survey.
3. On average, 60% and 10% of the vascular plants and bryophytes recorded across all vegetation surveys were detected by soil eDNA. Taxa detected by soil eDNA were more representative for the local taxa pool than for the specific plot, and corresponded to those surveyed over the 30-year period although most closely matched the current taxa composition. Soil eDNA detected abundant taxa better than rare ones although both rare taxa and taxa unrecorded by the visual survey were detected.
4. Our study highlights the potential of soil eDNA assessments for monitoring of vegetation responses over broad spatial and temporal scales. The method's ability to detect abundant taxa makes it suitable for assessment of vegetation composition in a specific area and for broad-scale plant diversity assessments.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
1. Several studies have shown the potential of eDNA-based proxies for plant identification, but little is known about their spatial and temporal resolution. This limits its use for plant biodiversity assessments and monitoring of vegetation responses to environmental changes. Here we calibrate the temporal and spatial plant signals detected with soil eDNA surveys by comparing with a standard visual above-ground vegetation survey.
2. Our approach compares vegetation in an old-growth boreal forest in southern Norway, surveyed in 100 permanent 1-m2 plots seven times over a 30-year period, with a single soil eDNA metabarcoding-based survey from soil samples collected at the same 100 plots in the year of the last vegetation survey.
3. On average, 60% and 10% of the vascular plants and bryophytes recorded across all vegetation surveys were detected by soil eDNA. Taxa detected by soil eDNA were more representative for the local taxa pool than for the specific plot, and corresponded to those surveyed over the 30-year period although most closely matched the current taxa composition. Soil eDNA detected abundant taxa better than rare ones although both rare taxa and taxa unrecorded by the visual survey were detected.
4. Our study highlights the potential of soil eDNA assessments for monitoring of vegetation responses over broad spatial and temporal scales. The method's ability to detect abundant taxa makes it suitable for assessment of vegetation composition in a specific area and for broad-scale plant diversity assessments.
2. Our approach compares vegetation in an old-growth boreal forest in southern Norway, surveyed in 100 permanent 1-m2 plots seven times over a 30-year period, with a single soil eDNA metabarcoding-based survey from soil samples collected at the same 100 plots in the year of the last vegetation survey.
3. On average, 60% and 10% of the vascular plants and bryophytes recorded across all vegetation surveys were detected by soil eDNA. Taxa detected by soil eDNA were more representative for the local taxa pool than for the specific plot, and corresponded to those surveyed over the 30-year period although most closely matched the current taxa composition. Soil eDNA detected abundant taxa better than rare ones although both rare taxa and taxa unrecorded by the visual survey were detected.
4. Our study highlights the potential of soil eDNA assessments for monitoring of vegetation responses over broad spatial and temporal scales. The method's ability to detect abundant taxa makes it suitable for assessment of vegetation composition in a specific area and for broad-scale plant diversity assessments.
Grandchamp, Anna; Berk, Katrin; Dohmen, Elias; Bornberg-Bauer, Erich
New Genomic Signals Underlying the Emergence of Human Proto-Genes Journal Article
In: Genes, vol. 13, no. 2, pp. 284, 2022.
@article{nokeyd,
title = {New Genomic Signals Underlying the Emergence of Human Proto-Genes},
author = {Anna Grandchamp and Katrin Berk and Elias Dohmen and Erich Bornberg-Bauer},
editor = {Manyuan Long and Esther Betran},
url = {https://bornberglab.org/wp-content/uploads/2022/02/Genes_Grandchamp_et_all_proto-genes_02_2022.pdf, Download},
doi = {https://doi.org/10.3390/genes13020284},
year = {2022},
date = {2022-01-31},
urldate = {2022-01-31},
journal = {Genes},
volume = {13},
number = {2},
pages = {284},
abstract = {De novo genes are novel genes which emerge from non-coding DNA. Until now, little is known about de novo genes’ properties, correlated to their age and mechanisms of emergence. In this study, we investigate four related properties: introns, upstream regulatory motifs, 5′ Untranslated regions (UTRs) and protein domains, in 23,135 human proto-genes. We found that proto-genes contain introns, whose number and position correlates with the genomic position of proto-gene emergence. The origin of these introns is debated, as our results suggest that 41% of proto-genes might have captured existing introns, and 13.7% of them do not splice the ORF. We show that proto-genes which emerged via overprinting tend to be more enriched in core promotor motifs, while intergenic and intronic genes are more enriched in enhancers, even if the TATA motif is most commonly found upstream in these genes. Intergenic and intronic 5′ UTRs of proto-genes have a lower potential to stabilise mRNA structures than exonic proto-genes and established human genes. Finally, we confirm that proteins expressed by proto-genes gain new putative domains with age. Overall, we find that regulatory motifs inducing transcription and translation of previously non-coding sequences may facilitate proto-gene emergence. Our study demonstrates that introns, 5′ UTRs, and domains have specific properties in proto-genes. We also emphasize that the genomic positions of de novo genes strongly impacts these properties.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
De novo genes are novel genes which emerge from non-coding DNA. Until now, little is known about de novo genes’ properties, correlated to their age and mechanisms of emergence. In this study, we investigate four related properties: introns, upstream regulatory motifs, 5′ Untranslated regions (UTRs) and protein domains, in 23,135 human proto-genes. We found that proto-genes contain introns, whose number and position correlates with the genomic position of proto-gene emergence. The origin of these introns is debated, as our results suggest that 41% of proto-genes might have captured existing introns, and 13.7% of them do not splice the ORF. We show that proto-genes which emerged via overprinting tend to be more enriched in core promotor motifs, while intergenic and intronic genes are more enriched in enhancers, even if the TATA motif is most commonly found upstream in these genes. Intergenic and intronic 5′ UTRs of proto-genes have a lower potential to stabilise mRNA structures than exonic proto-genes and established human genes. Finally, we confirm that proteins expressed by proto-genes gain new putative domains with age. Overall, we find that regulatory motifs inducing transcription and translation of previously non-coding sequences may facilitate proto-gene emergence. Our study demonstrates that introns, 5′ UTRs, and domains have specific properties in proto-genes. We also emphasize that the genomic positions of de novo genes strongly impacts these properties.
Séité, Sarah; Harrison, Mark C.; Sillam-Dussès, David; Lupoli, Roland; Dooren, Tom J. M. Van; Robert, Alain; Poissonnier, Laure-Anne; Lemainque, Arnaud; Renault, David; Acket, Sébastien; Andrieu, Muriel; Viscarra, José; Sul, Hei Sook; Beer, Z. Wilhelm; Bornberg-Bauer, Erich; Vasseur-Cogne, Mireille
Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite Journal Article
In: Communications Biology, vol. 5, no. 44, 2022.
@article{nokeye,
title = {Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite},
author = {Sarah Séité and Mark C. Harrison and David Sillam-Dussès and Roland Lupoli and Tom J. M. Van Dooren and Alain Robert and Laure-Anne Poissonnier and Arnaud Lemainque and David Renault and Sébastien Acket and Muriel Andrieu and José Viscarra and Hei Sook Sul and Z. Wilhelm Beer and Erich Bornberg-Bauer and Mireille Vasseur-Cogne},
url = {https://bornberglab.org/wp-content/uploads/2022/11/Seite22.pdf},
doi = {https://doi.org/10.1038/s42003-021-02974-6},
year = {2022},
date = {2022-01-13},
urldate = {2022-01-13},
journal = {Communications Biology},
volume = {5},
number = {44},
abstract = {Kings and queens of eusocial termites can live for decades, while queens sustain a nearly maximal fertility. To investigate the molecular mechanisms underlying their long lifespan, we carried out transcriptomics, lipidomics and metabolomics in Macrotermes natalensis on sterile short-lived workers, long-lived kings and five stages spanning twenty years of adult queen maturation. Reproductives share gene expression differences from workers in agreement with a reduction of several aging-related processes, involving upregulation of DNA damage repair and mitochondrial functions. Anti-oxidant gene expression is downregulated, while peroxidability of membranes in queens decreases. Against expectations, we observed an upregulated gene expression in fat bodies of reproductives of several components of the IIS pathway, including an insulin-like peptide, Ilp9. This pattern does not lead to deleterious fat storage in physogastric queens, while simple sugars dominate in their hemolymph and large amounts of resources are allocated towards oogenesis. Our findings support the notion that all processes causing aging need to be addressed simultaneously in order to prevent it.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Kings and queens of eusocial termites can live for decades, while queens sustain a nearly maximal fertility. To investigate the molecular mechanisms underlying their long lifespan, we carried out transcriptomics, lipidomics and metabolomics in Macrotermes natalensis on sterile short-lived workers, long-lived kings and five stages spanning twenty years of adult queen maturation. Reproductives share gene expression differences from workers in agreement with a reduction of several aging-related processes, involving upregulation of DNA damage repair and mitochondrial functions. Anti-oxidant gene expression is downregulated, while peroxidability of membranes in queens decreases. Against expectations, we observed an upregulated gene expression in fat bodies of reproductives of several components of the IIS pathway, including an insulin-like peptide, Ilp9. This pattern does not lead to deleterious fat storage in physogastric queens, while simple sugars dominate in their hemolymph and large amounts of resources are allocated towards oogenesis. Our findings support the notion that all processes causing aging need to be addressed simultaneously in order to prevent it.
2021
Klein, Brennen; Holmér, Ludvig; Smith, Keith M.; Johnson, Mackenzie M.; Stolp, Laura; Teufel, Ashley I.; Kleppe, April Snofrid
A computational exploration of resilience and evolvability of protein–protein interaction networks Journal Article
In: communications biology, vol. 2021, no. 4, pp. 1352, 2021.
@article{klein2021.pdf,
title = {A computational exploration of resilience and evolvability of protein–protein interaction networks},
author = {Brennen Klein and Ludvig Holmér and Keith M. Smith and Mackenzie M. Johnson and Laura Stolp and Ashley I. Teufel and April Snofrid Kleppe},
doi = {https://doi.org/10.1038/s42003-021-02867-8},
year = {2021},
date = {2021-12-02},
journal = {communications biology},
volume = {2021},
number = {4},
pages = {1352},
abstract = {Protein–protein interaction (PPI) networks represent complex intra-cellular protein interac- tions, and the presence or absence of such interactions can lead to biological changes in an organism. Recent network-based approaches have shown that a phenotype’s PPI network’s resilience to environmental perturbations is related to its placement in the tree of life; though we still do not know how or why certain intra-cellular factors can bring about this resilience. Here, we explore the influence of gene expression and network properties on PPI networks’ resilience. We use publicly available data of PPIs for E. coli, S. cerevisiae, and H. sapiens, where we compute changes in network resilience as new nodes (proteins) are added to the net- works under three node addition mechanisms—random, degree-based, and gene-expression- based attachments. By calculating the resilience of the resulting networks, we estimate the effectiveness of these node addition mechanisms. We demonstrate that adding nodes with gene-expression-based preferential attachment (as opposed to random or degree-based) preserves and can increase the original resilience of PPI network in all three species, regardless of gene expression distribution or network structure. These findings introduce a general notion of prospective resilience, which highlights the key role of network structures in understanding the evolvability of phenotypic traits.
5, Anshuman Swain 6,},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Protein–protein interaction (PPI) networks represent complex intra-cellular protein interac- tions, and the presence or absence of such interactions can lead to biological changes in an organism. Recent network-based approaches have shown that a phenotype’s PPI network’s resilience to environmental perturbations is related to its placement in the tree of life; though we still do not know how or why certain intra-cellular factors can bring about this resilience. Here, we explore the influence of gene expression and network properties on PPI networks’ resilience. We use publicly available data of PPIs for E. coli, S. cerevisiae, and H. sapiens, where we compute changes in network resilience as new nodes (proteins) are added to the net- works under three node addition mechanisms—random, degree-based, and gene-expression- based attachments. By calculating the resilience of the resulting networks, we estimate the effectiveness of these node addition mechanisms. We demonstrate that adding nodes with gene-expression-based preferential attachment (as opposed to random or degree-based) preserves and can increase the original resilience of PPI network in all three species, regardless of gene expression distribution or network structure. These findings introduce a general notion of prospective resilience, which highlights the key role of network structures in understanding the evolvability of phenotypic traits.
5, Anshuman Swain 6,
5, Anshuman Swain 6,
Buchholz, Patrick C. F.; Loo, Bert; Eenink, Bernard D. G.; Bornberg-Bauer, Erich; Pleiss, Jürgen
Ancestral sequences of a large promiscuous enzyme family correspond to bridges in sequence space in a network representation Journal Article
In: Journal of the Royal Society Interface, vol. 18, no. 184, 2021, ISSN: 1742-5662.
@article{Buchholz2021b,
title = {Ancestral sequences of a large promiscuous enzyme family correspond to bridges in sequence space in a network representation},
author = {Patrick C. F. Buchholz and Bert Loo and Bernard D. G. Eenink and Erich Bornberg-Bauer and Jürgen Pleiss},
url = {https://bornberglab.org/wp-content/uploads/2021/12/buchholzetal2021.pdf, Download},
doi = {https://doi.org/10.1098/rsif.2021.0389},
issn = {1742-5662},
year = {2021},
date = {2021-11-03},
urldate = {2021-11-03},
journal = {Journal of the Royal Society Interface},
volume = {18},
number = {184},
abstract = {Evolutionary relationships of protein families can be characterized either by networks or by trees. Whereas trees allow for hierarchical grouping and reconstruction of the most likely ancestral sequences, networks lack a time axis but allow for thresholds of pairwise sequence identity to be chosen and, therefore, the clustering of family members with presumably more similar functions. Here, we use the large family of arylsulfatases and phosphonate monoester hydrolases to investigate similarities, strengths and weaknesses in tree and network representations. For varying thresholds of pairwise sequence identity, values of betweenness centrality and clustering coefficients were derived for nodes of the reconstructed ancestors to measure the propensity to act as a bridge in a network. Based on these properties, ancestral protein sequences emerge as bridges in protein sequence networks. Interestingly, many ancestral protein sequences appear close to extant sequences. Therefore, reconstructed ancestor sequences might also be interpreted as yet-to-be-identified homologues. The concept of ancestor reconstruction is compared to consensus sequences, too. It was found that hub sequences in a network, e.g. reconstructed ancestral sequences that are connected to many neighbouring sequences, share closer similarity with derived consensus sequences. Therefore, some reconstructed ancestor sequences can also be interpreted as consensus sequences.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Evolutionary relationships of protein families can be characterized either by networks or by trees. Whereas trees allow for hierarchical grouping and reconstruction of the most likely ancestral sequences, networks lack a time axis but allow for thresholds of pairwise sequence identity to be chosen and, therefore, the clustering of family members with presumably more similar functions. Here, we use the large family of arylsulfatases and phosphonate monoester hydrolases to investigate similarities, strengths and weaknesses in tree and network representations. For varying thresholds of pairwise sequence identity, values of betweenness centrality and clustering coefficients were derived for nodes of the reconstructed ancestors to measure the propensity to act as a bridge in a network. Based on these properties, ancestral protein sequences emerge as bridges in protein sequence networks. Interestingly, many ancestral protein sequences appear close to extant sequences. Therefore, reconstructed ancestor sequences might also be interpreted as yet-to-be-identified homologues. The concept of ancestor reconstruction is compared to consensus sequences, too. It was found that hub sequences in a network, e.g. reconstructed ancestral sequences that are connected to many neighbouring sequences, share closer similarity with derived consensus sequences. Therefore, some reconstructed ancestor sequences can also be interpreted as consensus sequences.
Jongepier, Evelien; Séguret, Alice; Labutin, Anton; Feldmeyer, Barbara; Gstöttl, Claudia; Foitzik, Susanne; Heinze, Jürgen; Bornberg-Bauer, Erich
Convergent loss of chemoreceptors across independent origins of slave-making in ants Journal Article
In: Molecular Biology and Evolution, vol. 39, no. 1, pp. msab305, 2021.
@article{Jongepier2021,
title = {Convergent loss of chemoreceptors across independent origins of slave-making in ants},
author = {Evelien Jongepier and Alice Séguret and Anton Labutin and Barbara Feldmeyer and Claudia Gstöttl and Susanne Foitzik and Jürgen Heinze and Erich Bornberg-Bauer},
editor = {Patricia Wittkopp},
url = {https://academic.oup.com/mbe/article/39/1/msab305/6404594
https://bornberglab.org/wp-content/uploads/2022/05/jongepier-et-al-MBE-2021.pdf, Download},
doi = {https://doi.org/10.1093/molbev/msab305},
year = {2021},
date = {2021-10-20},
urldate = {2021-10-20},
journal = {Molecular Biology and Evolution},
volume = {39},
number = {1},
pages = {msab305},
abstract = {The evolution of an obligate parasitic lifestyle often leads to the reduction of morphological and physiological traits, which may be accompanied by loss of genes and functions. Slave-making ants are social parasites that exploit the work force of closely related ant species for social behaviors such as brood care and foraging. Recent divergence between these social parasites and their hosts enables comparative studies of gene family evolution. We sequenced the genomes of eight ant species, representing three independent origins of ant slavery. During the evolution of eusociality, chemoreceptor genes multiplied due to the importance of chemical communication in insect societies. We investigated the evolutionary fate of these chemoreceptors and found that slave-making ant genomes harbored only half as many gustatory receptors as their hosts’, potentially mirroring the outsourcing of foraging tasks to host workers. In addition, parasites had fewer odorant receptors and their loss shows striking patterns of convergence across independent origins of parasitism, in particular in orthologs often implicated in sociality like the 9-exon odorant receptors. These convergent losses represent a rare case of convergent molecular evolution at the level of individual genes. Thus, evolution can operate in a way that is both repeatable and reversible when independent ant lineages lose important social traits during the transition to a parasitic lifestyle.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The evolution of an obligate parasitic lifestyle often leads to the reduction of morphological and physiological traits, which may be accompanied by loss of genes and functions. Slave-making ants are social parasites that exploit the work force of closely related ant species for social behaviors such as brood care and foraging. Recent divergence between these social parasites and their hosts enables comparative studies of gene family evolution. We sequenced the genomes of eight ant species, representing three independent origins of ant slavery. During the evolution of eusociality, chemoreceptor genes multiplied due to the importance of chemical communication in insect societies. We investigated the evolutionary fate of these chemoreceptors and found that slave-making ant genomes harbored only half as many gustatory receptors as their hosts’, potentially mirroring the outsourcing of foraging tasks to host workers. In addition, parasites had fewer odorant receptors and their loss shows striking patterns of convergence across independent origins of parasitism, in particular in orthologs often implicated in sociality like the 9-exon odorant receptors. These convergent losses represent a rare case of convergent molecular evolution at the level of individual genes. Thus, evolution can operate in a way that is both repeatable and reversible when independent ant lineages lose important social traits during the transition to a parasitic lifestyle.
Rivard, Emily L.; Ludwig, Andrew G.; Patel, Prjal H.; Grandchamp, Anna; Arnold, Sarah E.; Berger, Alina; Scott, Emilie M.; Kelly, Brendan J.; Mascha, Grace C.; Bornberg-Bauer, Erich; Findlay, Geoffrey D.
A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster Bachelor Thesis
2021.
@bachelorthesis{Rivard2021,
title = {A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster},
author = {Emily L. Rivard and Andrew G. Ludwig and Prjal H. Patel and Anna Grandchamp and Sarah E. Arnold and Alina Berger and Emilie M. Scott and Brendan J. Kelly and Grace C. Mascha and Erich Bornberg-Bauer and Geoffrey D. Findlay},
url = {https://bornberglab.org/wp-content/uploads/2022/05/Rivard2021.pdf, Download},
doi = {https://doi.org/10.1371/journal.pgen.1009787},
year = {2021},
date = {2021-09-03},
urldate = {2021-09-03},
journal = {PLoS Genetics},
volume = {17},
number = {(9)},
pages = {e1009787},
abstract = {Comparative genomics has enabled the identification of genes that potentially evolved de novo from non-coding sequences. Many such genes are expressed in male reproductive tissues, but their functions remain poorly understood. To address this, we conducted a functional genetic screen of over 40 putative de novo genes with testis-enriched expression in Drosophila melanogaster and identified one gene, atlas, required for male fertility. Detailed genetic and cytological analyses showed that atlas is required for proper chromatin condensation during the final stages of spermatogenesis. Atlas protein is expressed in spermatid nuclei and facilitates the transition from histone- to protamine-based chromatin packaging. Complementary evolutionary analyses revealed the complex evolutionary history of atlas. The protein-coding portion of the gene likely arose at the base of the Drosophila genus on the X chromosome but was unlikely to be essential, as it was then lost in several independent lineages. Within the last ~15 million years, however, the gene moved to an autosome, where it fused with a conserved non-coding RNA and evolved a non-redundant role in male fertility. Altogether, this study provides insight into the integration of novel genes into biological processes, the links between genomic innovation and functional evolution, and the genetic control of a fundamental developmental process, gametogenesis.},
keywords = {},
pubstate = {published},
tppubtype = {bachelorthesis}
}
Comparative genomics has enabled the identification of genes that potentially evolved de novo from non-coding sequences. Many such genes are expressed in male reproductive tissues, but their functions remain poorly understood. To address this, we conducted a functional genetic screen of over 40 putative de novo genes with testis-enriched expression in Drosophila melanogaster and identified one gene, atlas, required for male fertility. Detailed genetic and cytological analyses showed that atlas is required for proper chromatin condensation during the final stages of spermatogenesis. Atlas protein is expressed in spermatid nuclei and facilitates the transition from histone- to protamine-based chromatin packaging. Complementary evolutionary analyses revealed the complex evolutionary history of atlas. The protein-coding portion of the gene likely arose at the base of the Drosophila genus on the X chromosome but was unlikely to be essential, as it was then lost in several independent lineages. Within the last ~15 million years, however, the gene moved to an autosome, where it fused with a conserved non-coding RNA and evolved a non-redundant role in male fertility. Altogether, this study provides insight into the integration of novel genes into biological processes, the links between genomic innovation and functional evolution, and the genetic control of a fundamental developmental process, gametogenesis.
Martens, Leonie; Rühle, Frank; Witten, Anika; Meder, Benjamin; Katus, Hugo A.; Arbustini, Eloisa; Hasenfuss, Gerd; Sinner, Moritz F.; Kaab, Stefan; Pankuweit, Sabine; Angermann, Christiane; Bornberg-Bauer, Erich; Stoll, Monika
A genetic variant alters the secondary structure of the lncRNA H19 and is associated with Dilated Cardiomyopathy Journal Article
In: RNA Biology, 2021.
@article{Martens2021,
title = {A genetic variant alters the secondary structure of the lncRNA H19 and is associated with Dilated Cardiomyopathy},
author = {Leonie Martens and Frank Rühle and Anika Witten and Benjamin Meder and Hugo A. Katus and Eloisa Arbustini and Gerd Hasenfuss and Moritz F. Sinner and Stefan Kaab and Sabine Pankuweit and Christiane Angermann and Erich Bornberg-Bauer and Monika Stoll},
url = {https://bornberglab.org/wp-content/uploads/2021/09/martens2021.pdf, Download},
doi = {10.1080/15476286.2021.1952756},
year = {2021},
date = {2021-07-27},
urldate = {2021-07-27},
journal = {RNA Biology},
abstract = {lncRNAs are at the core of many regulatory processes and have also been recognized to be involved in various complex diseases. They affect gene regulation through direct interactions with RNA, DNA or proteins. Accordingly, lncRNA structure is likely to be essential for their regulatory function. Point mutations, which manifest as SNPs (single nucleotide polymorphisms) in genome screens, can substantially alter their function and, subsequently, the expression of their downstream regulated genes. To test the effect of SNPs on structure, we investigated lncRNAs associated with dilated cardiomyopathy. Among 322 human candidate lncRNAs, we demonstrate first the significant association of an SNP located in lncRNA H19 using data from 1084 diseased and 751 control patients. H19 is generally highly expressed in the heart, with a complex expression pattern during heart development. Next, we used MFE (minimum free energy) folding to demonstrate a significant refolding in the secondary structure of this 861 nt long lncRNA. Since MFE folding may overlook the importance of sub-optimal structures, we showed that this refolding also manifests in the overall Boltzmann structure ensemble. There, the composition of structures is tremendously affected in their thermodynamic probabilities through the genetic variant. Finally, we confirmed these results experimentally, using SHAPE-Seq, corroborating that SNPs affecting such structures may explain hidden genetic variance not accounted for through genome wide association studies. Our results suggest that structural changes in lncRNAs, and lncRNA H19 in particular, affect regulatory processes and represent optimal targets for further in-depth studies probing their molecular interactions.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
lncRNAs are at the core of many regulatory processes and have also been recognized to be involved in various complex diseases. They affect gene regulation through direct interactions with RNA, DNA or proteins. Accordingly, lncRNA structure is likely to be essential for their regulatory function. Point mutations, which manifest as SNPs (single nucleotide polymorphisms) in genome screens, can substantially alter their function and, subsequently, the expression of their downstream regulated genes. To test the effect of SNPs on structure, we investigated lncRNAs associated with dilated cardiomyopathy. Among 322 human candidate lncRNAs, we demonstrate first the significant association of an SNP located in lncRNA H19 using data from 1084 diseased and 751 control patients. H19 is generally highly expressed in the heart, with a complex expression pattern during heart development. Next, we used MFE (minimum free energy) folding to demonstrate a significant refolding in the secondary structure of this 861 nt long lncRNA. Since MFE folding may overlook the importance of sub-optimal structures, we showed that this refolding also manifests in the overall Boltzmann structure ensemble. There, the composition of structures is tremendously affected in their thermodynamic probabilities through the genetic variant. Finally, we confirmed these results experimentally, using SHAPE-Seq, corroborating that SNPs affecting such structures may explain hidden genetic variance not accounted for through genome wide association studies. Our results suggest that structural changes in lncRNAs, and lncRNA H19 in particular, affect regulatory processes and represent optimal targets for further in-depth studies probing their molecular interactions.
Bornberg-Bauer, Erich; Hlouchova, Klara; Lange, Andreas
Structure and function of naturally evolved de novo proteins Journal Article
In: Current Opinion in Structural Biology, vol. 68, pp. 175-183, 2021.
@article{Bornberg-Bauer2021,
title = {Structure and function of naturally evolved de novo proteins},
author = {Erich Bornberg-Bauer and Klara Hlouchova and Andreas Lange},
url = {https://bornberglab.org/wp-content/uploads/2021/08/Bornberg-bauer2021.pdf, Download},
doi = {10.1016/j.sbi.2020.11.010},
year = {2021},
date = {2021-06-01},
journal = {Current Opinion in Structural Biology},
volume = {68},
pages = {175-183},
abstract = {Comparative evolutionary genomics has revealed that novel protein coding genes can emerge randomly from non-coding DNA. While most of the myriad of transcripts which continuously emerge vanish rapidly, some attain regulatory regions, become translated and survive. More surprisingly, sequence properties of de novo proteins are almost indistinguishable from randomly obtained sequences, yet de novo proteins may gain functions and integrate into eukaryotic cellular networks quite easily. We here discuss current knowledge on de novo proteins, their structures, functions and evolution. Since the existence of de novo proteins seems at odds with decade-long attempts to construct proteins with novel structures and functions from scratch, we suggest that a better understanding of de novo protein evolution may fuel new strategies for protein design.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Comparative evolutionary genomics has revealed that novel protein coding genes can emerge randomly from non-coding DNA. While most of the myriad of transcripts which continuously emerge vanish rapidly, some attain regulatory regions, become translated and survive. More surprisingly, sequence properties of de novo proteins are almost indistinguishable from randomly obtained sequences, yet de novo proteins may gain functions and integrate into eukaryotic cellular networks quite easily. We here discuss current knowledge on de novo proteins, their structures, functions and evolution. Since the existence of de novo proteins seems at odds with decade-long attempts to construct proteins with novel structures and functions from scratch, we suggest that a better understanding of de novo protein evolution may fuel new strategies for protein design.
Harrison, Mark C.; Niño, Luisa M. Jaimes; Rodrigues, Marisa Almeida; Ryll, Judith; Flatt, Thomas; Oettler, Jan; Bornberg-Bauer, Erich
Gene Coexpression Network Reveals Highly Conserved,Well- Regulated Anti-AgeingMechanisms in Old Ant Queens Journal Article
In: Genome Biology and Evolution, vol. 13, no. 6, 2021.
@article{Harrison2021,
title = {Gene Coexpression Network Reveals Highly Conserved,Well- Regulated Anti-AgeingMechanisms in Old Ant Queens},
author = {Mark C. Harrison and Luisa M. Jaimes Niño and Marisa Almeida Rodrigues and Judith Ryll and Thomas Flatt and Jan Oettler and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/08/harrison2021.pdf, Download},
doi = {10.1093/gbe/evab093},
year = {2021},
date = {2021-05-04},
journal = {Genome Biology and Evolution},
volume = {13},
number = {6},
abstract = {Evolutionary theories of ageing predict a reduction in selection efficiency with age, a so-called “selection shadow,” due to extrinsic mortality decreasing effective population size with age. Classic symptoms of ageing include a deterioration in transcriptional regulation and protein homeostasis. Understanding how ant queens defy the trade-off between fecundity and lifespan remains a major challenge for the evolutionary theory of ageing. It has often been discussed that the low extrinsic mortality of ant queens, that are generally well protected within the nest by workers and soldiers, should reduce the selection shadow acting on old queens. We tested this by comparing strength of selection acting on genes upregulated in young and old queens of the ant, Cardiocondyla obscurior. In support of a reduced selection shadow, we find old-biased genes to be under strong purifying selection. We also analyzed a gene coexpression network (GCN) with the aim to detect signs of ageing in the form of deteriorating regulation and proteostasis. We find no evidence for ageing. In fact, we detect higher connectivity in old queens indicating increased transcriptional regulation with age. Within the GCN, we discover five highly correlated modules that are upregulated with age. These old-biased modules regulate several antiageing mechanisms such as maintenance of proteostasis, transcriptional regulation, and stress response. We observe stronger purifying selection on central hub genes of these old-biased modules compared with young-biased modules. These results indicate a lack of transcriptional ageing in old C. obscurior queens, possibly facilitated by strong selection at old age and well-regulated antiageing mechanisms.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Evolutionary theories of ageing predict a reduction in selection efficiency with age, a so-called “selection shadow,” due to extrinsic mortality decreasing effective population size with age. Classic symptoms of ageing include a deterioration in transcriptional regulation and protein homeostasis. Understanding how ant queens defy the trade-off between fecundity and lifespan remains a major challenge for the evolutionary theory of ageing. It has often been discussed that the low extrinsic mortality of ant queens, that are generally well protected within the nest by workers and soldiers, should reduce the selection shadow acting on old queens. We tested this by comparing strength of selection acting on genes upregulated in young and old queens of the ant, Cardiocondyla obscurior. In support of a reduced selection shadow, we find old-biased genes to be under strong purifying selection. We also analyzed a gene coexpression network (GCN) with the aim to detect signs of ageing in the form of deteriorating regulation and proteostasis. We find no evidence for ageing. In fact, we detect higher connectivity in old queens indicating increased transcriptional regulation with age. Within the GCN, we discover five highly correlated modules that are upregulated with age. These old-biased modules regulate several antiageing mechanisms such as maintenance of proteostasis, transcriptional regulation, and stress response. We observe stronger purifying selection on central hub genes of these old-biased modules compared with young-biased modules. These results indicate a lack of transcriptional ageing in old C. obscurior queens, possibly facilitated by strong selection at old age and well-regulated antiageing mechanisms.
Fouks, Bertrand; Brand, Philipp; Nguyen, Hung N.; Herman, Jacob; Camara, Francisco; Ence, Daniel; Hagen, Darren E.; Hoff, Katharina J.; Nachweide, Stefanie; Romoth, Lars; Walden, Kimberly K. O.; Guigo, Roderic; Stanke, Mario; Narzisi, Giuseppe; Yandell, Mark; Robertson, Hugh M.; Koeniger, Nikolaus; Chantawannakul, Panuwan; Schatz, Michael C.; Worley, Kim C.; Robinson, Gene E.; Elsik, Christine G.; Rueppell, Olav
The genomic basis of evolutionary differentiation among honey bees Journal Article
In: Genome Research, vol. 31, no. 7, pp. 1203-1215, 2021.
@article{nokeyf,
title = {The genomic basis of evolutionary differentiation among honey bees},
author = {Bertrand Fouks and Philipp Brand and Hung N. Nguyen and Jacob Herman and Francisco Camara and Daniel Ence and Darren E. Hagen and Katharina J. Hoff and Stefanie Nachweide and Lars Romoth and Kimberly K. O. Walden and Roderic Guigo and Mario Stanke and Giuseppe Narzisi and Mark Yandell and Hugh M. Robertson and Nikolaus Koeniger and Panuwan Chantawannakul and Michael C. Schatz and Kim C. Worley and Gene E. Robinson and Christine G. Elsik and Olav Rueppell},
url = {https://bornberglab.org/wp-content/uploads/2022/11/Fouks21.pdf},
doi = {doi:10.1101/gr.272310.120},
year = {2021},
date = {2021-05-04},
journal = {Genome Research},
volume = {31},
number = {7},
pages = {1203-1215},
abstract = {In contrast to the western honey bee, Apis mellifera, other honey bee species have been largely neglected despite their importance and diversity. The genetic basis of the evolutionary diversification of honey bees remains largely unknown. Here, we provide a genome-wide comparison of three honey bee species, each representing one of the three subgenera of honey bees, namely the dwarf (Apis florea), giant (A. dorsata), and cavity-nesting (A. mellifera) honey bees with bumblebees as an outgroup. Our analyses resolve the phylogeny of honey bees with the dwarf honey bees diverging first. We find that evolution of increased eusocial complexity in Apis proceeds via increases in the complexity of gene regulation, which is in agreement with previous studies. However, this process seems to be related to pathways other than transcriptional control. Positive selection patterns across Apis reveal a trade-off between maintaining genome stability and generating genetic diversity, with a rapidly evolving piRNA pathway leading to genomes depleted of transposable elements, and a rapidly evolving DNA repair pathway associated with high recombination rates in all Apis species. Diversification within Apis is accompanied by positive selection in several genes whose putative functions present candidate mechanisms for lineage-specific adaptations, such as migration, immunity, and nesting behavior.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
In contrast to the western honey bee, Apis mellifera, other honey bee species have been largely neglected despite their importance and diversity. The genetic basis of the evolutionary diversification of honey bees remains largely unknown. Here, we provide a genome-wide comparison of three honey bee species, each representing one of the three subgenera of honey bees, namely the dwarf (Apis florea), giant (A. dorsata), and cavity-nesting (A. mellifera) honey bees with bumblebees as an outgroup. Our analyses resolve the phylogeny of honey bees with the dwarf honey bees diverging first. We find that evolution of increased eusocial complexity in Apis proceeds via increases in the complexity of gene regulation, which is in agreement with previous studies. However, this process seems to be related to pathways other than transcriptional control. Positive selection patterns across Apis reveal a trade-off between maintaining genome stability and generating genetic diversity, with a rapidly evolving piRNA pathway leading to genomes depleted of transposable elements, and a rapidly evolving DNA repair pathway associated with high recombination rates in all Apis species. Diversification within Apis is accompanied by positive selection in several genes whose putative functions present candidate mechanisms for lineage-specific adaptations, such as migration, immunity, and nesting behavior.
Séguret, Alice; Stolle, Eckart; Fleites-Ayil, Fernando A; Quezada-Euán, José Javier G; Hartfelder, Klaus; Meusemann, Karen; Harrison, Mark C.; Soro, Antonella; Paxton, Robert J
Transcriptomic Signatures of Ageing Vary in Solitary and Social Forms of an Orchid Bee Journal Article
In: Genome Biology and Evolution, vol. 13, no. 6, 2021.
@article{Séguret2021,
title = {Transcriptomic Signatures of Ageing Vary in Solitary and Social Forms of an Orchid Bee},
author = {Alice Séguret and Eckart Stolle and Fernando A Fleites-Ayil and José Javier G Quezada-Euán and Klaus Hartfelder and Karen Meusemann and Mark C. Harrison and Antonella Soro and Robert J Paxton},
url = {https://bornberglab.org/wp-content/uploads/2021/08/seguret_2021.pdf, Download},
year = {2021},
date = {2021-04-29},
journal = {Genome Biology and Evolution},
volume = {13},
number = {6},
abstract = {Eusocial insect queens are remarkable in their ability to maximize both fecundity and longevity, thus escaping the typical trade-off between these two traits. Several mechanisms have been proposed to underlie the remolding of the trade-off, such as reshaping of the juvenile hormone (JH) pathway, or caste-specific susceptibility to oxidative stress. However, it remains a challenge to disentangle the molecular mechanisms underlying the remolding of the trade-off in eusocial insects from caste-specific physiological attributes that have subsequently arisen. The socially polymorphic orchid bee Euglossa viridissima represents an excellent model to address the role of sociality per se in longevity as it allows direct comparisons of solitary and social individuals within a common genetic background. We investigated gene expression and JH levels in young and old bees from both solitary and social nests. We found 902 genes to be differentially expressed with age in solitary females, including genes involved in oxidative stress, versus only 100 genes in social dominant females, and 13 genes in subordinate females. A weighted gene coexpression network analysis further highlights pathways related to ageing in this species, including the target of rapamycin pathway. Eleven genes involved in translation, apoptosis, and DNA repair show concurrent age-related expression changes in solitary but not in social females, representing potential differences based on social status. JH titers did not vary with age or social status. Our results represent an important step in understanding the proximate mechanisms underlying the remodeling of the fecundity/longevity trade-off that accompanies the evolutionary transition from solitary life to eusociality.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Eusocial insect queens are remarkable in their ability to maximize both fecundity and longevity, thus escaping the typical trade-off between these two traits. Several mechanisms have been proposed to underlie the remolding of the trade-off, such as reshaping of the juvenile hormone (JH) pathway, or caste-specific susceptibility to oxidative stress. However, it remains a challenge to disentangle the molecular mechanisms underlying the remolding of the trade-off in eusocial insects from caste-specific physiological attributes that have subsequently arisen. The socially polymorphic orchid bee Euglossa viridissima represents an excellent model to address the role of sociality per se in longevity as it allows direct comparisons of solitary and social individuals within a common genetic background. We investigated gene expression and JH levels in young and old bees from both solitary and social nests. We found 902 genes to be differentially expressed with age in solitary females, including genes involved in oxidative stress, versus only 100 genes in social dominant females, and 13 genes in subordinate females. A weighted gene coexpression network analysis further highlights pathways related to ageing in this species, including the target of rapamycin pathway. Eleven genes involved in translation, apoptosis, and DNA repair show concurrent age-related expression changes in solitary but not in social females, representing potential differences based on social status. JH titers did not vary with age or social status. Our results represent an important step in understanding the proximate mechanisms underlying the remodeling of the fecundity/longevity trade-off that accompanies the evolutionary transition from solitary life to eusociality.
Lange, Andreas; Patel, Prajal H.; Heames, Brennen; Damry, Adam M.; Saenger, Thorsten; Jackson, Colin J.; Findlay, Geoffrey D.; Bornberg-Bauer, Erich
Structural and functional characterization of a putative de novo gene in Drosophila Journal Article
In: Nature Communications, vol. 12, no. 1667, pp. 1-13, 2021.
@article{Lange2021,
title = {Structural and functional characterization of a putative de novo gene in Drosophila},
author = {Andreas Lange and Prajal H. Patel and Brennen Heames and Adam M. Damry and Thorsten Saenger and Colin J. Jackson and Geoffrey D. Findlay and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/lange2021.pdf, Download},
doi = {10.1038/s41467-021-21667-6},
year = {2021},
date = {2021-03-12},
urldate = {2021-03-12},
journal = {Nature Communications},
volume = {12},
number = {1667},
pages = {1-13},
abstract = {Comparative genomic studies have repeatedly shown that new protein-coding genes can emerge de novo from noncoding DNA. Still unknown is how and when the structures of encoded de novo proteins emerge and evolve. Combining biochemical, genetic and evolutionary analyses, we elucidate the function and structure of goddard, a gene which appears to have evolved de novo at least 50 million years ago within the Drosophila genus. Previous studies found that goddard is required for male fertility. Here, we show that Goddard protein localizes to elongating sperm axonemes and that in its absence, elongated spermatids fail to undergo individualization. Combining modelling, NMR and circular dichroism (CD) data, we show that Goddard protein contains a large central α-helix, but is otherwise partially disordered. We find similar results for Goddard’s orthologs from divergent fly species and their reconstructed ancestral sequences. Accordingly, Goddard’s structure appears to have been maintained with only minor changes over millions of years.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Comparative genomic studies have repeatedly shown that new protein-coding genes can emerge de novo from noncoding DNA. Still unknown is how and when the structures of encoded de novo proteins emerge and evolve. Combining biochemical, genetic and evolutionary analyses, we elucidate the function and structure of goddard, a gene which appears to have evolved de novo at least 50 million years ago within the Drosophila genus. Previous studies found that goddard is required for male fertility. Here, we show that Goddard protein localizes to elongating sperm axonemes and that in its absence, elongated spermatids fail to undergo individualization. Combining modelling, NMR and circular dichroism (CD) data, we show that Goddard protein contains a large central α-helix, but is otherwise partially disordered. We find similar results for Goddard’s orthologs from divergent fly species and their reconstructed ancestral sequences. Accordingly, Goddard’s structure appears to have been maintained with only minor changes over millions of years.
He, Shulin; Sieksmeyer, Thorben; Che, Yanli; Mora, M. Alejandra Esparza; Stiblik, Petr; Banasiak, Ronald; Harrison, Mark C.; Šobotník, Jan; Wang, Zongqing; Johnston, Paul R.; McMahon, Dino P.
Evidence for reduced immune gene diversity and activity during the evolution of termites Journal Article
In: Proceedings of the Royal Society B, vol. 288, no. 1945, 2021.
@article{He2021,
title = {Evidence for reduced immune gene diversity and activity during the evolution of termites},
author = {Shulin He and Thorben Sieksmeyer and Yanli Che and M. Alejandra Esparza Mora and Petr Stiblik and Ronald Banasiak and Mark C. Harrison and Jan Šobotník and Zongqing Wang and Paul R. Johnston and Dino P. McMahon},
url = {https://bornberglab.org/wp-content/uploads/2021/08/he2021.pdf, Download},
doi = {10.1098/rspb.2020.3168},
year = {2021},
date = {2021-02-17},
journal = {Proceedings of the Royal Society B},
volume = {288},
number = {1945},
abstract = {The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence.
Stoldt, Marah; Klein, Linda; Beros, Sara; Buter, Falk; Jongepier, Evelien; Feldmeyer, Barbara; Foitzik, Susanne
Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity Journal Article
In: Genes, vol. 12(1), no. 95, 2021.
@article{Stoldt2021,
title = {Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity},
author = {Marah Stoldt and Linda Klein and Sara Beros and Falk Buter and Evelien Jongepier and Barbara Feldmeyer and Susanne Foitzik},
url = {https://bornberglab.org/wp-content/uploads/2022/05/Stoldt2021.pdf, Download},
doi = {10.3390/genes12010095},
year = {2021},
date = {2021-01-13},
urldate = {2021-01-13},
journal = {Genes},
volume = {12(1)},
number = {95},
abstract = {Most species are either parasites or exploited by parasites, making parasite–host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain phenotypic changes in the ant Temnothorax nylanderi, the intermediate host of the cestode Anomotaenia brevis. In addition to behavioral and morphological alterations, infected workers exhibit prolonged lifespans, comparable to that of queens, which live up to two decades. We used transcriptomic data from cestodes and ants of different castes and infection status to investigate the molecular underpinnings of phenotypic alterations in infected workers and explored whether the extended lifespan of queens and infected workers has a common molecular basis. Infected workers and queens commonly upregulated only six genes, one of them with a known anti-aging function. Both groups overexpressed immune genes, although not the same ones. Our findings suggest that the lifespan extension of infected workers is not achieved via the expression of queen-specific genes. The analysis of the cestodes’ transcriptome revealed dominant expression of genes of the mitochondrial respiratory transport chain, which indicates an active metabolism and shedding light on the physiology of the parasite in its cysticercoid stage.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Most species are either parasites or exploited by parasites, making parasite–host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain phenotypic changes in the ant Temnothorax nylanderi, the intermediate host of the cestode Anomotaenia brevis. In addition to behavioral and morphological alterations, infected workers exhibit prolonged lifespans, comparable to that of queens, which live up to two decades. We used transcriptomic data from cestodes and ants of different castes and infection status to investigate the molecular underpinnings of phenotypic alterations in infected workers and explored whether the extended lifespan of queens and infected workers has a common molecular basis. Infected workers and queens commonly upregulated only six genes, one of them with a known anti-aging function. Both groups overexpressed immune genes, although not the same ones. Our findings suggest that the lifespan extension of infected workers is not achieved via the expression of queen-specific genes. The analysis of the cestodes’ transcriptome revealed dominant expression of genes of the mitochondrial respiratory transport chain, which indicates an active metabolism and shedding light on the physiology of the parasite in its cysticercoid stage.
2020
Harrison, Mark C.; Chernyshova, Anna M.; Thompson, Graham J.
No obvious transcriptome‐wide signature of indirect selection in termites Journal Article
In: Journal of Evolutionary Biology, vol. 34, no. 2, pp. 403-415, 2020.
@article{Harrison2020,
title = {No obvious transcriptome‐wide signature of indirect selection in termites},
author = {Mark C. Harrison and Anna M. Chernyshova and Graham J. Thompson},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Harrison2020.pdf, Download},
doi = {10.1111/jeb.13749},
year = {2020},
date = {2020-12-08},
journal = {Journal of Evolutionary Biology},
volume = {34},
number = {2},
pages = {403-415},
abstract = {The evolution of sterile helper castes in social insects implies selection on genes that underlie variation in this nonreproductive phenotype. These focal genes confer no direct fitness and are presumed to evolve through indirect fitness effects on the helper's reproducing relatives. This separation of a gene's phenotypic effect on one caste and its fitness effect on another suggests that genes for this and other forms of reproductive altruism are buffered from selection and will thus evolve closer to the neutral rate than genes directly selected for selfish reproduction. We test this hypothesis by comparing the strength of selection at loci associated in their expression with reproductive versus sterile castes in termites. Specifically, we gather caste‐biased gene expression data from four termite transcriptomes and measure the global dN/dS ratio across gene sets and phylogenetic lineages. We find that the majority of examined orthologous gene groups show patterns of nucleotide substitution that are consistent with strong purifying selection and display little evidence for distinct signatures of direct versus indirect selection in reproductive and sterile castes. For one particular species (Reticulitermes flavipes), the strength of purifying selection is relaxed in a reproductive nymph‐biased gene set, which opposes the nearly neutral idea. In other species, the synonymous rate (dS) alone was often found to be the highest in the sterile worker caste, suggesting a more subtle signature of indirect selection or an altogether different relationship between caste‐biased expression and rates of molecular evolution.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The evolution of sterile helper castes in social insects implies selection on genes that underlie variation in this nonreproductive phenotype. These focal genes confer no direct fitness and are presumed to evolve through indirect fitness effects on the helper's reproducing relatives. This separation of a gene's phenotypic effect on one caste and its fitness effect on another suggests that genes for this and other forms of reproductive altruism are buffered from selection and will thus evolve closer to the neutral rate than genes directly selected for selfish reproduction. We test this hypothesis by comparing the strength of selection at loci associated in their expression with reproductive versus sterile castes in termites. Specifically, we gather caste‐biased gene expression data from four termite transcriptomes and measure the global dN/dS ratio across gene sets and phylogenetic lineages. We find that the majority of examined orthologous gene groups show patterns of nucleotide substitution that are consistent with strong purifying selection and display little evidence for distinct signatures of direct versus indirect selection in reproductive and sterile castes. For one particular species (Reticulitermes flavipes), the strength of purifying selection is relaxed in a reproductive nymph‐biased gene set, which opposes the nearly neutral idea. In other species, the synonymous rate (dS) alone was often found to be the highest in the sterile worker caste, suggesting a more subtle signature of indirect selection or an altogether different relationship between caste‐biased expression and rates of molecular evolution.
Scharsack, Jörn P.; Wieczorek, Bartholomäus; Schmidt‐Drewello, Alexander; Büscher, Janine; Franke, Frederik; Moore, Andrew D.; Branca, Antoine; Witten, Anika; Stoll, Monika; Bornberg-Bauer, Erich; Wicke, Susann; Kurtz, Joachim
Climate change facilitates a parasite’s host exploitation via temperature-mediated immunometabolic processes Journal Article
In: Global Change Biology, vol. 27, no. 1, pp. 94-107, 2020.
@article{Scharsack2020,
title = {Climate change facilitates a parasite’s host exploitation via temperature-mediated immunometabolic processes},
author = {Jörn P. Scharsack and Bartholomäus Wieczorek and Alexander Schmidt‐Drewello and Janine Büscher and Frederik Franke and Andrew D. Moore and Antoine Branca and Anika Witten and Monika Stoll and Erich Bornberg-Bauer and Susann Wicke and Joachim Kurtz},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Scharsack2020.pdf, Download},
doi = {10.1111/gcb.15402},
year = {2020},
date = {2020-10-17},
journal = {Global Change Biology},
volume = {27},
number = {1},
pages = {94-107},
abstract = {Global climate change can influence organismic interactions like those between hosts and parasites. Rising temperatures may exacerbate the exploitation of hosts by parasites, especially in ectothermic systems. The metabolic activity of ectotherms is strongly linked to temperature and generally increases when temperatures rise. We hypothesized that temperature change in combination with parasite infection interferes with the host's immunometabolism. We used a parasite, the avian cestode Schistocephalus solidus, which taps most of its resources from the metabolism of an ectothermic intermediate host, the three‐spined stickleback. We experimentally exposed sticklebacks to this parasite, and studied liver transcriptomes 50 days after infection at 13°C and 24°C, to assess their immunometabolic responses. Furthermore, we monitored fitness parameters of the parasite and examined immunity and body condition of the sticklebacks at 13°C, 18°C and 24°C after 36, 50 and 64 days of infection. At low temperatures (13°C), S. solidus growth was constrained, presumably also by the more active stickleback's immune system, thus delaying its infectivity for the final host to 64 days. Warmer temperature (18°C and 24°C) enhanced S. solidus growth, and it became infective to the final host already after 36 days. Overall, S. solidus produced many more viable offspring after development at elevated temperatures. In contrast, stickleback hosts had lower body conditions, and their immune system was less active at warm temperature. The stickleback's liver transcriptome revealed that mainly metabolic processes were differentially regulated between temperatures, whereas immune genes were not strongly affected. Temperature effects on gene expression were strongly enhanced in infected sticklebacks, and even in exposed‐but‐not‐infected hosts. These data suggest that the parasite exposure in concert with rising temperature, as to be expected with global climate change, shifted the host's immunometabolism, thus providing nutrients for the enormous growth of the parasite and, at the same time suppressing immune defence.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Global climate change can influence organismic interactions like those between hosts and parasites. Rising temperatures may exacerbate the exploitation of hosts by parasites, especially in ectothermic systems. The metabolic activity of ectotherms is strongly linked to temperature and generally increases when temperatures rise. We hypothesized that temperature change in combination with parasite infection interferes with the host's immunometabolism. We used a parasite, the avian cestode Schistocephalus solidus, which taps most of its resources from the metabolism of an ectothermic intermediate host, the three‐spined stickleback. We experimentally exposed sticklebacks to this parasite, and studied liver transcriptomes 50 days after infection at 13°C and 24°C, to assess their immunometabolic responses. Furthermore, we monitored fitness parameters of the parasite and examined immunity and body condition of the sticklebacks at 13°C, 18°C and 24°C after 36, 50 and 64 days of infection. At low temperatures (13°C), S. solidus growth was constrained, presumably also by the more active stickleback's immune system, thus delaying its infectivity for the final host to 64 days. Warmer temperature (18°C and 24°C) enhanced S. solidus growth, and it became infective to the final host already after 36 days. Overall, S. solidus produced many more viable offspring after development at elevated temperatures. In contrast, stickleback hosts had lower body conditions, and their immune system was less active at warm temperature. The stickleback's liver transcriptome revealed that mainly metabolic processes were differentially regulated between temperatures, whereas immune genes were not strongly affected. Temperature effects on gene expression were strongly enhanced in infected sticklebacks, and even in exposed‐but‐not‐infected hosts. These data suggest that the parasite exposure in concert with rising temperature, as to be expected with global climate change, shifted the host's immunometabolism, thus providing nutrients for the enormous growth of the parasite and, at the same time suppressing immune defence.
Dowling, Daniel; Schmitz, Jonathan F.; Bornberg-Bauer, Erich
Stochastic Gain and Loss of Novel Transcribed Open Reading Frames in the Human Lineage Journal Article
In: Genome Biology and Evolution, vol. 12, no. 11, pp. 2183–2195, 2020.
@article{Dowling2020,
title = {Stochastic Gain and Loss of Novel Transcribed Open Reading Frames in the Human Lineage},
author = {Daniel Dowling and Jonathan F. Schmitz and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Dowling2020.pdf, Download},
doi = {10.1093/gbe/evaa194},
year = {2020},
date = {2020-09-16},
journal = {Genome Biology and Evolution},
volume = {12},
number = {11},
pages = {2183–2195},
abstract = {In addition to known genes, much of the human genome is transcribed into RNA. Chance formation of novel open reading frames (ORFs) can lead to the translation of myriad new proteins. Some of these ORFs may yield advantageous adaptive de novo proteins. However, widespread translation of noncoding DNA can also produce hazardous protein molecules, which can misfold and/or form toxic aggregates. The dynamics of how de novo proteins emerge from potentially toxic raw materials and what influences their long-term survival are unknown. Here, using transcriptomic data from human and five other primates, we generate a set of transcribed human ORFs at six conservation levels to investigate which properties influence the early emergence and long-term retention of these expressed ORFs. As these taxa diverged from each other relatively recently, we present a fine scale view of the evolution of novel sequences over recent evolutionary time. We find that novel human-restricted ORFs are preferentially located on GC-rich gene-dense chromosomes, suggesting their retention is linked to pre-existing genes. Sequence properties such as intrinsic structural disorder and aggregation propensity—which have been proposed to play a role in survival of de novo genes—remain unchanged over time. Even very young sequences code for proteins with low aggregation propensities, suggesting that genomic regions with many novel transcribed ORFs are concomitantly less likely to produce ORFs which code for harmful toxic proteins. Our data indicate that the survival of these novel ORFs is largely stochastic rather than shaped by selection.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
In addition to known genes, much of the human genome is transcribed into RNA. Chance formation of novel open reading frames (ORFs) can lead to the translation of myriad new proteins. Some of these ORFs may yield advantageous adaptive de novo proteins. However, widespread translation of noncoding DNA can also produce hazardous protein molecules, which can misfold and/or form toxic aggregates. The dynamics of how de novo proteins emerge from potentially toxic raw materials and what influences their long-term survival are unknown. Here, using transcriptomic data from human and five other primates, we generate a set of transcribed human ORFs at six conservation levels to investigate which properties influence the early emergence and long-term retention of these expressed ORFs. As these taxa diverged from each other relatively recently, we present a fine scale view of the evolution of novel sequences over recent evolutionary time. We find that novel human-restricted ORFs are preferentially located on GC-rich gene-dense chromosomes, suggesting their retention is linked to pre-existing genes. Sequence properties such as intrinsic structural disorder and aggregation propensity—which have been proposed to play a role in survival of de novo genes—remain unchanged over time. Even very young sequences code for proteins with low aggregation propensities, suggesting that genomic regions with many novel transcribed ORFs are concomitantly less likely to produce ORFs which code for harmful toxic proteins. Our data indicate that the survival of these novel ORFs is largely stochastic rather than shaped by selection.
Schmitz, Jonathan F.; Chain, Frédéric J. J.; Bornberg-Bauer, Erich
Evolution of novel genes in three-spined stickleback populations Journal Article
In: Heredity, vol. 125, pp. 50-59, 2020.
@article{Schmitz2020,
title = {Evolution of novel genes in three-spined stickleback populations},
author = {Jonathan F. Schmitz and Frédéric J. J. Chain and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Schmitz2020.pdf, Download},
doi = {0.1038/s41437-020-0319-7},
year = {2020},
date = {2020-06-04},
journal = {Heredity},
volume = {125},
pages = {50-59},
abstract = {Eukaryotic genomes frequently acquire new protein-coding genes which may significantly impact an organism’s fitness. Novel genes can be created, for example, by duplication of large genomic regions or de novo, from previously non-coding DNA. Either way, creation of a novel transcript is an essential early step during novel gene emergence. Most studies on the gain-and-loss dynamics of novel genes so far have compared genomes between species, constraining analyses to genes that have remained fixed over long time scales. However, the importance of novel genes for rapid adaptation among populations has recently been shown. Therefore, since little is known about the evolutionary dynamics of transcripts across natural populations, we here study transcriptomes from several tissues and nine geographically distinct populations of an ecological model species, the three-spined stickleback. Our findings suggest that novel genes typically start out as transcripts with low expression and high tissue specificity. Early expression regulation appears to be mediated by gene-body methylation. Although most new and narrowly expressed genes are rapidly lost, those that survive and subsequently spread through populations tend to gain broader and higher expression levels. The properties of the encoded proteins, such as disorder and aggregation propensity, hardly change. Correspondingly, young novel genes are not preferentially under positive selection but older novel genes more often overlap with FST outlier regions. Taken together, expression of the surviving novel genes is rapidly regulated, probably via epigenetic mechanisms, while structural properties of encoded proteins are non-debilitating and might only change much later.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Eukaryotic genomes frequently acquire new protein-coding genes which may significantly impact an organism’s fitness. Novel genes can be created, for example, by duplication of large genomic regions or de novo, from previously non-coding DNA. Either way, creation of a novel transcript is an essential early step during novel gene emergence. Most studies on the gain-and-loss dynamics of novel genes so far have compared genomes between species, constraining analyses to genes that have remained fixed over long time scales. However, the importance of novel genes for rapid adaptation among populations has recently been shown. Therefore, since little is known about the evolutionary dynamics of transcripts across natural populations, we here study transcriptomes from several tissues and nine geographically distinct populations of an ecological model species, the three-spined stickleback. Our findings suggest that novel genes typically start out as transcripts with low expression and high tissue specificity. Early expression regulation appears to be mediated by gene-body methylation. Although most new and narrowly expressed genes are rapidly lost, those that survive and subsequently spread through populations tend to gain broader and higher expression levels. The properties of the encoded proteins, such as disorder and aggregation propensity, hardly change. Correspondingly, young novel genes are not preferentially under positive selection but older novel genes more often overlap with FST outlier regions. Taken together, expression of the surviving novel genes is rapidly regulated, probably via epigenetic mechanisms, while structural properties of encoded proteins are non-debilitating and might only change much later.
Grandchamp, Anna; Monget, Philippe
The membrane receptors that appeared before their ligand: The different proposed scenarios Journal Article
In: Plos One, vol. 15, no. 5, pp. e0231813, 2020.
@article{nokey,
title = {The membrane receptors that appeared before their ligand: The different proposed scenarios},
author = {Anna Grandchamp and Philippe Monget},
editor = {Plos One},
year = {2020},
date = {2020-05-22},
urldate = {2020-05-22},
journal = {Plos One},
volume = {15},
number = {5},
pages = {e0231813},
abstract = {The interactions between membrane receptors and their endogenous ligands are key interactions in organisms. Recently, we have shown that a high number of genes encoding human receptors appeared at the same moment as their ligand in the animal tree of life. However, a set of receptors appeared before their present ligand. Different scenarios have been proposed to explain how a receptor can be conserved if its ligand is not yet appeared. However, these scenarios have been proposed individually and have never been studied in a global way. In this study, we investigated 30 mammalian pairs of ligand/receptor for which the first ligand appeared after its receptor in the tree of life, by using common indexes of selection, and proposed different scenarios explaining the earlier appearance of a receptor relative to its ligand. Based on 3D structural studies, our indexes allowed us to classify the evolution of these partners into different scenarios: 1) a scenario where the binding interface of the receptor is already present and under purifying selection before the appearance of the ligand; 2) a scenario where the binding interface seems to have appeared progressively, and 3) a scenario where the binding site seems to have been reshuffled since its appearance. As some scenarios were confirmed by the literature, we concluded that simple indexes can give a good highlight of the evolutive history of two partners that did not appear at the same time. Based on these scenarios, we also hypothesize that the replacement of a ligand by another is a frequent phenomenon during evolution.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The interactions between membrane receptors and their endogenous ligands are key interactions in organisms. Recently, we have shown that a high number of genes encoding human receptors appeared at the same moment as their ligand in the animal tree of life. However, a set of receptors appeared before their present ligand. Different scenarios have been proposed to explain how a receptor can be conserved if its ligand is not yet appeared. However, these scenarios have been proposed individually and have never been studied in a global way. In this study, we investigated 30 mammalian pairs of ligand/receptor for which the first ligand appeared after its receptor in the tree of life, by using common indexes of selection, and proposed different scenarios explaining the earlier appearance of a receptor relative to its ligand. Based on 3D structural studies, our indexes allowed us to classify the evolution of these partners into different scenarios: 1) a scenario where the binding interface of the receptor is already present and under purifying selection before the appearance of the ligand; 2) a scenario where the binding interface seems to have appeared progressively, and 3) a scenario where the binding site seems to have been reshuffled since its appearance. As some scenarios were confirmed by the literature, we concluded that simple indexes can give a good highlight of the evolutive history of two partners that did not appear at the same time. Based on these scenarios, we also hypothesize that the replacement of a ligand by another is a frequent phenomenon during evolution.
Oeyen, Jan Philip; Baa-Puyoulet, Patrice; Benoit, Joshua B; Beukeboom, Leo W; Bornberg-Bauer, Erich; Buttstedt, Anja; Calevro, Federica; Cash, Elizabeth I; Chao, Hsu; Charles, Hubert; Chen, Mei-Ju May; Childers, Christopher; Cridge, Andrew G; Dearden, Peter; Dinh, Huyen; Doddapaneni, Harsha Vardhan; Dolan, Amanda; Donath, Alexander; Dowling, Daniel; Dugan, Shannon; Duncan, Elizabeth; Elpidina, Elena N; Friedrich, Markus; Geuverink, Elzemiek; Gibson, Joshua D; Grath, Sonja; Grimmelikhuijzen, Cornelis J P; Große-Wilde, Ewald; Gudobba, Cameron; Han, Yi; Hansson, Bill S; Hauser, Frank; Hughes, Daniel S T; Ioannidis, Panagiotis; Jacquin-Joly, Emmanuelle; Jennings, Emily C; Jones, Jeffery W; Klasberg, Steffen; Lee, Sandra L; Lesný, Peter; Lovegrove, Mackenzie; Martin, Sebastian; Martynov, Alexander G; Mayer, Christoph; Montagné, Nicolas; Moris, Victoria C; Munoz-Torres, Monica; Murali, Shwetha Canchi; Muzny, Donna M; Oppert, Brenda; Parisot, Nicolas; Pauli, Thomas; Peters, Ralph S; Petersen, Malte; Pick, Christian; Persyn, Emma; Podsiadlowski, Lars; Poelchau, Monica F; Provataris, Panagiotis; Qu, Jiaxin; Reijnders, Maarten J M F; Reumont, Björn Marcus; Rosendale, Andrew J; Simao, Felipe A; Skelly, John; Sotiropoulos, Alexandros G; Stahl, Aaron L; Sumitani, Megumi; Szuter, Elise M; Tidswell, Olivia; Tsitlakidis, Evangelos; Vedder, Lucia; Waterhouse, Robert M; Werren, John H; Wilbrandt, Jeanne; Worley, Kim C; Yamamoto, Daisuke S; Zande, Louis; Zdobnov, Evgeny M; Ziesmann, Tanja; Gibbs, Richard A; Richards, Stephen; Hatakeyama, Masatsugu; Misof, Bernhard; Niehuis, Oliver
Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera Journal Article
In: Genome Biology and Evolution, vol. 12, no. 7, pp. 1099–1188, 2020.
@article{Oeyen2020,
title = {Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera},
author = {Jan Philip Oeyen and Patrice Baa-Puyoulet and Joshua B Benoit and Leo W Beukeboom and Erich Bornberg-Bauer and Anja Buttstedt and Federica Calevro and Elizabeth I Cash and Hsu Chao and Hubert Charles and Mei-Ju May Chen and Christopher Childers and Andrew G Cridge and Peter Dearden and Huyen Dinh and Harsha Vardhan Doddapaneni and Amanda Dolan and Alexander Donath and Daniel Dowling and Shannon Dugan and Elizabeth Duncan and Elena N Elpidina and Markus Friedrich and Elzemiek Geuverink and Joshua D Gibson and Sonja Grath and Cornelis J P Grimmelikhuijzen and Ewald Große-Wilde and Cameron Gudobba and Yi Han and Bill S Hansson and Frank Hauser and Daniel S T Hughes and Panagiotis Ioannidis and Emmanuelle Jacquin-Joly and Emily C Jennings and Jeffery W Jones and Steffen Klasberg and Sandra L Lee and Peter Lesný and Mackenzie Lovegrove and Sebastian Martin and Alexander G Martynov and Christoph Mayer and Nicolas Montagné and Victoria C Moris and Monica Munoz-Torres and Shwetha Canchi Murali and Donna M Muzny and Brenda Oppert and Nicolas Parisot and Thomas Pauli and Ralph S Peters and Malte Petersen and Christian Pick and Emma Persyn and Lars Podsiadlowski and Monica F Poelchau and Panagiotis Provataris and Jiaxin Qu and Maarten J M F Reijnders and Björn Marcus Reumont and Andrew J Rosendale and Felipe A Simao and John Skelly and Alexandros G Sotiropoulos and Aaron L Stahl and Megumi Sumitani and Elise M Szuter and Olivia Tidswell and Evangelos Tsitlakidis and Lucia Vedder and Robert M Waterhouse and John H Werren and Jeanne Wilbrandt and Kim C Worley and Daisuke S Yamamoto and Louis Zande and Evgeny M Zdobnov and Tanja Ziesmann and Richard A Gibbs and Stephen Richards and Masatsugu Hatakeyama and Bernhard Misof and Oliver Niehuis},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Oeyen2020.pdf, Download},
doi = {10.1093/gbe/evaa106},
year = {2020},
date = {2020-05-22},
journal = {Genome Biology and Evolution},
volume = {12},
number = {7},
pages = {1099–1188},
abstract = {The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.
Heames, Brennen; Schmitz, Jonathan F.; Bornberg-Bauer, Erich
A Continuum of Evolving De Novo Genes Drives Protein‑Coding Novelty in Drosophila Journal Article
In: Journal of Molecular Evolution, vol. 88, pp. 382–398, 2020.
@article{Heames2020,
title = {A Continuum of Evolving De Novo Genes Drives Protein‑Coding Novelty in Drosophila},
author = {Brennen Heames and Jonathan F. Schmitz and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Heames2020.pdf, Download},
doi = {10.1007/s00239-020-09939-z},
year = {2020},
date = {2020-04-07},
journal = {Journal of Molecular Evolution},
volume = {88},
pages = {382–398},
abstract = {Orphan genes, lacking detectable homologs in outgroup species, typically represent 10–30% of eukaryotic genomes. Efforts to find the source of these young genes indicate that de novo emergence from non-coding DNA may in part explain their prevalence. Here, we investigate the roots of orphan gene emergence in the Drosophila genus. Across the annotated proteomes of twelve species, we find 6297 orphan genes within 4953 taxon-specific clusters of orthologs. By inferring the ancestral DNA as non-coding for between 550 and 2467 (8.7–39.2%) of these genes, we describe for the first time how de novo emergence contributes to the abundance of clade-specific Drosophila genes. In support of them having functional roles, we show that de novo genes have robust expression and translational support. However, the distinct nucleotide sequences of de novo genes, which have characteristics intermediate between intergenic regions and conserved genes, reflect their recent birth from non-coding DNA. We find that de novo genes encode more disordered proteins than both older genes and intergenic regions. Together, our results suggest that gene emergence from non-coding DNA provides an abundant source of material for the evolution of new proteins. Following gene birth, gradual evolution over large evolutionary timescales moulds sequence properties towards those of conserved genes, resulting in a continuum of properties whose starting points depend on the nucleotide sequences of an initial pool of novel genes.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Orphan genes, lacking detectable homologs in outgroup species, typically represent 10–30% of eukaryotic genomes. Efforts to find the source of these young genes indicate that de novo emergence from non-coding DNA may in part explain their prevalence. Here, we investigate the roots of orphan gene emergence in the Drosophila genus. Across the annotated proteomes of twelve species, we find 6297 orphan genes within 4953 taxon-specific clusters of orthologs. By inferring the ancestral DNA as non-coding for between 550 and 2467 (8.7–39.2%) of these genes, we describe for the first time how de novo emergence contributes to the abundance of clade-specific Drosophila genes. In support of them having functional roles, we show that de novo genes have robust expression and translational support. However, the distinct nucleotide sequences of de novo genes, which have characteristics intermediate between intergenic regions and conserved genes, reflect their recent birth from non-coding DNA. We find that de novo genes encode more disordered proteins than both older genes and intergenic regions. Together, our results suggest that gene emergence from non-coding DNA provides an abundant source of material for the evolution of new proteins. Following gene birth, gradual evolution over large evolutionary timescales moulds sequence properties towards those of conserved genes, resulting in a continuum of properties whose starting points depend on the nucleotide sequences of an initial pool of novel genes.
Gstöttl, Claudia; Stoldt, Marah; Jongepier, Evelien; Bornberg-Bauer, Erich; Feldmeyer, Barbara; Heinze, Jürgen; Foitzik, Susanne
Comparative analyses of caste, sex, and developmental stage‐specific transcriptomes in two Temnothorax ants Journal Article
In: Ecology and Evolution, vol. 10, no. 10, pp. 4193-4203, 2020.
@article{Gstöttl2020,
title = {Comparative analyses of caste, sex, and developmental stage‐specific transcriptomes in two Temnothorax ants},
author = {Claudia Gstöttl and Marah Stoldt and Evelien Jongepier and Erich Bornberg-Bauer and Barbara Feldmeyer and Jürgen Heinze and Susanne Foitzik},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Gstoettl2020.pdf, Download},
doi = {10.1002/ece3.6187},
year = {2020},
date = {2020-03-30},
journal = {Ecology and Evolution},
volume = {10},
number = {10},
pages = {4193-4203},
abstract = {Social insects dominate arthropod communities worldwide due to cooperation and division of labor in their societies. This, however, makes them vulnerable to exploitation by social parasites, such as slave‐making ants. Slave‐making ant workers pillage brood from neighboring nests of related host ant species. After emergence, host workers take over all nonreproductive colony tasks, whereas slavemakers have lost the ability to care for themselves and their offspring. Here, we compared transcriptomes of different developmental stages (larvae, pupae, and adults), castes (queens and workers), and sexes of two related ant species, the slavemaker Temnothorax americanus and its host Temnothorax longispinosus. Our aim was to investigate commonalities and differences in group‐specific transcriptomes, whereupon across‐species differences possibly can be explained by their divergent lifestyles. Larvae and pupae showed the highest similarity between the two species and upregulated genes with enriched functions of translation and chitin metabolism, respectively. Workers commonly upregulated oxidation‐reduction genes, possibly indicative of their active lifestyle. Host workers, but not workers of the slavemaker, upregulated a “social behavior” gene. In slavemaker queens and workers, genes associated with the regulation of transposable elements were upregulated. Queens of both species showed transcriptomic signals of anti‐aging mechanisms, with hosts upregulating various DNA repair pathways and slavemaker queens investing in trehalose metabolism. The transcriptomes of males showed enriched functions for quite general terms realized in different genes and pathways in each species. In summary, the strong interspecific commonalities in larvae, pupae, and workers were reflected in the same enriched Gene Ontology (GO) terms. Less commonalities occurred in the transcriptomes of queens and males, which apparently utilize different pathways to achieve a long life and sperm production, respectively. We found that all analyzed groups in this study show characteristic GO terms, with similar patterns in both species.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Social insects dominate arthropod communities worldwide due to cooperation and division of labor in their societies. This, however, makes them vulnerable to exploitation by social parasites, such as slave‐making ants. Slave‐making ant workers pillage brood from neighboring nests of related host ant species. After emergence, host workers take over all nonreproductive colony tasks, whereas slavemakers have lost the ability to care for themselves and their offspring. Here, we compared transcriptomes of different developmental stages (larvae, pupae, and adults), castes (queens and workers), and sexes of two related ant species, the slavemaker Temnothorax americanus and its host Temnothorax longispinosus. Our aim was to investigate commonalities and differences in group‐specific transcriptomes, whereupon across‐species differences possibly can be explained by their divergent lifestyles. Larvae and pupae showed the highest similarity between the two species and upregulated genes with enriched functions of translation and chitin metabolism, respectively. Workers commonly upregulated oxidation‐reduction genes, possibly indicative of their active lifestyle. Host workers, but not workers of the slavemaker, upregulated a “social behavior” gene. In slavemaker queens and workers, genes associated with the regulation of transposable elements were upregulated. Queens of both species showed transcriptomic signals of anti‐aging mechanisms, with hosts upregulating various DNA repair pathways and slavemaker queens investing in trehalose metabolism. The transcriptomes of males showed enriched functions for quite general terms realized in different genes and pathways in each species. In summary, the strong interspecific commonalities in larvae, pupae, and workers were reflected in the same enriched Gene Ontology (GO) terms. Less commonalities occurred in the transcriptomes of queens and males, which apparently utilize different pathways to achieve a long life and sperm production, respectively. We found that all analyzed groups in this study show characteristic GO terms, with similar patterns in both species.
Dohmen, Elias; Klasberg, Steffen; Bornberg-Bauer, Erich; Perrey, Sören; Kemena, Carsten
The modular nature of protein evolution: domain rearrangement rates across eukaryotic life Journal Article
In: BMC Evolutionary Biology, vol. 20, no. 30, pp. 1-13, 2020.
@article{Dohmen2020,
title = {The modular nature of protein evolution: domain rearrangement rates across eukaryotic life},
author = {Elias Dohmen and Steffen Klasberg and Erich Bornberg-Bauer and Sören Perrey and Carsten Kemena},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Dohmen2020.pdf, Download},
doi = {10.1186/s12862-020-1591-0},
year = {2020},
date = {2020-02-14},
urldate = {2020-02-14},
journal = {BMC Evolutionary Biology},
volume = {20},
number = {30},
pages = {1-13},
abstract = {Background
Modularity is important for evolutionary innovation. The recombination of existing units to form larger complexes with new functionalities spares the need to create novel elements from scratch. In proteins, this principle can be observed at the level of protein domains, functional subunits which are regularly rearranged to acquire new functions.
Results
In this study we analyse the mechanisms leading to new domain arrangements in five major eukaryotic clades (vertebrates, insects, fungi, monocots and eudicots) at unprecedented depth and breadth. This allows, for the first time, to directly compare rates of rearrangements between different clades and identify both lineage specific and general patterns of evolution in the context of domain rearrangements. We analyse arrangement changes along phylogenetic trees by reconstructing ancestral domain content in combination with feasible single step events, such as fusion or fission. Using this approach we explain up to 70% of all rearrangements by tracing them back to their precursors. We find that rates in general and the ratio between these rates for a given clade in particular, are highly consistent across all clades. In agreement with previous studies, fusions are the most frequent event leading to new domain arrangements. A lineage specific pattern in fungi reveals exceptionally high loss rates compared to other clades, supporting recent studies highlighting the importance of loss for evolutionary innovation. Furthermore, our methodology allows us to link domain emergences at specific nodes in the phylogenetic tree to important functional developments, such as the origin of hair in mammals.
Conclusions
Our results demonstrate that domain rearrangements are based on a canonical set of mutational events with rates which lie within a relatively narrow and consistent range. In addition, gained knowledge about these rates provides a basis for advanced domain-based methodologies for phylogenetics and homology analysis which complement current sequence-based methods.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
Modularity is important for evolutionary innovation. The recombination of existing units to form larger complexes with new functionalities spares the need to create novel elements from scratch. In proteins, this principle can be observed at the level of protein domains, functional subunits which are regularly rearranged to acquire new functions.
Results
In this study we analyse the mechanisms leading to new domain arrangements in five major eukaryotic clades (vertebrates, insects, fungi, monocots and eudicots) at unprecedented depth and breadth. This allows, for the first time, to directly compare rates of rearrangements between different clades and identify both lineage specific and general patterns of evolution in the context of domain rearrangements. We analyse arrangement changes along phylogenetic trees by reconstructing ancestral domain content in combination with feasible single step events, such as fusion or fission. Using this approach we explain up to 70% of all rearrangements by tracing them back to their precursors. We find that rates in general and the ratio between these rates for a given clade in particular, are highly consistent across all clades. In agreement with previous studies, fusions are the most frequent event leading to new domain arrangements. A lineage specific pattern in fungi reveals exceptionally high loss rates compared to other clades, supporting recent studies highlighting the importance of loss for evolutionary innovation. Furthermore, our methodology allows us to link domain emergences at specific nodes in the phylogenetic tree to important functional developments, such as the origin of hair in mammals.
Conclusions
Our results demonstrate that domain rearrangements are based on a canonical set of mutational events with rates which lie within a relatively narrow and consistent range. In addition, gained knowledge about these rates provides a basis for advanced domain-based methodologies for phylogenetics and homology analysis which complement current sequence-based methods.
Modularity is important for evolutionary innovation. The recombination of existing units to form larger complexes with new functionalities spares the need to create novel elements from scratch. In proteins, this principle can be observed at the level of protein domains, functional subunits which are regularly rearranged to acquire new functions.
Results
In this study we analyse the mechanisms leading to new domain arrangements in five major eukaryotic clades (vertebrates, insects, fungi, monocots and eudicots) at unprecedented depth and breadth. This allows, for the first time, to directly compare rates of rearrangements between different clades and identify both lineage specific and general patterns of evolution in the context of domain rearrangements. We analyse arrangement changes along phylogenetic trees by reconstructing ancestral domain content in combination with feasible single step events, such as fusion or fission. Using this approach we explain up to 70% of all rearrangements by tracing them back to their precursors. We find that rates in general and the ratio between these rates for a given clade in particular, are highly consistent across all clades. In agreement with previous studies, fusions are the most frequent event leading to new domain arrangements. A lineage specific pattern in fungi reveals exceptionally high loss rates compared to other clades, supporting recent studies highlighting the importance of loss for evolutionary innovation. Furthermore, our methodology allows us to link domain emergences at specific nodes in the phylogenetic tree to important functional developments, such as the origin of hair in mammals.
Conclusions
Our results demonstrate that domain rearrangements are based on a canonical set of mutational events with rates which lie within a relatively narrow and consistent range. In addition, gained knowledge about these rates provides a basis for advanced domain-based methodologies for phylogenetics and homology analysis which complement current sequence-based methods.
Thomas, Gregg W. C.; Dohmen, Elias; Hughes, Daniel S. T.; Murali, Shwetha C.; Poelchau, Monica; Glastad, Karl; Anstead, Clare A.; Ayoub, Nadia A.; Batterham, Phillip; Bellair, Michelle; Binford, Gretta J.; Chao, Hsu; Chen, Yolanda H.; Childers, Christopher; Dinh, Huyen; Doddapaneni, HarshaVardhan; Duan, Jian J.; Dugan, Shannon; Esposito, Lauren A.; Friedrich, Markus; Garb, Jessica; Gasser, Robin B.; Goodisman, Michael A. D.; Gundersen-Rindal, Dawn E.; Han, Yi; Handler, Alfred M.; Hatakeyama, Masatsugu; Hering, Lars; Hunter, Wayne B.; Ioannidis, Panagiotis; Jayaseelan, Joy C.; Kalra, Divya; Khila, Abderrahman; Korhonen, Pasi K.; Lee, Carol Eunmi; Lee, Sandra L.; Li, Yiyuan; Lindsey, Amelia R. I.; Mayer, Georg; McGregor, Alistair P.; McKenna, Duane D.; Misof, Bernhard; Munidasa, Mala; Munoz-Torres, Monica; Muzny, Donna M.; Niehuis, Oliver; Osuji-Lacy, Nkechinyere; Palli, Subba R.; Panfilio, Kristen A.; Pechmann, Matthias; Perry, Trent; Peters, Ralph S.; Poynton, Helen C.; Prpic, Nikola-Michael; Qu, Jiaxin; Rotenberg, Dorith; Schal, Coby; Schoville, Sean D.; Scully, Erin D.; Skinner, Evette; Sloan, Daniel B.; Stouthamer, Richard; Strand, Michael R.; Szucsich, Nikolaus U.; Wijeratne, Asela; Young, Neil D.; Zattara, Eduardo E.; Benoit, Joshua B.; Zdobnov, Evgeny M.; Pfrender, Michael E.; Hackett, Kevin J.; Werren, John H.; Worley, Kim C.; Gibbs, Richard A.; Chipman, Ariel D.; Waterhouse, Robert M.; Bornberg-Bauer, Erich; Hahn, Matthew W.; Richards, Stephen
Gene content evolution in the arthropods Journal Article
In: Genome Biology, vol. 21, no. 15, pp. 1-14, 2020.
@article{Thomas2020,
title = {Gene content evolution in the arthropods},
author = {Gregg W. C. Thomas and Elias Dohmen and Daniel S. T. Hughes and Shwetha C. Murali and Monica Poelchau and Karl Glastad and Clare A. Anstead and Nadia A. Ayoub and Phillip Batterham and Michelle Bellair and Gretta J. Binford and Hsu Chao and Yolanda H. Chen and Christopher Childers and Huyen Dinh and HarshaVardhan Doddapaneni and Jian J. Duan and Shannon Dugan and Lauren A. Esposito and Markus Friedrich and Jessica Garb and Robin B. Gasser and Michael A. D. Goodisman and Dawn E. Gundersen-Rindal and Yi Han and Alfred M. Handler and Masatsugu Hatakeyama and Lars Hering and Wayne B. Hunter and Panagiotis Ioannidis and Joy C. Jayaseelan and Divya Kalra and Abderrahman Khila and Pasi K. Korhonen and Carol Eunmi Lee and Sandra L. Lee and Yiyuan Li and Amelia R. I. Lindsey and Georg Mayer and Alistair P. McGregor and Duane D. McKenna and Bernhard Misof and Mala Munidasa and Monica Munoz-Torres and Donna M. Muzny and Oliver Niehuis and Nkechinyere Osuji-Lacy and Subba R. Palli and Kristen A. Panfilio and Matthias Pechmann and Trent Perry and Ralph S. Peters and Helen C. Poynton and Nikola-Michael Prpic and Jiaxin Qu and Dorith Rotenberg and Coby Schal and Sean D. Schoville and Erin D. Scully and Evette Skinner and Daniel B. Sloan and Richard Stouthamer and Michael R. Strand and Nikolaus U. Szucsich and Asela Wijeratne and Neil D. Young and Eduardo E. Zattara and Joshua B. Benoit and Evgeny M. Zdobnov and Michael E. Pfrender and Kevin J. Hackett and John H. Werren and Kim C. Worley and Richard A. Gibbs and Ariel D. Chipman and Robert M. Waterhouse and Erich Bornberg-Bauer and Matthew W. Hahn and Stephen Richards},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Thomas2020.pdf, Download https://www.uni-muenster.de/news/view.php?cmdid=10785&lang=en, WWU press release
https://www.sib.swiss/about-sib/news/10635-unravelling-arthropod-genomic-diversity-over-500-million-years-of-evolution, SIB press release with video
https://www.laborpraxis.vogel.de/innovation-liegt-in-den-genen-a-1081485/, Interview with Elias Dohmen (in German)
https://facultyopinions.com/prime/737249072, F1000 Faculty Opinions Recommendation},
doi = {https://doi.org/10.1186/s13059-019-1925-7},
year = {2020},
date = {2020-01-23},
urldate = {2020-01-23},
journal = {Genome Biology},
volume = {21},
number = {15},
pages = {1-14},
abstract = {Background
Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods.
Results
Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception.
Conclusions
These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods.
Results
Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception.
Conclusions
These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.
Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods.
Results
Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception.
Conclusions
These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.
2019
Loo, Bert; Heberlein, Magdalena; Mair, Philip; Zinchenko, Anastasia; Schüürmann, Jan; Eenink, Bernard D. G.; Holstein, Josephin M.; Dilkaute, Carina; Jose, Joachim; Hollfelder, Florian; Bornberg-Bauer, Erich
High-Throughput, Lysis-Free Screening for Sulfatase Activity Using Escherichia coli Autodisplay in Microdroplets Journal Article
In: ACS synthetic biology, vol. 8, no. 12, pp. 2690-2700, 2019.
@article{vanLoo2019,
title = {High-Throughput, Lysis-Free Screening for Sulfatase Activity Using Escherichia coli Autodisplay in Microdroplets},
author = {Bert Loo and Magdalena Heberlein and Philip Mair and Anastasia Zinchenko and Jan Schüürmann and Bernard D. G. Eenink and Josephin M. Holstein and Carina Dilkaute and Joachim Jose and Florian Hollfelder and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Loo2019.pdf, Download},
doi = {10.1021/acssynbio.9b00274},
year = {2019},
date = {2019-11-18},
journal = {ACS synthetic biology},
volume = {8},
number = {12},
pages = {2690-2700},
abstract = {Directed evolution of enzymes toward improved catalytic performance has become a powerful tool in protein engineering. To be effective, a directed evolution campaign requires the use of high-throughput screening. In this study we describe the development of an ultra high-throughput lysis-free procedure to screen for improved sulfatase activity by combining microdroplet-based single-variant activity sorting with E. coli autodisplay. For the first step in a 4-step screening procedure, we quantitatively screened >105 variants of the homodimeric arylsulfatase from Silicibacter pomeroyi (SpAS1), displayed on the E. coli cell surface, for improved sulfatase activity using fluorescence activated droplet sorting. Compartmentalization of the fluorescent reaction product with living E. coli cells autodisplaying the sulfatase variants ensured the continuous linkage of genotype and phenotype during droplet sorting and allowed for direct recovery by simple regrowth of the sorted cells. The use of autodisplay on living cells simplified and reduced the degree of liquid handling during all steps in the screening procedure to the single event of simply mixing substrate and cells. The percentage of apparent improved variants was enriched >10-fold as a result of droplet sorting. We ultimately identified 25 SpAS1 variants with improved performance toward 4-nitrophenyl sulfate (up to 6.2-fold) and/or fluorescein disulfate (up to 30-fold). In SpAS1 variants with improved performance toward the bulky fluorescein disulfate, many of the beneficial mutations occur in residues that form hydrogen bonds between α-helices in the C-terminal oligomerization region, suggesting a previously unknown role for the dimer interface in shaping the substrate binding site of SpAS1.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Directed evolution of enzymes toward improved catalytic performance has become a powerful tool in protein engineering. To be effective, a directed evolution campaign requires the use of high-throughput screening. In this study we describe the development of an ultra high-throughput lysis-free procedure to screen for improved sulfatase activity by combining microdroplet-based single-variant activity sorting with E. coli autodisplay. For the first step in a 4-step screening procedure, we quantitatively screened >105 variants of the homodimeric arylsulfatase from Silicibacter pomeroyi (SpAS1), displayed on the E. coli cell surface, for improved sulfatase activity using fluorescence activated droplet sorting. Compartmentalization of the fluorescent reaction product with living E. coli cells autodisplaying the sulfatase variants ensured the continuous linkage of genotype and phenotype during droplet sorting and allowed for direct recovery by simple regrowth of the sorted cells. The use of autodisplay on living cells simplified and reduced the degree of liquid handling during all steps in the screening procedure to the single event of simply mixing substrate and cells. The percentage of apparent improved variants was enriched >10-fold as a result of droplet sorting. We ultimately identified 25 SpAS1 variants with improved performance toward 4-nitrophenyl sulfate (up to 6.2-fold) and/or fluorescein disulfate (up to 30-fold). In SpAS1 variants with improved performance toward the bulky fluorescein disulfate, many of the beneficial mutations occur in residues that form hydrogen bonds between α-helices in the C-terminal oligomerization region, suggesting a previously unknown role for the dimer interface in shaping the substrate binding site of SpAS1.
Kleppe, April Snofrid; Bornberg-Bauer, Erich
Translational readthrough goes unseen by natural selection Journal Article Forthcoming
In: Forthcoming.
@article{Kleppe2019,
title = {Translational readthrough goes unseen by natural selection},
author = {April Snofrid Kleppe and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/10/kleppe2019.pdf, Download},
doi = {10.1101/844621},
year = {2019},
date = {2019-11-15},
urldate = {2019-11-15},
abstract = {Occasionally during protein synthesis, the ribosome bypasses the stop codon and
continues translation to the next stop codon in frame. This error is called translational
readthrough (TR). Earlier research suggest that TR is a relatively common error, in
several taxa, yet the evolutionary relevance of this translational error is still unclear. By
analysing ribosome profiling data, we have conducted species comparisons between
yeasts to infer conservation of TR between orthologs. Moreover, we infer the
evolutionary rate of error prone and canonically translated proteins to deduct
differential selective pressure. We find that about 40% of error prone proteins in
Schizosaccharomyces pombe do not have any orthologs in Saccharomyces cerevisiae, but
that 60% of error prone proteins in S. pombe are undergoing canonical translation in S.
cerevisiae. Error prone proteins tend to have a higher GC-content in the 3'-UTR, unlike
their canonically translated ortholog. We do not find the same trends for GC-content of
the CDS. We discuss the role of 3'-UTR and GC-content regarding translational
readthrough. Moreover, we find that there is neither selective pressure against or for TR.
We suggest that TR is a near-neutral error that goes unseen by natural selection. We
speculate that TR yield neutral protein isoforms that are not being purged. We suggest
that isoforms, yielded by TR, increase proteomic diversity in the cell, which is readily
available upon sudden environmental shifts and which therefore may become adaptive.},
keywords = {},
pubstate = {forthcoming},
tppubtype = {article}
}
Occasionally during protein synthesis, the ribosome bypasses the stop codon and
continues translation to the next stop codon in frame. This error is called translational
readthrough (TR). Earlier research suggest that TR is a relatively common error, in
several taxa, yet the evolutionary relevance of this translational error is still unclear. By
analysing ribosome profiling data, we have conducted species comparisons between
yeasts to infer conservation of TR between orthologs. Moreover, we infer the
evolutionary rate of error prone and canonically translated proteins to deduct
differential selective pressure. We find that about 40% of error prone proteins in
Schizosaccharomyces pombe do not have any orthologs in Saccharomyces cerevisiae, but
that 60% of error prone proteins in S. pombe are undergoing canonical translation in S.
cerevisiae. Error prone proteins tend to have a higher GC-content in the 3'-UTR, unlike
their canonically translated ortholog. We do not find the same trends for GC-content of
the CDS. We discuss the role of 3'-UTR and GC-content regarding translational
readthrough. Moreover, we find that there is neither selective pressure against or for TR.
We suggest that TR is a near-neutral error that goes unseen by natural selection. We
speculate that TR yield neutral protein isoforms that are not being purged. We suggest
that isoforms, yielded by TR, increase proteomic diversity in the cell, which is readily
available upon sudden environmental shifts and which therefore may become adaptive.
continues translation to the next stop codon in frame. This error is called translational
readthrough (TR). Earlier research suggest that TR is a relatively common error, in
several taxa, yet the evolutionary relevance of this translational error is still unclear. By
analysing ribosome profiling data, we have conducted species comparisons between
yeasts to infer conservation of TR between orthologs. Moreover, we infer the
evolutionary rate of error prone and canonically translated proteins to deduct
differential selective pressure. We find that about 40% of error prone proteins in
Schizosaccharomyces pombe do not have any orthologs in Saccharomyces cerevisiae, but
that 60% of error prone proteins in S. pombe are undergoing canonical translation in S.
cerevisiae. Error prone proteins tend to have a higher GC-content in the 3'-UTR, unlike
their canonically translated ortholog. We do not find the same trends for GC-content of
the CDS. We discuss the role of 3'-UTR and GC-content regarding translational
readthrough. Moreover, we find that there is neither selective pressure against or for TR.
We suggest that TR is a near-neutral error that goes unseen by natural selection. We
speculate that TR yield neutral protein isoforms that are not being purged. We suggest
that isoforms, yielded by TR, increase proteomic diversity in the cell, which is readily
available upon sudden environmental shifts and which therefore may become adaptive.
Yang, Gloria; Anderson, Dave W; Baier, Florian; Dohmen, Elias; Hong, Nansook; Carr, Paul D; Kamerlin, Shina Caroline Lynn; Jackson, Colin J; Bornberg-Bauer, Erich; Tokuriki, Nobuhiko
Higher-order epistasis shapes the fitness landscape of a xenobiotic-degrading enzyme Journal Article
In: Nature Chemical Biology, vol. 15, pp. pages1120–1128, 2019.
@article{Yang2019,
title = {Higher-order epistasis shapes the fitness landscape of a xenobiotic-degrading enzyme},
author = {Gloria Yang and Dave W Anderson and Florian Baier and Elias Dohmen and Nansook Hong and Paul D Carr and Shina Caroline Lynn Kamerlin and Colin J Jackson and Erich Bornberg-Bauer and Nobuhiko Tokuriki},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Yang2019.pdf, Download
https://www.hfsp.org/hfsp-news-events/travel-time-back-roots-how-bacteria-learned-live-poison, HFSP - Travel in time: bacteria learn to live on poison https://www.uni-muenster.de/news/view.php?cmdid=10589&lang=en, WWU Münster press release
https://www.laborpraxis.vogel.de/innovation-liegt-in-den-genen-a-1081485/, Interview with Elias Dohmen (in German) https://facultyopinions.com/prime/736779419#tab=recommendations, F1000 Faculty Opinions Recommendation},
doi = {10.1038/s41589-019-0386-3},
year = {2019},
date = {2019-10-21},
urldate = {2019-10-21},
journal = {Nature Chemical Biology},
volume = {15},
pages = {pages1120–1128},
abstract = {Characterizing the adaptive landscapes that encompass the emergence of novel enzyme functions can provide molecular insights into both enzymatic and evolutionary mechanisms. Here, we combine ancestral protein reconstruction with biochemical, structural and mutational analyses to characterize the functional evolution of methyl-parathion hydrolase (MPH), an organophosphate-degrading enzyme. We identify five mutations that are necessary and sufficient for the evolution of MPH from an ancestral dihydrocoumarin hydrolase. In-depth analyses of the adaptive landscapes encompassing this evolutionary transition revealed that the mutations form a complex interaction network, defined in part by higher-order epistasis, that constrained the adaptive pathways available. By also characterizing the adaptive landscapes in terms of their functional activities towards three additional organophosphate substrates, we reveal that subtle differences in the polarity of the substrate substituents drastically alter the network of epistatic interactions. Our work suggests that the mutations function collectively to enable substrate recognition via subtle structural repositioning.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Characterizing the adaptive landscapes that encompass the emergence of novel enzyme functions can provide molecular insights into both enzymatic and evolutionary mechanisms. Here, we combine ancestral protein reconstruction with biochemical, structural and mutational analyses to characterize the functional evolution of methyl-parathion hydrolase (MPH), an organophosphate-degrading enzyme. We identify five mutations that are necessary and sufficient for the evolution of MPH from an ancestral dihydrocoumarin hydrolase. In-depth analyses of the adaptive landscapes encompassing this evolutionary transition revealed that the mutations form a complex interaction network, defined in part by higher-order epistasis, that constrained the adaptive pathways available. By also characterizing the adaptive landscapes in terms of their functional activities towards three additional organophosphate substrates, we reveal that subtle differences in the polarity of the substrate substituents drastically alter the network of epistatic interactions. Our work suggests that the mutations function collectively to enable substrate recognition via subtle structural repositioning.
Bornberg-Bauer, Erich; Heames, Brennen
Becoming a de Novo gene Journal Article
In: Nature Ecology & Evolution, 2019.
@article{Bornberg-Bauer2019,
title = {Becoming a de Novo gene},
author = {Erich Bornberg-Bauer and Brennen Heames},
url = {https://bornberglab.org/wp-content/uploads/2021/10/bornberg-bauer_heames_becoming_a_denovo_gene_120319.pdf, Download},
year = {2019},
date = {2019-10-01},
journal = {Nature Ecology & Evolution},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Hartke, Juliane; Schell, Tilman; Jongepier, Evelien; Schmidt, Hanno; Sprenger, Philipp P; Paule, Juraj; Bornberg-Bauer, Erich; Schmitt, Thomas; Menzel, Florian; Pfenninger, Markus; Feldmeyer, Barbara
Hybrid genome assembly of a neotropical mutualistic ant Journal Article
In: Genome Biology and Evolution, vol. 11, no. 8, pp. 2306–2311, 2019.
@article{Hartke2019,
title = {Hybrid genome assembly of a neotropical mutualistic ant},
author = {Juliane Hartke and Tilman Schell and Evelien Jongepier and Hanno Schmidt and Philipp P Sprenger and Juraj Paule and Erich Bornberg-Bauer and Thomas Schmitt and Florian Menzel and Markus Pfenninger and Barbara Feldmeyer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Hartke2019.pdf, Downloads},
doi = {10.1093/gbe/evz159},
year = {2019},
date = {2019-07-22},
journal = {Genome Biology and Evolution},
volume = {11},
number = {8},
pages = {2306–2311},
abstract = {The success of social insects is largely intertwined with their highly advanced chemical communication system that facilitates recognition and discrimination of species and nest-mates, recruitment, and division of labor. Hydrocarbons, which cover the cuticle of insects, not only serve as waterproofing agents but also constitute a major component of this communication system. Two cryptic Crematogaster species, which share their nest with Camponotus ants, show striking diversity in their cuticular hydrocarbon (CHC) profile. This mutualistic system therefore offers a great opportunity to study the genetic basis of CHC divergence between sister species. As a basis for further genome-wide studies high-quality genomes are needed. Here, we present the annotated draft genome for Crematogaster levior A. By combining the three most commonly used sequencing techniques—Illumina, PacBio, and Oxford Nanopore—we constructed a high-quality de novo ant genome. We show that even low coverage of long reads can add significantly to overall genome contiguity. Annotation of desaturase and elongase genes, which play a role in CHC biosynthesis revealed one of the largest repertoires in ants and a higher number of desaturases in general than in other Hymenoptera. This may provide a mechanistic explanation for the high diversity observed in C. levior CHC profiles.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The success of social insects is largely intertwined with their highly advanced chemical communication system that facilitates recognition and discrimination of species and nest-mates, recruitment, and division of labor. Hydrocarbons, which cover the cuticle of insects, not only serve as waterproofing agents but also constitute a major component of this communication system. Two cryptic Crematogaster species, which share their nest with Camponotus ants, show striking diversity in their cuticular hydrocarbon (CHC) profile. This mutualistic system therefore offers a great opportunity to study the genetic basis of CHC divergence between sister species. As a basis for further genome-wide studies high-quality genomes are needed. Here, we present the annotated draft genome for Crematogaster levior A. By combining the three most commonly used sequencing techniques—Illumina, PacBio, and Oxford Nanopore—we constructed a high-quality de novo ant genome. We show that even low coverage of long reads can add significantly to overall genome contiguity. Annotation of desaturase and elongase genes, which play a role in CHC biosynthesis revealed one of the largest repertoires in ants and a higher number of desaturases in general than in other Hymenoptera. This may provide a mechanistic explanation for the high diversity observed in C. levior CHC profiles.
Huang, Yun; Feulner, Philine G. D.; Eizaguirre, Christophe; Lenz, Tobias L; Bornberg-Bauer, Erich; Milinski, Manfred; Reusch, Thorsten B H; Chain, Frédéric J. J.
In: Genome Biology and Evolution, vol. 11, no. 8, pp. 2344–2359, 2019.
@article{Huang2019,
title = {Genome-Wide Genotype-Expression Relationships Reveal Both Copy Number and Single Nucleotide Differentiation Contribute to Differential Gene Expression between Stickleback Ecotypes},
author = {Yun Huang and Philine G. D. Feulner and Christophe Eizaguirre and Tobias L Lenz and Erich Bornberg-Bauer and Manfred Milinski and Thorsten B H Reusch and Frédéric J. J. Chain},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Huang2019.pdf, Download},
doi = {10.1093/gbe/evz148},
year = {2019},
date = {2019-07-12},
urldate = {2019-07-12},
journal = {Genome Biology and Evolution},
volume = {11},
number = {8},
pages = {2344–2359},
abstract = {Repeated and independent emergence of trait divergence that matches habitat differences is a sign of parallel evolution by natural selection. Yet, the molecular underpinnings that are targeted by adaptive evolution often remain elusive. We investigate this question by combining genome-wide analyses of copy number variants (CNVs), single nucleotide polymorphisms (SNPs), and gene expression across four pairs of lake and river populations of the three-spined stickleback (Gasterosteus aculeatus). We tested whether CNVs that span entire genes and SNPs occurring in putative cis-regulatory regions contribute to gene expression differences between sticklebacks from lake and river origins. We found 135 gene CNVs that showed a significant positive association between gene copy number and gene expression, suggesting that CNVs result in dosage effects that can fuel phenotypic variation and serve as substrates for habitat-specific selection. Copy number differentiation between lake and river sticklebacks also contributed to expression differences of two immune-related genes in immune tissues, cathepsin A and GIMAP7. In addition, we identified SNPs in cis-regulatory regions (eSNPs) associated with the expression of 1,865 genes, including one eSNP upstream of a carboxypeptidase gene where both the SNP alleles differentiated and the gene was differentially expressed between lake and river populations. Our study highlights two types of mutations as important sources of genetic variation involved in the evolution of gene expression and in potentially facilitating repeated adaptation to novel environments.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Repeated and independent emergence of trait divergence that matches habitat differences is a sign of parallel evolution by natural selection. Yet, the molecular underpinnings that are targeted by adaptive evolution often remain elusive. We investigate this question by combining genome-wide analyses of copy number variants (CNVs), single nucleotide polymorphisms (SNPs), and gene expression across four pairs of lake and river populations of the three-spined stickleback (Gasterosteus aculeatus). We tested whether CNVs that span entire genes and SNPs occurring in putative cis-regulatory regions contribute to gene expression differences between sticklebacks from lake and river origins. We found 135 gene CNVs that showed a significant positive association between gene copy number and gene expression, suggesting that CNVs result in dosage effects that can fuel phenotypic variation and serve as substrates for habitat-specific selection. Copy number differentiation between lake and river sticklebacks also contributed to expression differences of two immune-related genes in immune tissues, cathepsin A and GIMAP7. In addition, we identified SNPs in cis-regulatory regions (eSNPs) associated with the expression of 1,865 genes, including one eSNP upstream of a carboxypeptidase gene where both the SNP alleles differentiated and the gene was differentially expressed between lake and river populations. Our study highlights two types of mutations as important sources of genetic variation involved in the evolution of gene expression and in potentially facilitating repeated adaptation to novel environments.
Kemena, Carsten; Dohmen, Elias; Bornberg-Bauer, Erich
DOGMA: a web server for proteome and transcriptome quality assessment Journal Article
In: Nucleic Acids Research, vol. 47, no. W1, pp. W507–W510, 2019.
@article{Kemena2019,
title = {DOGMA: a web server for proteome and transcriptome quality assessment},
author = {Carsten Kemena and Elias Dohmen and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Kemena2019.pdf, Download},
doi = {10.1093/nar/gkz366},
year = {2019},
date = {2019-05-11},
journal = {Nucleic Acids Research},
volume = {47},
number = {W1},
pages = {W507–W510},
abstract = {Even in the era of next generation sequencing, in which bioinformatics tools abound, annotating transcriptomes and proteomes remains a challenge. This can have major implications for the reliability of studies based on these datasets. Therefore, quality assessment represents a crucial step prior to downstream analyses on novel transcriptomes and proteomes. DOGMA allows such a quality assessment to be carried out. The data of interest are evaluated based on a comparison with a core set of conserved protein domains and domain arrangements. Depending on the studied species, DOGMA offers precomputed core sets for different phylogenetic clades. We now developed a web server for the DOGMA software, offering a user-friendly, simple to use interface. Additionally, the server provides a graphical representation of the analysis results and their placement in comparison to publicly available data. The server is freely available under https://domainworld-services.uni-muenster.de/dogma/. Additionally, for large scale analyses the software can be downloaded free of charge from https://domainworld.uni-muenster.de.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Even in the era of next generation sequencing, in which bioinformatics tools abound, annotating transcriptomes and proteomes remains a challenge. This can have major implications for the reliability of studies based on these datasets. Therefore, quality assessment represents a crucial step prior to downstream analyses on novel transcriptomes and proteomes. DOGMA allows such a quality assessment to be carried out. The data of interest are evaluated based on a comparison with a core set of conserved protein domains and domain arrangements. Depending on the studied species, DOGMA offers precomputed core sets for different phylogenetic clades. We now developed a web server for the DOGMA software, offering a user-friendly, simple to use interface. Additionally, the server provides a graphical representation of the analysis results and their placement in comparison to publicly available data. The server is freely available under https://domainworld-services.uni-muenster.de/dogma/. Additionally, for large scale analyses the software can be downloaded free of charge from https://domainworld.uni-muenster.de.
Kaur, Rajbir; Stoldt, Marah; Jongepier, Evelien; Feldmeyer, Barbara; Menzel, Florian; Bornberg-Bauer, Erich; Foitzik, Susanne
Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite Journal Article
In: Philosophical Transactions of the Royal Society B, vol. 374, no. 1769, 2019.
@article{Kaur2019,
title = {Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite},
author = {Rajbir Kaur and Marah Stoldt and Evelien Jongepier and Barbara Feldmeyer and Florian Menzel and Erich Bornberg-Bauer and Susanne Foitzik},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Kaur2019.pdf, Download},
doi = {10.1098/rstb.2018.0192},
year = {2019},
date = {2019-02-11},
journal = {Philosophical Transactions of the Royal Society B},
volume = {374},
number = {1769},
abstract = {The geographical mosaic theory of coevolution predicts that species interactions vary between locales. Depending on who leads the coevolutionary arms race, the effectivity of parasite attack or host defence strategies will explain parasite prevalence. Here, we compare behaviour and brain transcriptomes of Temnothorax longispinosus ant workers when defending their nest against an invading social parasite, the slavemaking ant Temnothorax americanus. A full-factorial design allowed us to test whether behaviour and gene expression are linked to parasite pressure on host populations or to the ecological success of parasite populations. Albeit host defences had been shown before to covary with local parasite pressure, we found parasite success to be much more important. Our chemical and behavioural analyses revealed that parasites from high prevalence sites carry lower concentrations of recognition cues and are less often attacked by hosts. This link was further supported by gene expression analysis. Our study reveals that host–parasite interactions are strongly influenced by social parasite strategies, so that variation in parasite prevalence is determined by parasite traits rather than the efficacy of host defence. Gene functions associated with parasite success indicated strong neuronal responses in hosts, including long-term changes in gene regulation, indicating an enduring impact of parasites on host behaviour.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The geographical mosaic theory of coevolution predicts that species interactions vary between locales. Depending on who leads the coevolutionary arms race, the effectivity of parasite attack or host defence strategies will explain parasite prevalence. Here, we compare behaviour and brain transcriptomes of Temnothorax longispinosus ant workers when defending their nest against an invading social parasite, the slavemaking ant Temnothorax americanus. A full-factorial design allowed us to test whether behaviour and gene expression are linked to parasite pressure on host populations or to the ecological success of parasite populations. Albeit host defences had been shown before to covary with local parasite pressure, we found parasite success to be much more important. Our chemical and behavioural analyses revealed that parasites from high prevalence sites carry lower concentrations of recognition cues and are less often attacked by hosts. This link was further supported by gene expression analysis. Our study reveals that host–parasite interactions are strongly influenced by social parasite strategies, so that variation in parasite prevalence is determined by parasite traits rather than the efficacy of host defence. Gene functions associated with parasite success indicated strong neuronal responses in hosts, including long-term changes in gene regulation, indicating an enduring impact of parasites on host behaviour.
2018
Kurafeiski, Jasmin D; Pinto, Paulo; Bornberg-Bauer, Erich
Evolutionary Potential of Cis-Regulatory Mutations to Cause Rapid Changes in Transcription Factor Binding Journal Article
In: Genome Biology and Evolution, vol. 11, no. 2, pp. 406–414, 2018.
@article{Kurafeiski2018,
title = {Evolutionary Potential of Cis-Regulatory Mutations to Cause Rapid Changes in Transcription Factor Binding},
author = {Jasmin D Kurafeiski and Paulo Pinto and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Kurafeiski2019.pdf, Download},
doi = {10.1093/gbe/evy269},
year = {2018},
date = {2018-12-28},
urldate = {2018-12-28},
journal = {Genome Biology and Evolution},
volume = {11},
number = {2},
pages = {406–414},
abstract = {Transcriptional regulation is crucial for all biological processes and well investigated at the molecular level for a wide range of organisms. However, it is quite unclear how innovations, such as the activity of a novel regulatory element, evolve. In the case of transcription factor (TF) binding, both a novel TF and a novel-binding site would need to evolve concertedly. Since promiscuous functions have recently been identified as important intermediate steps in creating novel specific functions in many areas such as enzyme evolution and protein–protein interactions, we ask here how promiscuous binding of TFs to TF-binding sites (TFBSs) affects the robustness and evolvability of this tightly regulated system. Specifically, we investigate the binding behavior of several hundred TFs from different species at unprecedented breadth. Our results illustrate multiple aspects of TF-binding interactions, ranging from correlations between the strength of the interaction bond and specificity, to preferences regarding TFBS nucleotide composition in relation to both domains and binding specificity. We identified a subset of high A/T binding motifs. Motifs in this subset had many functionally neutral one-error mutants, and were bound by multiple different binding domains. Our results indicate that, especially for some TF–TFBS associations, low binding specificity confers high degrees of evolvability, that is that few mutations facilitate rapid changes in transcriptional regulation, in particular for large and old TF families. In this study we identify binding motifs exhibiting behavior indicating high evolutionary potential for innovations in transcriptional regulation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Transcriptional regulation is crucial for all biological processes and well investigated at the molecular level for a wide range of organisms. However, it is quite unclear how innovations, such as the activity of a novel regulatory element, evolve. In the case of transcription factor (TF) binding, both a novel TF and a novel-binding site would need to evolve concertedly. Since promiscuous functions have recently been identified as important intermediate steps in creating novel specific functions in many areas such as enzyme evolution and protein–protein interactions, we ask here how promiscuous binding of TFs to TF-binding sites (TFBSs) affects the robustness and evolvability of this tightly regulated system. Specifically, we investigate the binding behavior of several hundred TFs from different species at unprecedented breadth. Our results illustrate multiple aspects of TF-binding interactions, ranging from correlations between the strength of the interaction bond and specificity, to preferences regarding TFBS nucleotide composition in relation to both domains and binding specificity. We identified a subset of high A/T binding motifs. Motifs in this subset had many functionally neutral one-error mutants, and were bound by multiple different binding domains. Our results indicate that, especially for some TF–TFBS associations, low binding specificity confers high degrees of evolvability, that is that few mutations facilitate rapid changes in transcriptional regulation, in particular for large and old TF families. In this study we identify binding motifs exhibiting behavior indicating high evolutionary potential for innovations in transcriptional regulation.
Kleppe, April Snofrid; Bornberg-Bauer, Erich
Robustness by intrinsically disordered C-termini and translational readthrough Journal Article
In: Nucleic Acids Research, vol. 46, no. 19, pp. 10184–10194, 2018.
@article{Kleppe2018,
title = {Robustness by intrinsically disordered C-termini and translational readthrough},
author = {April Snofrid Kleppe and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Kleppe2018.pdf, Download},
doi = {10.1093/nar/gky778},
year = {2018},
date = {2018-09-22},
journal = {Nucleic Acids Research},
volume = {46},
number = {19},
pages = {10184–10194},
abstract = {During protein synthesis genetic instructions are passed from DNA via mRNA to the ribosome to assemble a protein chain. Occasionally, stop codons in the mRNA are bypassed and translation continues into the untranslated region (3′-UTR). This process, called translational readthrough (TR), yields a protein chain that becomes longer than would be predicted from the DNA sequence alone. Protein sequences vary in propensity for translational errors, which may yield evolutionary constraints by limiting evolutionary paths. Here we investigated TR in Saccharomyces cerevisiae by analysing ribosome profiling data. We clustered proteins as either prone or non-prone to TR, and conducted comparative analyses. We find that a relatively high frequency (5%) of genes undergo TR, including ribosomal subunit proteins. Our main finding is that proteins undergoing TR are highly expressed and have a higher proportion of intrinsically disordered C-termini. We suggest that highly expressed proteins may compensate for the deleterious effects of TR by having intrinsically disordered C-termini, which may provide conformational flexibility but without distorting native function. Moreover, we discuss whether minimizing deleterious effects of TR is also enabling exploration of the phenotypic landscape of protein isoforms.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
During protein synthesis genetic instructions are passed from DNA via mRNA to the ribosome to assemble a protein chain. Occasionally, stop codons in the mRNA are bypassed and translation continues into the untranslated region (3′-UTR). This process, called translational readthrough (TR), yields a protein chain that becomes longer than would be predicted from the DNA sequence alone. Protein sequences vary in propensity for translational errors, which may yield evolutionary constraints by limiting evolutionary paths. Here we investigated TR in Saccharomyces cerevisiae by analysing ribosome profiling data. We clustered proteins as either prone or non-prone to TR, and conducted comparative analyses. We find that a relatively high frequency (5%) of genes undergo TR, including ribosomal subunit proteins. Our main finding is that proteins undergoing TR are highly expressed and have a higher proportion of intrinsically disordered C-termini. We suggest that highly expressed proteins may compensate for the deleterious effects of TR by having intrinsically disordered C-termini, which may provide conformational flexibility but without distorting native function. Moreover, we discuss whether minimizing deleterious effects of TR is also enabling exploration of the phenotypic landscape of protein isoforms.
Schmitz, Jonathan F.; Ullrich, Kristian K.; Bornberg-Bauer, Erich
Incipient de novo genes can evolve from frozen accidents that escaped rapid transcript turnover Journal Article
In: Nature Ecology & Evolution, vol. 2, pp. 1626–1632, 2018.
@article{Schmitz2018,
title = {Incipient de novo genes can evolve from frozen accidents that escaped rapid transcript turnover},
author = {Jonathan F. Schmitz and Kristian K. Ullrich and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/schmitz2018.pdf, Download},
doi = {10.1038/s41559-018-0639-7},
year = {2018},
date = {2018-09-10},
journal = {Nature Ecology & Evolution},
volume = {2},
pages = {1626–1632},
abstract = {A recent surge of studies have suggested that many novel genes arise de novo from previously noncoding DNA and not by duplication. However, most studies concentrated on longer evolutionary time scales and rarely considered protein structural properties. Therefore, it remains unclear how these properties are shaped by evolution, depend on genetic mechanisms and influence gene survival. Here we compare open reading frames (ORFs) from high coverage transcriptomes from mouse and another four mammals covering 160 million years of evolution. We find that novel ORFs pervasively emerge from noncoding regions but are rapidly lost again, while relatively fewer arise from the divergence of coding sequences but are retained much longer. We also find that a subset (14%) of the mouse-specific ORFs bind ribosomes and are potentially translated, showing that such ORFs can be the starting points of gene emergence. Surprisingly, disorder and other protein properties of young ORFs hardly change with gene age in short time frames. Only length and nucleotide composition change significantly. Thus, some transcribed de novo genes resemble ‘frozen accidents’ of randomly emerged ORFs that survived initial purging. This perspective complies with very recent studies indicating that some neutrally evolving transcripts containing random protein sequences may be translated and be viable starting points of de novo gene emergence.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
A recent surge of studies have suggested that many novel genes arise de novo from previously noncoding DNA and not by duplication. However, most studies concentrated on longer evolutionary time scales and rarely considered protein structural properties. Therefore, it remains unclear how these properties are shaped by evolution, depend on genetic mechanisms and influence gene survival. Here we compare open reading frames (ORFs) from high coverage transcriptomes from mouse and another four mammals covering 160 million years of evolution. We find that novel ORFs pervasively emerge from noncoding regions but are rapidly lost again, while relatively fewer arise from the divergence of coding sequences but are retained much longer. We also find that a subset (14%) of the mouse-specific ORFs bind ribosomes and are potentially translated, showing that such ORFs can be the starting points of gene emergence. Surprisingly, disorder and other protein properties of young ORFs hardly change with gene age in short time frames. Only length and nucleotide composition change significantly. Thus, some transcribed de novo genes resemble ‘frozen accidents’ of randomly emerged ORFs that survived initial purging. This perspective complies with very recent studies indicating that some neutrally evolving transcripts containing random protein sequences may be translated and be viable starting points of de novo gene emergence.
Bornberg-Bauer, Erich; Harrison, Mark C.; Jongepier, Evelien
The first cockroach genome and its significance for understanding development and the evolution of insect eusociality Journal Article
In: Journal of Experimental Zoology Part B, 2018.
@article{Bornberg-Bauer2018,
title = {The first cockroach genome and its significance for understanding development and the evolution of insect eusociality},
author = {Erich Bornberg-Bauer and Mark C. Harrison and Evelien Jongepier},
url = {https://bornberglab.org/wp-content/uploads/2021/10/EBB_JEZB_Editorial20180910.pdf, Download},
doi = {10.1002/jez.b.22826},
year = {2018},
date = {2018-07-30},
journal = {Journal of Experimental Zoology Part B},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Harrison, Mark C.; Arning, Nicolas; Kremer, Lukas P. M.; Ylla, Guillem; Belles, Xavier; Bornberg-Bauer, Erich; Huylmans, Ann K.; Jongepier, Evelien; Piulachs, Maria‐Dolors; Richards, Stephen; Schal, Coby
Expansions of key protein families in the German cockroach highlight the molecular basis of its remarkable success as a global indoor pest Journal Article
In: Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, vol. 330, no. 5, pp. 254-264, 2018.
@article{Harrison2018b,
title = {Expansions of key protein families in the German cockroach highlight the molecular basis of its remarkable success as a global indoor pest},
author = {Mark C. Harrison and Nicolas Arning and Lukas P. M. Kremer and Guillem Ylla and Xavier Belles and Erich Bornberg-Bauer and Ann K. Huylmans and Evelien Jongepier and Maria‐Dolors Piulachs and Stephen Richards and Coby Schal},
url = {https://bornberglab.org/wp-content/uploads/2021/10/Harrison20182.pdf, Download},
doi = {10.1002/jez.b.22824},
year = {2018},
date = {2018-07-11},
urldate = {2018-07-11},
journal = {Journal of Experimental Zoology Part B: Molecular and Developmental Evolution},
volume = {330},
number = {5},
pages = {254-264},
abstract = {The German cockroach, Blattella germanica, is a worldwide pest that infests buildings, including homes, restaurants, and hospitals, often living in unsanitary conditions. As a disease vector and producer of allergens, this species has major health and economic impacts on humans. Factors contributing to the success of the German cockroach include its resistance to a broad range of insecticides, immunity to many pathogens, and its ability, as an extreme generalist omnivore, to survive on most food sources. The recently published genome shows that B. germanica has an exceptionally high number of protein coding genes. In this study, we investigate the functions of the 93 significantly expanded gene families with the aim to better understand the success of B. germanica as a major pest despite such inhospitable conditions. We find major expansions in gene families with functions related to the detoxification of insecticides and allelochemicals, defense against pathogens, digestion, sensory perception, and gene regulation. These expansions might have allowed B. germanica to develop multiple resistance mechanisms to insecticides and pathogens, and enabled a broad, flexible diet, thus explaining its success in unsanitary conditions and under recurrent chemical control. The findings and resources presented here provide insights for better understanding molecular mechanisms that will facilitate more effective cockroach control.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The German cockroach, Blattella germanica, is a worldwide pest that infests buildings, including homes, restaurants, and hospitals, often living in unsanitary conditions. As a disease vector and producer of allergens, this species has major health and economic impacts on humans. Factors contributing to the success of the German cockroach include its resistance to a broad range of insecticides, immunity to many pathogens, and its ability, as an extreme generalist omnivore, to survive on most food sources. The recently published genome shows that B. germanica has an exceptionally high number of protein coding genes. In this study, we investigate the functions of the 93 significantly expanded gene families with the aim to better understand the success of B. germanica as a major pest despite such inhospitable conditions. We find major expansions in gene families with functions related to the detoxification of insecticides and allelochemicals, defense against pathogens, digestion, sensory perception, and gene regulation. These expansions might have allowed B. germanica to develop multiple resistance mechanisms to insecticides and pathogens, and enabled a broad, flexible diet, thus explaining its success in unsanitary conditions and under recurrent chemical control. The findings and resources presented here provide insights for better understanding molecular mechanisms that will facilitate more effective cockroach control.
Kremer, Lukas P. M.; Korb, Judith; Bornberg-Bauer, Erich
Reconstructed evolution of insulin receptors in insects reveals duplications in early insects and cockroaches Journal Article
In: Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, vol. 330, no. 5, pp. 305-311, 2018.
@article{Kremer2018,
title = {Reconstructed evolution of insulin receptors in insects reveals duplications in early insects and cockroaches},
author = {Lukas P. M. Kremer and Judith Korb and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Kremer2018.pdf, Download},
doi = {10.1002/jez.b.22809},
year = {2018},
date = {2018-06-10},
journal = {Journal of Experimental Zoology Part B: Molecular and Developmental Evolution},
volume = {330},
number = {5},
pages = {305-311},
abstract = {Social insects show an extreme degree of phenotypic plasticity. In highly eusocial species, this manifests in the generation of distinct castes with extreme differences in both morphology and life span. The molecular basis of these differences is highly entangled and not fully understood, but several recent studies demonstrated that insulin/insulin‐like growth factor signaling (IIS) is one of the key pathways. Here, we investigate the molecular evolution of insect insulin receptors (InRs), which are membrane‐bound dimers that enable IIS by relaying extracellular signals to intracellular signaling cascades. Classic models of invertebrate IIS include only one InR gene, but some recent studies on less commonly studied insects have found two InRs, which act in an antagonistic manner to facilitate polyphenism in at least one documented case. We search 22 arthropod genomes and identify several InR copies and their evolutionary origin that were lacking from previous annotations. Phylogenetic analysis shows that the two insect InR genes date back at least 400 million years to a common ancestor of winged insects. Most notably, we also identified the evolutionary origin of a third InR copy that is unique to the clade of Blattodea, just before therein the eusocial termites evolved. One of the InR paralogs consistently shows caste‐biased expression in all three termites, which strongly suggests a role in caste differentiation. These results have important ramifications for past and future InR inhibition/InR knockdown experiments in insects and they provide a set of key genes regulating life span and morphology in termite castes.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Social insects show an extreme degree of phenotypic plasticity. In highly eusocial species, this manifests in the generation of distinct castes with extreme differences in both morphology and life span. The molecular basis of these differences is highly entangled and not fully understood, but several recent studies demonstrated that insulin/insulin‐like growth factor signaling (IIS) is one of the key pathways. Here, we investigate the molecular evolution of insect insulin receptors (InRs), which are membrane‐bound dimers that enable IIS by relaying extracellular signals to intracellular signaling cascades. Classic models of invertebrate IIS include only one InR gene, but some recent studies on less commonly studied insects have found two InRs, which act in an antagonistic manner to facilitate polyphenism in at least one documented case. We search 22 arthropod genomes and identify several InR copies and their evolutionary origin that were lacking from previous annotations. Phylogenetic analysis shows that the two insect InR genes date back at least 400 million years to a common ancestor of winged insects. Most notably, we also identified the evolutionary origin of a third InR copy that is unique to the clade of Blattodea, just before therein the eusocial termites evolved. One of the InR paralogs consistently shows caste‐biased expression in all three termites, which strongly suggests a role in caste differentiation. These results have important ramifications for past and future InR inhibition/InR knockdown experiments in insects and they provide a set of key genes regulating life span and morphology in termite castes.
Jongepier, Evelien; Kemena, Carsten; Lopez-Ezquerra, Alberto; Belles, Xavier; Bornberg-Bauer, Erich; Korb, Judith
Remodeling of the juvenile hormone pathway through caste‐biased gene expression and positive selection along a gradient of termite eusociality Journal Article
In: Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, vol. 330, no. 5, pp. 296-304, 2018.
@article{Jongepier2018,
title = {Remodeling of the juvenile hormone pathway through caste‐biased gene expression and positive selection along a gradient of termite eusociality},
author = {Evelien Jongepier and Carsten Kemena and Alberto Lopez-Ezquerra and Xavier Belles and Erich Bornberg-Bauer and Judith Korb},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Jongepier2018.pdf, Download},
doi = {10.1002/jez.b.22805},
year = {2018},
date = {2018-05-29},
journal = {Journal of Experimental Zoology Part B: Molecular and Developmental Evolution},
volume = {330},
number = {5},
pages = {296-304},
abstract = {The evolution of division of labor between sterile and fertile individuals represents one of the major transitions in biological complexity. A fascinating gradient in eusociality evolved among the ancient hemimetabolous insects, ranging from noneusocial cockroaches through the primitively social lower termites—where workers retain the ability to reproduce—to the higher termites, characterized by lifetime commitment to worker sterility. Juvenile hormone (JH) is a prime candidate for the regulation of reproductive division of labor in termites, as it plays a key role in insect postembryonic development and reproduction. We compared the expression of JH pathway genes between workers and queens in two lower termites (Zootermopsis nevadensis and Cryptotermes secundus) and a higher termite (Macrotermes natalensis) to that of analogous nymphs and adult females of the noneusocial cockroach Blattella germanica. JH biosynthesis and metabolism genes ranged from reproductive female‐biased expression in the cockroach to predominantly worker‐biased expression in the lower termites. Remarkably, the expression profile of JH pathway genes sets the higher termite apart from the two lower termites, as well as the cockroach, indicating that JH signaling has undergone major changes in this eusocial termite. These changes go beyond mere shifts in gene expression between the different castes, as we find evidence for positive selection in several termite JH pathway genes. Thus, remodeling of the JH pathway may have played a major role in termite social evolution, representing a striking case of convergent molecular evolution between the termites and the distantly related social hymenoptera.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The evolution of division of labor between sterile and fertile individuals represents one of the major transitions in biological complexity. A fascinating gradient in eusociality evolved among the ancient hemimetabolous insects, ranging from noneusocial cockroaches through the primitively social lower termites—where workers retain the ability to reproduce—to the higher termites, characterized by lifetime commitment to worker sterility. Juvenile hormone (JH) is a prime candidate for the regulation of reproductive division of labor in termites, as it plays a key role in insect postembryonic development and reproduction. We compared the expression of JH pathway genes between workers and queens in two lower termites (Zootermopsis nevadensis and Cryptotermes secundus) and a higher termite (Macrotermes natalensis) to that of analogous nymphs and adult females of the noneusocial cockroach Blattella germanica. JH biosynthesis and metabolism genes ranged from reproductive female‐biased expression in the cockroach to predominantly worker‐biased expression in the lower termites. Remarkably, the expression profile of JH pathway genes sets the higher termite apart from the two lower termites, as well as the cockroach, indicating that JH signaling has undergone major changes in this eusocial termite. These changes go beyond mere shifts in gene expression between the different castes, as we find evidence for positive selection in several termite JH pathway genes. Thus, remodeling of the JH pathway may have played a major role in termite social evolution, representing a striking case of convergent molecular evolution between the termites and the distantly related social hymenoptera.
Klasberg, Steffen; Bitard-Feildel, Tristan; Callebaut, Isabelle; Bornberg-Bauer, Erich
Origins and structural properties of novel and de novo protein domains during insect evolution Journal Article
In: The FEBS journal, vol. 285, no. 14, pp. 2605-2625, 2018.
@article{Klasberg2018,
title = {Origins and structural properties of novel and de novo protein domains during insect evolution},
author = {Steffen Klasberg and Tristan Bitard-Feildel and Isabelle Callebaut and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Klasberg2018.pdf, Download},
doi = {10.1111/febs.14504},
year = {2018},
date = {2018-05-26},
journal = {The FEBS journal},
volume = {285},
number = {14},
pages = {2605-2625},
abstract = {Over long time scales, protein evolution is characterized by modular rearrangements of protein domains. Such rearrangements are mainly caused by gene duplication, fusion and terminal losses. To better understand domain emergence mechanisms we investigated 32 insect genomes covering a speciation gradient ranging from ~ 2 to ~ 390 mya. We use established domain models and foldable domains delineated by hydrophobic cluster analysis (HCA), which does not require homologous sequences, to also identify domains which have likely arisen de novo, that is, from previously noncoding DNA. Our results indicate that most novel domains emerge terminally as they originate from ORF extensions while fewer arise in middle arrangements, resulting from exonization of intronic or intergenic regions. Many novel domains rapidly migrate between terminal or middle positions and single‐ and multidomain arrangements. Young domains, such as most HCA‐defined domains, are under strong selection pressure as they show signals of purifying selection. De novo domains, linked to ancient domains or defined by HCA, have higher degrees of intrinsic disorder and disorder‐to‐order transition upon binding than ancient domains. However, the corresponding DNA sequences of the novel domains of de novo origins could only rarely be found in sister genomes. We conclude that novel domains are often recruited by other proteins and undergo important structural modifications shortly after their emergence, but evolve too fast to be characterized by cross‐species comparisons alone.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Over long time scales, protein evolution is characterized by modular rearrangements of protein domains. Such rearrangements are mainly caused by gene duplication, fusion and terminal losses. To better understand domain emergence mechanisms we investigated 32 insect genomes covering a speciation gradient ranging from ~ 2 to ~ 390 mya. We use established domain models and foldable domains delineated by hydrophobic cluster analysis (HCA), which does not require homologous sequences, to also identify domains which have likely arisen de novo, that is, from previously noncoding DNA. Our results indicate that most novel domains emerge terminally as they originate from ORF extensions while fewer arise in middle arrangements, resulting from exonization of intronic or intergenic regions. Many novel domains rapidly migrate between terminal or middle positions and single‐ and multidomain arrangements. Young domains, such as most HCA‐defined domains, are under strong selection pressure as they show signals of purifying selection. De novo domains, linked to ancient domains or defined by HCA, have higher degrees of intrinsic disorder and disorder‐to‐order transition upon binding than ancient domains. However, the corresponding DNA sequences of the novel domains of de novo origins could only rarely be found in sister genomes. We conclude that novel domains are often recruited by other proteins and undergo important structural modifications shortly after their emergence, but evolve too fast to be characterized by cross‐species comparisons alone.
Loo, Bert; Schober, Markus; Valkov, Eugene; Heberlein, Magdalena; Bornberg-Bauer, Erich; Faber, Kurt; Hyvönen, Marko; Hollfelder, Florian
In: Journal of Molecular Biology, vol. 430, no. 7, pp. 1004-1023, 2018.
@article{vanLoo2018,
title = {Structural and Mechanistic Analysis of the Choline Sulfatase from Sinorhizobium melliloti: A Class I Sulfatase Specific for an Alkyl Sulfate Ester},
author = {Bert Loo and Markus Schober and Eugene Valkov and Magdalena Heberlein and Erich Bornberg-Bauer and Kurt Faber and Marko Hyvönen and Florian Hollfelder},
url = {https://bornberglab.org/wp-content/uploads/2021/03/loo2018.pdf, Download},
doi = {10.1016/j.jmb.2018.02.010},
year = {2018},
date = {2018-03-30},
journal = {Journal of Molecular Biology},
volume = {430},
number = {7},
pages = {1004-1023},
abstract = {Hydrolysis of organic sulfate esters proceeds by two distinct mechanisms, water attacking at either sulfur (S–O bond cleavage) or carbon (C–O bond cleavage). In primary and secondary alkyl sulfates, attack at carbon is favored, whereas in aromatic sulfates and sulfated sugars, attack at sulfur is preferred. This mechanistic distinction is mirrored in the classification of enzymes that catalyze sulfate ester hydrolysis: arylsulfatases (ASs) catalyze S–O cleavage in sulfate sugars and arylsulfates, and alkyl sulfatases break the C–O bond of alkyl sulfates. Sinorhizobium meliloti choline sulfatase (SmCS) efficiently catalyzes the hydrolysis of alkyl sulfate choline-O-sulfate (kcat/KM = 4.8 × 103 s− 1 M− 1) as well as arylsulfate 4-nitrophenyl sulfate (kcat/KM = 12 s− 1 M− 1). Its 2.8-Å resolution X-ray structure shows a buried, largely hydrophobic active site in which a conserved glutamate (Glu386) plays a role in recognition of the quaternary ammonium group of the choline substrate. SmCS structurally resembles members of the alkaline phosphatase superfamily, being most closely related to dimeric ASs and tetrameric phosphonate monoester hydrolases. Although > 70% of the amino acids between protomers align structurally (RMSDs 1.79–1.99 Å), the oligomeric structures show distinctly different packing and protomer–protomer interfaces. The latter also play an important role in active site formation. Mutagenesis of the conserved active site residues typical for ASs, H218O-labeling studies and the observation of catalytically promiscuous behavior toward phosphoesters confirm the close relation to alkaline phosphatase superfamily members and suggest that SmCS is an AS that catalyzes S–O cleavage in alkyl sulfate esters with extreme catalytic proficiency.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Hydrolysis of organic sulfate esters proceeds by two distinct mechanisms, water attacking at either sulfur (S–O bond cleavage) or carbon (C–O bond cleavage). In primary and secondary alkyl sulfates, attack at carbon is favored, whereas in aromatic sulfates and sulfated sugars, attack at sulfur is preferred. This mechanistic distinction is mirrored in the classification of enzymes that catalyze sulfate ester hydrolysis: arylsulfatases (ASs) catalyze S–O cleavage in sulfate sugars and arylsulfates, and alkyl sulfatases break the C–O bond of alkyl sulfates. Sinorhizobium meliloti choline sulfatase (SmCS) efficiently catalyzes the hydrolysis of alkyl sulfate choline-O-sulfate (kcat/KM = 4.8 × 103 s− 1 M− 1) as well as arylsulfate 4-nitrophenyl sulfate (kcat/KM = 12 s− 1 M− 1). Its 2.8-Å resolution X-ray structure shows a buried, largely hydrophobic active site in which a conserved glutamate (Glu386) plays a role in recognition of the quaternary ammonium group of the choline substrate. SmCS structurally resembles members of the alkaline phosphatase superfamily, being most closely related to dimeric ASs and tetrameric phosphonate monoester hydrolases. Although > 70% of the amino acids between protomers align structurally (RMSDs 1.79–1.99 Å), the oligomeric structures show distinctly different packing and protomer–protomer interfaces. The latter also play an important role in active site formation. Mutagenesis of the conserved active site residues typical for ASs, H218O-labeling studies and the observation of catalytically promiscuous behavior toward phosphoesters confirm the close relation to alkaline phosphatase superfamily members and suggest that SmCS is an AS that catalyzes S–O cleavage in alkyl sulfate esters with extreme catalytic proficiency.
Lopez-Ezquerra, Alberto; Mitschke, Andreas; Bornberg-Bauer, Erich; Joop, Gerrit
Tribolium castaneum gene expression changes after Paranosema whitei infection Journal Article
In: Journal of Invertebrate Pathology, vol. 153, pp. 92-98, 2018.
@article{Lopez-Ezquerra2018,
title = {Tribolium castaneum gene expression changes after Paranosema whitei infection},
author = {Alberto Lopez-Ezquerra and Andreas Mitschke and Erich Bornberg-Bauer and Gerrit Joop},
url = {https://bornberglab.org/wp-content/uploads/2021/10/lopez2018.pdf, Download},
doi = {10.1016/j.jip.2018.02.009},
year = {2018},
date = {2018-03-01},
journal = {Journal of Invertebrate Pathology},
volume = {153},
pages = {92-98},
abstract = {Background
Microsporidia are obligate parasites that possess some of the smallest eukaryotic genomes. Several insect species are susceptible to infections by microsporidian parasites. Paranosema whitei frequently infects young larvae of Tribolium castaneum and obligately kills the host whereupon transmission to subsequent hosts is accomplished via spores. P. whitei infection results in developmental arrest of T. castaneum, preventing larvae from pupation. The mechanisms underlying P. whitei virulence as well as the molecular underpinning of host defenses remain uncharacterized. In the present study, we evaluated gene expression differences of T. castaneum infected with the microsporidian parasite P. whitei.
Results
More than 1500 T. castaneum genes were differentially expressed after infection with P. whitei. Several important host pathways appeared to be differentially expressed after infection, where immune genes were among the highest differential expressed genes. Genes involved in the Toll pathway and its effectors were specifically upregulated. Furthermore, iron homeostasis processes and transmembrane transport appeared significantly altered after P. whitei infection. Krüppel homolog 1 (Kr-h1) and other genes of the juvenile hormone (JH) pathway appeared differentially expressed after parasite infection. In addition, a small number of long intergenic non-coding RNAs (lincRNAs) appeared differentially expressed after P. whitei infection.
Conclusion
In this study we characterized for the first time using RNA-seq the immune response of T. castaneum to P. whitei. Other pathways (transmembrane transport, iron homeostasis, protein synthesis, JH) indicate possible alterations of the host by the parasite such as a possible developmental arrest caused by JH regulation. Furthermore we find evidence that some lincRNAs might be connected to defense as previously reported for other insect species.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
Microsporidia are obligate parasites that possess some of the smallest eukaryotic genomes. Several insect species are susceptible to infections by microsporidian parasites. Paranosema whitei frequently infects young larvae of Tribolium castaneum and obligately kills the host whereupon transmission to subsequent hosts is accomplished via spores. P. whitei infection results in developmental arrest of T. castaneum, preventing larvae from pupation. The mechanisms underlying P. whitei virulence as well as the molecular underpinning of host defenses remain uncharacterized. In the present study, we evaluated gene expression differences of T. castaneum infected with the microsporidian parasite P. whitei.
Results
More than 1500 T. castaneum genes were differentially expressed after infection with P. whitei. Several important host pathways appeared to be differentially expressed after infection, where immune genes were among the highest differential expressed genes. Genes involved in the Toll pathway and its effectors were specifically upregulated. Furthermore, iron homeostasis processes and transmembrane transport appeared significantly altered after P. whitei infection. Krüppel homolog 1 (Kr-h1) and other genes of the juvenile hormone (JH) pathway appeared differentially expressed after parasite infection. In addition, a small number of long intergenic non-coding RNAs (lincRNAs) appeared differentially expressed after P. whitei infection.
Conclusion
In this study we characterized for the first time using RNA-seq the immune response of T. castaneum to P. whitei. Other pathways (transmembrane transport, iron homeostasis, protein synthesis, JH) indicate possible alterations of the host by the parasite such as a possible developmental arrest caused by JH regulation. Furthermore we find evidence that some lincRNAs might be connected to defense as previously reported for other insect species.
Microsporidia are obligate parasites that possess some of the smallest eukaryotic genomes. Several insect species are susceptible to infections by microsporidian parasites. Paranosema whitei frequently infects young larvae of Tribolium castaneum and obligately kills the host whereupon transmission to subsequent hosts is accomplished via spores. P. whitei infection results in developmental arrest of T. castaneum, preventing larvae from pupation. The mechanisms underlying P. whitei virulence as well as the molecular underpinning of host defenses remain uncharacterized. In the present study, we evaluated gene expression differences of T. castaneum infected with the microsporidian parasite P. whitei.
Results
More than 1500 T. castaneum genes were differentially expressed after infection with P. whitei. Several important host pathways appeared to be differentially expressed after infection, where immune genes were among the highest differential expressed genes. Genes involved in the Toll pathway and its effectors were specifically upregulated. Furthermore, iron homeostasis processes and transmembrane transport appeared significantly altered after P. whitei infection. Krüppel homolog 1 (Kr-h1) and other genes of the juvenile hormone (JH) pathway appeared differentially expressed after parasite infection. In addition, a small number of long intergenic non-coding RNAs (lincRNAs) appeared differentially expressed after P. whitei infection.
Conclusion
In this study we characterized for the first time using RNA-seq the immune response of T. castaneum to P. whitei. Other pathways (transmembrane transport, iron homeostasis, protein synthesis, JH) indicate possible alterations of the host by the parasite such as a possible developmental arrest caused by JH regulation. Furthermore we find evidence that some lincRNAs might be connected to defense as previously reported for other insect species.
Kemena, Carsten; Bornberg-Bauer, Erich
A roadmap to domain based proteomics Book Chapter
In: Computational Methods in Protein Evolution, Humana Press, 2018.
@inbook{Kemena2018,
title = {A roadmap to domain based proteomics},
author = {Carsten Kemena and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/10/Kemena20192.pdf, Download},
year = {2018},
date = {2018-02-09},
urldate = {2018-02-09},
booktitle = {Computational Methods in Protein Evolution},
journal = {Computational Methods in Protein Evolution},
publisher = {Humana Press},
abstract = {Protein domains are reusable segments of proteins and play an important role in protein evolution. By combining the elements from a relatively small set of domains into unique arrangements, a large number of proteins can be generated. Since domains often have specific functions, changes in their arrangement usually affect the overall protein function. Furthermore, domains are well amenable to computational representations, e.g., by HMMs (Hidden Markov Models) and these HMMs are widely represented in various data bases. Therefore, domains can be efficiently used for proteomic analyses. Here, we describe how domains are annotated using different domain databases and then how to assess the annotation quality of proteomes. We next show how functional annotations of domains in large scale data such as whole genomes or transcriptomes can be used to analyze molecular differences between species. Furthermore, we describe methods to analyze the changes in domain content of proteins which significantly helps to characterize and reconstruct the modular evolution of proteins. Altogether, domain based methods offer a computationally highly effective approach to analyze large amounts of proteomic data in an evolutionary setting.},
keywords = {},
pubstate = {published},
tppubtype = {inbook}
}
Protein domains are reusable segments of proteins and play an important role in protein evolution. By combining the elements from a relatively small set of domains into unique arrangements, a large number of proteins can be generated. Since domains often have specific functions, changes in their arrangement usually affect the overall protein function. Furthermore, domains are well amenable to computational representations, e.g., by HMMs (Hidden Markov Models) and these HMMs are widely represented in various data bases. Therefore, domains can be efficiently used for proteomic analyses. Here, we describe how domains are annotated using different domain databases and then how to assess the annotation quality of proteomes. We next show how functional annotations of domains in large scale data such as whole genomes or transcriptomes can be used to analyze molecular differences between species. Furthermore, we describe methods to analyze the changes in domain content of proteins which significantly helps to characterize and reconstruct the modular evolution of proteins. Altogether, domain based methods offer a computationally highly effective approach to analyze large amounts of proteomic data in an evolutionary setting.
Harrison, Mark C.; Jongepier, Evelien; Robertson, Hugh M.; Arning, Nicolas; Bitard-Feildel, Tristan; Chao, Hsu; Childers, Christopher P.; Dinh, Huyen; Doddapaneni, Harshavardhan; Dugan, Shannon; Gowin, Johannes; Greiner, Carolin; Han, Yi; Hu, Haofu; Hughes, Daniel S. T.; Huylmans, Ann K.; Kemena, Carsten; Kremer, Lukas P. M.; Lee, Sandra L.; Lopez-Ezquerra, Alberto; Mallet, Ludovic; Monroy-Kuhn, Jose M.; Moser, Annabell; Murali, Shwetha C.; Muzny, Donna M.; Otani, Saria; Piulachs, Maria-Dolors; Poelchau, Monica; Qu, Jiaxin; Schaub, Florentine; Wada-Katsumata, Ayako; Worley, Kim C.; Xie, Qiaolin; Ylla, Guillem; Poulsen, Michael; Gibbs, Richard A.; Schal, Coby; Richards, Stephen; Belles, Xavier; Korb, Judith; Bornberg-Bauer, Erich
Hemimetabolous genomes reveal molecular basis of termite eusociality Journal Article
In: Nature Ecology & Evolution, vol. 2, pp. 557–566, 2018.
@article{Harrison2018,
title = {Hemimetabolous genomes reveal molecular basis of termite eusociality},
author = {Mark C. Harrison and Evelien Jongepier and Hugh M. Robertson and Nicolas Arning and Tristan Bitard-Feildel and Hsu Chao and Christopher P. Childers and Huyen Dinh and Harshavardhan Doddapaneni and Shannon Dugan and Johannes Gowin and Carolin Greiner and Yi Han and Haofu Hu and Daniel S. T. Hughes and Ann K. Huylmans and Carsten Kemena and Lukas P. M. Kremer and Sandra L. Lee and Alberto Lopez-Ezquerra and Ludovic Mallet and Jose M. Monroy-Kuhn and Annabell Moser and Shwetha C. Murali and Donna M. Muzny and Saria Otani and Maria-Dolors Piulachs and Monica Poelchau and Jiaxin Qu and Florentine Schaub and Ayako Wada-Katsumata and Kim C. Worley and Qiaolin Xie and Guillem Ylla and Michael Poulsen and Richard A. Gibbs and Coby Schal and Stephen Richards and Xavier Belles and Judith Korb and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Harrison2018.pdf, Download},
doi = {10.1038/s41559-017-0459-1},
year = {2018},
date = {2018-02-05},
urldate = {2018-02-05},
journal = {Nature Ecology & Evolution},
volume = {2},
pages = {557–566},
abstract = {Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the 2-Gb genome of the German cockroach, Blattella germanica, and the 1.3-Gb genome of the drywood termite Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the 2-Gb genome of the German cockroach, Blattella germanica, and the 1.3-Gb genome of the drywood termite Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.
2017
Lopez-Ezquerra, Alberto; Harrison, Mark C.; Bornberg-Bauer, Erich
Comparative analysis of lincRNA in insect species Journal Article
In: BMC Evolutionary Biology, vol. 17, no. 1, pp. 1-11, 2017.
@article{Lopez-Ezquerra2017,
title = {Comparative analysis of lincRNA in insect species},
author = {Alberto Lopez-Ezquerra and Mark C. Harrison and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Lopez-Ezquerra2017.pdf, Download},
doi = {10.1186/s12862-017-0985-0},
year = {2017},
date = {2017-07-03},
journal = {BMC Evolutionary Biology},
volume = {17},
number = {1},
pages = {1-11},
abstract = {Background
The ever increasing availability of genomes makes it possible to investigate and compare not only the genomic complements of genes and proteins, but also of RNAs. One class of RNAs, the long noncoding RNAs (lncRNAs) and, in particular, their subclass of long intergenic noncoding RNAs (lincRNAs) have recently gained much attention because of their roles in regulation of important biological processes such as immune response or cell differentiation and as possible evolutionary precursors for protein coding genes. lincRNAs seem to be poorly conserved at the sequence level but at least some lincRNAs have conserved structural elements and syntenic genomic positions. Previous studies showed that transposable elements are a main contribution to the evolution of lincRNAs in mammals. In contrast, plant lincRNA emergence and evolution has been linked with local duplication events. However, little is known about their evolutionary dynamics in general and in insect genomes in particular.
Results
Here we compared lincRNAs between seven insect genomes and investigated possible evolutionary changes and functional roles. We find very low sequence conservation between different species and that similarities within a species are mostly due to their association with transposable elements (TE) and simple repeats. Furthermore, we find that TEs are less frequent in lincRNA exons than in their introns, indicating that TEs may have been removed by selection. When we analysed the predicted thermodynamic stabilities of lincRNAs we found that they are more stable than their randomized controls which might indicate some selection pressure to maintain certain structural elements. We list several of the most stable lincRNAs which could serve as prime candidates for future functional studies. We also discuss the possibility of de novo protein coding genes emerging from lincRNAs. This is because lincRNAs with high GC content and potentially with longer open reading frames (ORF) are candidate loci where de novo gene emergence might occur.
Conclusion
The processes responsible for the emergence and diversification of lincRNAs in insects remain unclear. Both duplication and transposable elements may be important for the creation of new lincRNAs in insects.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
The ever increasing availability of genomes makes it possible to investigate and compare not only the genomic complements of genes and proteins, but also of RNAs. One class of RNAs, the long noncoding RNAs (lncRNAs) and, in particular, their subclass of long intergenic noncoding RNAs (lincRNAs) have recently gained much attention because of their roles in regulation of important biological processes such as immune response or cell differentiation and as possible evolutionary precursors for protein coding genes. lincRNAs seem to be poorly conserved at the sequence level but at least some lincRNAs have conserved structural elements and syntenic genomic positions. Previous studies showed that transposable elements are a main contribution to the evolution of lincRNAs in mammals. In contrast, plant lincRNA emergence and evolution has been linked with local duplication events. However, little is known about their evolutionary dynamics in general and in insect genomes in particular.
Results
Here we compared lincRNAs between seven insect genomes and investigated possible evolutionary changes and functional roles. We find very low sequence conservation between different species and that similarities within a species are mostly due to their association with transposable elements (TE) and simple repeats. Furthermore, we find that TEs are less frequent in lincRNA exons than in their introns, indicating that TEs may have been removed by selection. When we analysed the predicted thermodynamic stabilities of lincRNAs we found that they are more stable than their randomized controls which might indicate some selection pressure to maintain certain structural elements. We list several of the most stable lincRNAs which could serve as prime candidates for future functional studies. We also discuss the possibility of de novo protein coding genes emerging from lincRNAs. This is because lincRNAs with high GC content and potentially with longer open reading frames (ORF) are candidate loci where de novo gene emergence might occur.
Conclusion
The processes responsible for the emergence and diversification of lincRNAs in insects remain unclear. Both duplication and transposable elements may be important for the creation of new lincRNAs in insects.
The ever increasing availability of genomes makes it possible to investigate and compare not only the genomic complements of genes and proteins, but also of RNAs. One class of RNAs, the long noncoding RNAs (lncRNAs) and, in particular, their subclass of long intergenic noncoding RNAs (lincRNAs) have recently gained much attention because of their roles in regulation of important biological processes such as immune response or cell differentiation and as possible evolutionary precursors for protein coding genes. lincRNAs seem to be poorly conserved at the sequence level but at least some lincRNAs have conserved structural elements and syntenic genomic positions. Previous studies showed that transposable elements are a main contribution to the evolution of lincRNAs in mammals. In contrast, plant lincRNA emergence and evolution has been linked with local duplication events. However, little is known about their evolutionary dynamics in general and in insect genomes in particular.
Results
Here we compared lincRNAs between seven insect genomes and investigated possible evolutionary changes and functional roles. We find very low sequence conservation between different species and that similarities within a species are mostly due to their association with transposable elements (TE) and simple repeats. Furthermore, we find that TEs are less frequent in lincRNA exons than in their introns, indicating that TEs may have been removed by selection. When we analysed the predicted thermodynamic stabilities of lincRNAs we found that they are more stable than their randomized controls which might indicate some selection pressure to maintain certain structural elements. We list several of the most stable lincRNAs which could serve as prime candidates for future functional studies. We also discuss the possibility of de novo protein coding genes emerging from lincRNAs. This is because lincRNAs with high GC content and potentially with longer open reading frames (ORF) are candidate loci where de novo gene emergence might occur.
Conclusion
The processes responsible for the emergence and diversification of lincRNAs in insects remain unclear. Both duplication and transposable elements may be important for the creation of new lincRNAs in insects.
Loo, Bert; Bornberg-Bauer, Erich
Enzyme sub‐functionalization driven by regulation Journal Article
In: EMBO Reports, vol. 18, no. 7, pp. 1043-1045, 2017.
@article{vanLoo2017,
title = {Enzyme sub‐functionalization driven by regulation},
author = {Bert Loo and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Loo2017.pdf, Download},
doi = {10.15252/embr.201744383},
year = {2017},
date = {2017-06-14},
journal = {EMBO Reports},
volume = {18},
number = {7},
pages = {1043-1045},
abstract = {The emergence of functional novelties during protein evolution has puzzled scientists for many years. Most proposed models focus on repeated duplication‐divergence cycles, but the entanglement of selection pressures acting on the control of transcriptional and enzymatic activity, for example, by metabolites, has not been addressed so far. In this issue of EMBO Reports, Noda‐Garcia et al 1 describe two glutamate dehydrogenase paralogs from Bacillus subtilis with very similar sequences and under two distinct modes of activity control. The functional divergence of these two enzymes during evolution is driven by an interlinked combination of differences between their enzymatic properties and their transcriptional regulation. This article thus illuminates another level of complexity in molecular evolution that may help understand the hitherto unexplained co‐existence of paralogous genes that at first sight appear to be functionally redundant.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The emergence of functional novelties during protein evolution has puzzled scientists for many years. Most proposed models focus on repeated duplication‐divergence cycles, but the entanglement of selection pressures acting on the control of transcriptional and enzymatic activity, for example, by metabolites, has not been addressed so far. In this issue of EMBO Reports, Noda‐Garcia et al 1 describe two glutamate dehydrogenase paralogs from Bacillus subtilis with very similar sequences and under two distinct modes of activity control. The functional divergence of these two enzymes during evolution is driven by an interlinked combination of differences between their enzymatic properties and their transcriptional regulation. This article thus illuminates another level of complexity in molecular evolution that may help understand the hitherto unexplained co‐existence of paralogous genes that at first sight appear to be functionally redundant.
Gubala, Anna M.; Schmitz, Jonathan F.; Kearns, Michael J.; Vinh, Tery T.; Bornberg-Bauer, Erich; Wolfner, Mariana F.; Findlay, Geoffrey D.
The Goddard and Saturn Genes Are Essential for Drosophila Male Fertility and May Have Arisen De Novo Journal Article
In: Molecular Biology and Evolution, vol. 34, no. 5, pp. 1066–1082, 2017.
@article{Gubala2017,
title = {The Goddard and Saturn Genes Are Essential for Drosophila Male Fertility and May Have Arisen De Novo},
author = {Anna M. Gubala and Jonathan F. Schmitz and Michael J. Kearns and Tery T. Vinh and Erich Bornberg-Bauer and Mariana F. Wolfner and Geoffrey D. Findlay},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Gubala2017.pdf, Download},
doi = {10.1093/molbev/msx057},
year = {2017},
date = {2017-01-19},
journal = {Molecular Biology and Evolution},
volume = {34},
number = {5},
pages = {1066–1082},
abstract = {New genes arise through a variety of mechanisms, including the duplication of existing genes and the de novo birth of genes from noncoding DNA sequences. While there are numerous examples of duplicated genes with important functional roles, the functions of de novo genes remain largely unexplored. Many newly evolved genes are expressed in the male reproductive tract, suggesting that these evolutionary innovations may provide advantages to males experiencing sexual selection. Using testis-specific RNA interference, we screened 11 putative de novo genes in Drosophila melanogaster for effects on male fertility and identified two, goddard and saturn, that are essential for spermatogenesis and sperm function. Goddard knockdown (KD) males fail to produce mature sperm, while saturn KD males produce few sperm, and these function inefficiently once transferred to females. Consistent with a de novo origin, both genes are identifiable only in Drosophila and are predicted to encode proteins with no sequence similarity to any annotated protein. However, since high levels of divergence prevented the unambiguous identification of the noncoding sequences from which each gene arose, we consider goddard and saturn to be putative de novo genes. Within Drosophila, both genes have been lost in certain lineages, but show conserved, male-specific patterns of expression in the species in which they are found. Goddard is consistently found in single-copy and evolves under purifying selection. In contrast, saturn has diversified through gene duplication and positive selection. These data suggest that de novo genes can acquire essential roles in male reproduction.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
New genes arise through a variety of mechanisms, including the duplication of existing genes and the de novo birth of genes from noncoding DNA sequences. While there are numerous examples of duplicated genes with important functional roles, the functions of de novo genes remain largely unexplored. Many newly evolved genes are expressed in the male reproductive tract, suggesting that these evolutionary innovations may provide advantages to males experiencing sexual selection. Using testis-specific RNA interference, we screened 11 putative de novo genes in Drosophila melanogaster for effects on male fertility and identified two, goddard and saturn, that are essential for spermatogenesis and sperm function. Goddard knockdown (KD) males fail to produce mature sperm, while saturn KD males produce few sperm, and these function inefficiently once transferred to females. Consistent with a de novo origin, both genes are identifiable only in Drosophila and are predicted to encode proteins with no sequence similarity to any annotated protein. However, since high levels of divergence prevented the unambiguous identification of the noncoding sequences from which each gene arose, we consider goddard and saturn to be putative de novo genes. Within Drosophila, both genes have been lost in certain lineages, but show conserved, male-specific patterns of expression in the species in which they are found. Goddard is consistently found in single-copy and evolves under purifying selection. In contrast, saturn has diversified through gene duplication and positive selection. These data suggest that de novo genes can acquire essential roles in male reproduction.
Schmitz, Jonathan F.; Bornberg-Bauer, Erich
Fact or fiction: updates on how protein-coding genes might emerge de novo from previously non-coding DNA Journal Article
In: F1000 Research, vol. 6, 2017.
@article{Schmitz2019,
title = {Fact or fiction: updates on how protein-coding genes might emerge de novo from previously non-coding DNA},
author = {Jonathan F. Schmitz and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/03/Schmitz2017.pdf, Download},
doi = {10.12688/f1000research.10079.1},
year = {2017},
date = {2017-01-19},
journal = {F1000 Research},
volume = {6},
abstract = {Over the last few years, there has been an increasing amount of evidence for the de novo emergence of protein-coding genes, i.e. out of non-coding DNA. Here, we review the current literature and summarize the state of the field. We focus specifically on open questions and challenges in the study of de novo protein-coding genes such as the identification and verification of de novo-emerged genes. The greatest obstacle to date is the lack of high-quality genomic data with very short divergence times which could help precisely pin down the location of origin of a de novo gene. We conclude that, while there is plenty of evidence from a genetics perspective, there is a lack of functional studies of bona fide de novo genes and almost no knowledge about protein structures and how they come about during the emergence of de novo protein-coding genes. We suggest that future studies should concentrate on the functional and structural characterization of de novo protein-coding genes as well as the detailed study of the emergence of functional de novo protein-coding genes.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Over the last few years, there has been an increasing amount of evidence for the de novo emergence of protein-coding genes, i.e. out of non-coding DNA. Here, we review the current literature and summarize the state of the field. We focus specifically on open questions and challenges in the study of de novo protein-coding genes such as the identification and verification of de novo-emerged genes. The greatest obstacle to date is the lack of high-quality genomic data with very short divergence times which could help precisely pin down the location of origin of a de novo gene. We conclude that, while there is plenty of evidence from a genetics perspective, there is a lack of functional studies of bona fide de novo genes and almost no knowledge about protein structures and how they come about during the emergence of de novo protein-coding genes. We suggest that future studies should concentrate on the functional and structural characterization of de novo protein-coding genes as well as the detailed study of the emergence of functional de novo protein-coding genes.
2016
Schüler, Andreas; Bornberg-Bauer, Erich
Evolution of Protein Domain Repeats in Metazoa Journal Article
In: Molecular Biology and Evolution, vol. 33, no. 12, pp. 3170–3182, 2016.
@article{Schüler2016,
title = {Evolution of Protein Domain Repeats in Metazoa},
author = {Andreas Schüler and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/schuler2016.pdf, Download},
doi = {https://doi.org/10.1093/molbev/msw194},
year = {2016},
date = {2016-09-26},
journal = {Molecular Biology and Evolution},
volume = {33},
number = {12},
pages = {3170–3182},
abstract = {Repeats are ubiquitous elements of proteins and they play important roles for cellular function and during evolution. Repeats are, however, also notoriously difficult to capture computationally and large scale studies so far had difficulties in linking genetic causes, structural properties and evolutionary trajectories of protein repeats. Here we apply recently developed methods for repeat detection and analysis to a large dataset comprising over hundred metazoan genomes. We find that repeats in larger protein families experience generally very few insertions or deletions (indels) of repeat units but there is also a significant fraction of noteworthy volatile outliers with very high indel rates. Analysis of structural data indicates that repeats with an open structure and independently folding units are more volatile and more likely to be intrinsically disordered. Such disordered repeats are also significantly enriched in sites with a high functional potential such as linear motifs. Furthermore, the most volatile repeats have a high sequence similarity between their units. Since many volatile repeats also show signs of recombination, we conclude they are often shaped by concerted evolution. Intriguingly, many of these conserved yet volatile repeats are involved in host-pathogen interactions where they might foster fast but subtle adaptation in biological arms races.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Repeats are ubiquitous elements of proteins and they play important roles for cellular function and during evolution. Repeats are, however, also notoriously difficult to capture computationally and large scale studies so far had difficulties in linking genetic causes, structural properties and evolutionary trajectories of protein repeats. Here we apply recently developed methods for repeat detection and analysis to a large dataset comprising over hundred metazoan genomes. We find that repeats in larger protein families experience generally very few insertions or deletions (indels) of repeat units but there is also a significant fraction of noteworthy volatile outliers with very high indel rates. Analysis of structural data indicates that repeats with an open structure and independently folding units are more volatile and more likely to be intrinsically disordered. Such disordered repeats are also significantly enriched in sites with a high functional potential such as linear motifs. Furthermore, the most volatile repeats have a high sequence similarity between their units. Since many volatile repeats also show signs of recombination, we conclude they are often shaped by concerted evolution. Intriguingly, many of these conserved yet volatile repeats are involved in host-pathogen interactions where they might foster fast but subtle adaptation in biological arms races.
Jueterbock, A.; Franssen, Susanne U.; Bergmann, N.; Gu, Jenny; Coyer, J. A.; Reusch, T. B. H.; Bornberg-Bauer, Erich; Olsen, J. L.
Phylogeographic differentiation versus transcriptomic adaptation to warm temperatures in Zostera marina, a globally important seagrass Journal Article
In: Molecular Ecology, vol. 25, no. 21, pp. 5396-5411, 2016.
@article{Jueterbock2016,
title = {Phylogeographic differentiation versus transcriptomic adaptation to warm temperatures in Zostera marina, a globally important seagrass},
author = {A. Jueterbock and Susanne U. Franssen and N. Bergmann and Jenny Gu and J. A. Coyer and T. B. H. Reusch and Erich Bornberg-Bauer and J. L. Olsen},
url = {https://bornberglab.org/wp-content/uploads/2021/04/jueterbock2016.pdf, Download},
doi = {https://doi.org/10.1111/mec.13829},
year = {2016},
date = {2016-09-06},
journal = {Molecular Ecology},
volume = {25},
number = {21},
pages = {5396-5411},
abstract = {Populations distributed across a broad thermal cline are instrumental in addressing adaptation to increasing temperatures under global warming. Using a space‐for‐time substitution design, we tested for parallel adaptation to warm temperatures along two independent thermal clines in Zostera marina, the most widely distributed seagrass in the temperate Northern Hemisphere. A North–South pair of populations was sampled along the European and North American coasts and exposed to a simulated heatwave in a common‐garden mesocosm. Transcriptomic responses under control, heat stress and recovery were recorded in 99 RNAseq libraries with ~13 000 uniquely annotated, expressed genes. We corrected for phylogenetic differentiation among populations to discriminate neutral from adaptive differentiation. The two southern populations recovered faster from heat stress and showed parallel transcriptomic differentiation, as compared with northern populations. Among 2389 differentially expressed genes, 21 exceeded neutral expectations and were likely involved in parallel adaptation to warm temperatures. However, the strongest differentiation following phylogenetic correction was between the three Atlantic populations and the Mediterranean population with 128 of 4711 differentially expressed genes exceeding neutral expectations. Although adaptation to warm temperatures is expected to reduce sensitivity to heatwaves, the continued resistance of seagrass to further anthropogenic stresses may be impaired by heat‐induced downregulation of genes related to photosynthesis, pathogen defence and stress tolerance.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Populations distributed across a broad thermal cline are instrumental in addressing adaptation to increasing temperatures under global warming. Using a space‐for‐time substitution design, we tested for parallel adaptation to warm temperatures along two independent thermal clines in Zostera marina, the most widely distributed seagrass in the temperate Northern Hemisphere. A North–South pair of populations was sampled along the European and North American coasts and exposed to a simulated heatwave in a common‐garden mesocosm. Transcriptomic responses under control, heat stress and recovery were recorded in 99 RNAseq libraries with ~13 000 uniquely annotated, expressed genes. We corrected for phylogenetic differentiation among populations to discriminate neutral from adaptive differentiation. The two southern populations recovered faster from heat stress and showed parallel transcriptomic differentiation, as compared with northern populations. Among 2389 differentially expressed genes, 21 exceeded neutral expectations and were likely involved in parallel adaptation to warm temperatures. However, the strongest differentiation following phylogenetic correction was between the three Atlantic populations and the Mediterranean population with 128 of 4711 differentially expressed genes exceeding neutral expectations. Although adaptation to warm temperatures is expected to reduce sensitivity to heatwaves, the continued resistance of seagrass to further anthropogenic stresses may be impaired by heat‐induced downregulation of genes related to photosynthesis, pathogen defence and stress tolerance.
Klasberg, Steffen; Bitard-Feildel, Tristan; Mallet, Ludovic
Computational Identification of Novel Genes: Current and Future Perspectives Journal Article
In: Bioinformatics and Biology Insights, vol. 10, 2016.
@article{Klasberg2016,
title = {Computational Identification of Novel Genes: Current and Future Perspectives},
author = {Steffen Klasberg and Tristan Bitard-Feildel and Ludovic Mallet},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Klasberg2016.pdf, Download},
doi = {https://doi.org/10.4137/BBI.S39950},
year = {2016},
date = {2016-08-01},
journal = {Bioinformatics and Biology Insights},
volume = {10},
abstract = {While it has long been thought that all genomic novelties are derived from the existing material, many genes lacking homology to known genes were found in recent genome projects. Some of these novel genes were proposed to have evolved de novo, ie, out of noncoding sequences, whereas some have been shown to follow a duplication and divergence process. Their discovery called for an extension of the historical hypotheses about gene origination. Besides the theoretical breakthrough, increasing evidence accumulated that novel genes play important roles in evolutionary processes, including adaptation and speciation events. Different techniques are available to identify genes and classify them as novel. Their classification as novel is usually based on their similarity to known genes, or lack thereof, detected by comparative genomics or against databases. Computational approaches are further prime methods that can be based on existing models or leveraging biological evidences from experiments. Identification of novel genes remains however a challenging task. With the constant software and technologies updates, no gold standard, and no available benchmark, evaluation and characterization of genomic novelty is a vibrant field. In this review, the classical and state-of-the-art tools for gene prediction are introduced. The current methods for novel gene detection are presented; the methodological strategies and their limits are discussed along with perspective approaches for further studies},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
While it has long been thought that all genomic novelties are derived from the existing material, many genes lacking homology to known genes were found in recent genome projects. Some of these novel genes were proposed to have evolved de novo, ie, out of noncoding sequences, whereas some have been shown to follow a duplication and divergence process. Their discovery called for an extension of the historical hypotheses about gene origination. Besides the theoretical breakthrough, increasing evidence accumulated that novel genes play important roles in evolutionary processes, including adaptation and speciation events. Different techniques are available to identify genes and classify them as novel. Their classification as novel is usually based on their similarity to known genes, or lack thereof, detected by comparative genomics or against databases. Computational approaches are further prime methods that can be based on existing models or leveraging biological evidences from experiments. Identification of novel genes remains however a challenging task. With the constant software and technologies updates, no gold standard, and no available benchmark, evaluation and characterization of genomic novelty is a vibrant field. In this review, the classical and state-of-the-art tools for gene prediction are introduced. The current methods for novel gene detection are presented; the methodological strategies and their limits are discussed along with perspective approaches for further studies
Greenwood, Jenny M.; Lopez-Ezquerra, Alberto; Behrens, Sarah; Branca, Antoine; Mallet, Ludovic
Current analysis of next generation sequencing data with a focus on host-parasite interactions Journal Article
In: Zoology, vol. 119, pp. 298-306, 2016.
@article{Greenwood2016,
title = {Current analysis of next generation sequencing data with a focus on host-parasite interactions},
author = {Jenny M. Greenwood and Alberto Lopez-Ezquerra and Sarah Behrens and Antoine Branca and Ludovic Mallet},
url = {https://bornberglab.org/wp-content/uploads/2021/04/greenwood2016.pdf, Download},
doi = {https://doi.org/10.1016/j.zool.2016.06.010},
year = {2016},
date = {2016-06-22},
urldate = {2016-06-22},
journal = {Zoology},
volume = {119},
pages = {298-306},
abstract = {Among the most common forms of interaction between species are those between hosts and their parasites and they have important implications for evolutionary theory. Understanding both the phenotypic and genotypic processes governing such interactions is a major endeavour in biology, but is a complex and challenging task. The development of next generation sequencing technologies has recently opened up this field from a molecular perspective, allowing us access to the genomic data underlying laboratory or wild phenotypes. The data obtained from such technologies has many advantages over previous methods, such as being more abundant, often more accurate, less labour intensive to generate and more cost effective to produce. We present a review of the impact of next generation sequencing data on the study of host-parasite evolution and current topics being explored with this data. We focus on two main data types, genomic and transcriptomic. We discuss popular computational approaches which can help us characterise the molecular forces driving host-parasite systems and highlight some studies which have utilised such approaches to gain information about
particular immune processes. We furthermore highlight some promising perspectives from emerging and new technologies which will allow researchers to reach a deeper understanding of these interactions},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Among the most common forms of interaction between species are those between hosts and their parasites and they have important implications for evolutionary theory. Understanding both the phenotypic and genotypic processes governing such interactions is a major endeavour in biology, but is a complex and challenging task. The development of next generation sequencing technologies has recently opened up this field from a molecular perspective, allowing us access to the genomic data underlying laboratory or wild phenotypes. The data obtained from such technologies has many advantages over previous methods, such as being more abundant, often more accurate, less labour intensive to generate and more cost effective to produce. We present a review of the impact of next generation sequencing data on the study of host-parasite evolution and current topics being explored with this data. We focus on two main data types, genomic and transcriptomic. We discuss popular computational approaches which can help us characterise the molecular forces driving host-parasite systems and highlight some studies which have utilised such approaches to gain information about
particular immune processes. We furthermore highlight some promising perspectives from emerging and new technologies which will allow researchers to reach a deeper understanding of these interactions
particular immune processes. We furthermore highlight some promising perspectives from emerging and new technologies which will allow researchers to reach a deeper understanding of these interactions
Schmitz, Jonathan F.; Zimmer, Fabian; Bornberg-Bauer, Erich
Mechanisms of transcription factor evolution in Metazoa Journal Article
In: Nucleic Acids Research, vol. 44, no. 13, pp. 6287–6297, 2016.
@article{Schmitz2016,
title = {Mechanisms of transcription factor evolution in Metazoa},
author = {Jonathan F. Schmitz and Fabian Zimmer and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Schmitz2016.pdf, Download},
doi = {https://doi.org/10.1093/nar/gkw492},
year = {2016},
date = {2016-06-10},
journal = {Nucleic Acids Research},
volume = {44},
number = {13},
pages = {6287–6297},
abstract = {Transcriptions factors (TFs) are pivotal for the regulation of virtually all cellular processes, including growth and development. Expansions of TF families are causally linked to increases in organismal complexity. Here we study the evolutionary dynamics, genetic causes and functional implications of the five largest metazoan TF families. We find that family expansions dominate across the whole metazoan tree; however, some branches experience exceptional family-specific accelerated expansions. Additionally, we find that such expansions are often predated by modular domain rearrangements, which spur the expansion of a new sub-family by separating it from the rest of the TF family in terms of protein–protein interactions. This separation allows for radical shifts in the functional spectrum of a duplicated TF. We also find functional differentiation inside TF sub-families as changes in expression specificity. Furthermore, accelerated family expansions are facilitated by repeats of sequence motifs such as C2H2 zinc fingers. We quantify whole genome duplications and single gene duplications as sources of TF family expansions, implying that some, but not all, TF duplicates are preferentially retained. We conclude that trans-regulatory changes (domain rearrangements) are instrumental for fundamental functional innovations, that cis-regulatory changes (affecting expression) accomplish wide-spread fine tuning and both jointly contribute to the functional diversification of TFs.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Transcriptions factors (TFs) are pivotal for the regulation of virtually all cellular processes, including growth and development. Expansions of TF families are causally linked to increases in organismal complexity. Here we study the evolutionary dynamics, genetic causes and functional implications of the five largest metazoan TF families. We find that family expansions dominate across the whole metazoan tree; however, some branches experience exceptional family-specific accelerated expansions. Additionally, we find that such expansions are often predated by modular domain rearrangements, which spur the expansion of a new sub-family by separating it from the rest of the TF family in terms of protein–protein interactions. This separation allows for radical shifts in the functional spectrum of a duplicated TF. We also find functional differentiation inside TF sub-families as changes in expression specificity. Furthermore, accelerated family expansions are facilitated by repeats of sequence motifs such as C2H2 zinc fingers. We quantify whole genome duplications and single gene duplications as sources of TF family expansions, implying that some, but not all, TF duplicates are preferentially retained. We conclude that trans-regulatory changes (domain rearrangements) are instrumental for fundamental functional innovations, that cis-regulatory changes (affecting expression) accomplish wide-spread fine tuning and both jointly contribute to the functional diversification of TFs.
Elsner, Daniel; Kremer, Lukas P. M.; Arning, Nicolas; Bornberg-Bauer, Erich
Comparative genomic approaches to investigate molecular traits specific to social insects Journal Article
In: Current Opinion in Insect Science, vol. 16, pp. 87-94, 2016.
@article{Elsner2016,
title = {Comparative genomic approaches to investigate molecular traits specific to social insects},
author = {Daniel Elsner and Lukas P. M. Kremer and Nicolas Arning and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/elsner2016.pdf, Download},
doi = {https://doi.org/10.1016/j.cois.2016.05.016},
year = {2016},
date = {2016-05-27},
journal = {Current Opinion in Insect Science},
volume = {16},
pages = {87-94},
abstract = {Ageing is a feature of nearly all known organisms and, by its connection to survival, appears to trade off with fecundity. However, in some organisms such as in queens of social insects, this negative relation appears reversed and individuals live long and reproduce much. Since new experimental techniques, transcriptomes and genomes of many social insects have recently become available, a comparison of these data in a phylogenetic framework becomes feasible. This allows the study of general trends, species specific oddities and evolutionary dynamics of the molecular properties and changes which underlie ageing, fecundity and the reversal of this negative association. In the framework of social insect evolution, we review the most important recent insights, computational methods, their applications and data resources which are available.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Ageing is a feature of nearly all known organisms and, by its connection to survival, appears to trade off with fecundity. However, in some organisms such as in queens of social insects, this negative relation appears reversed and individuals live long and reproduce much. Since new experimental techniques, transcriptomes and genomes of many social insects have recently become available, a comparison of these data in a phylogenetic framework becomes feasible. This allows the study of general trends, species specific oddities and evolutionary dynamics of the molecular properties and changes which underlie ageing, fecundity and the reversal of this negative association. In the framework of social insect evolution, we review the most important recent insights, computational methods, their applications and data resources which are available.
Haase, David; Rieger, Jenny K.; Witten, Anika; Stoll, Monika; Bornberg-Bauer, Erich; Kalbe, Martin; Schmidt-Drewello, Alexander; P.Scharsack, Jörn; Reusch, Thorsten B. H.
In: Zoology, vol. 119, no. 4, pp. 307-313, 2016.
@article{Haase2016,
title = {Comparative transcriptomics of stickleback immune gene responses upon infection by two helminth parasites, Diplostomum pseudospathaceum and Schistocephalus solidus},
author = {David Haase and Jenny K. Rieger and Anika Witten and Monika Stoll and Erich Bornberg-Bauer and Martin Kalbe and Alexander Schmidt-Drewello and Jörn P.Scharsack and Thorsten B. H. Reusch},
url = {https://bornberglab.org/wp-content/uploads/2021/04/haase2016.pdf, Download},
doi = {https://doi.org/10.1016/j.zool.2016.05.005},
year = {2016},
date = {2016-05-23},
journal = {Zoology},
volume = {119},
number = {4},
pages = {307-313},
abstract = {Immune systems of vertebrates are much more diverse than previously thought, in particular at the base of the vertebrate clade. RNA-seq was used to describe in detail the transcriptomic response of stickleback hosts to infection by two helminth parasites, the trematode Diplostomum pseudospathaceum (2 genotypes plus a genotype mix) and the cestode Schistocephalus solidus. Based on a global transcription profiling, we present immune genes that are active during chronic or multiple repeated infection. We found that the transcription profiles of D. pseudospathaceum genotypes were as divergent as those of the two parasite species. When comparing the host immune response, only 5 immune genes were consistently upregulated upon infection by both species. These genes indicated a role for enhanced toll like receptor (TLR) activity (CTSK, CYP27B1) and an associated positive regulation of macrophages (CYP27B1, THBS1) for general helminth defense. We interpret the largely differentiated gene expression response among parasite species as general redundancy of the vertebrate immune system, which was also visible in genotype-specific responses among the different D. pseudospathaceum infections. The present study provides the first evidence that IL4-mediated activation of T-helper lymphocyte cells is also important in anti-helminthic immune responses of teleost fish.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Immune systems of vertebrates are much more diverse than previously thought, in particular at the base of the vertebrate clade. RNA-seq was used to describe in detail the transcriptomic response of stickleback hosts to infection by two helminth parasites, the trematode Diplostomum pseudospathaceum (2 genotypes plus a genotype mix) and the cestode Schistocephalus solidus. Based on a global transcription profiling, we present immune genes that are active during chronic or multiple repeated infection. We found that the transcription profiles of D. pseudospathaceum genotypes were as divergent as those of the two parasite species. When comparing the host immune response, only 5 immune genes were consistently upregulated upon infection by both species. These genes indicated a role for enhanced toll like receptor (TLR) activity (CTSK, CYP27B1) and an associated positive regulation of macrophages (CYP27B1, THBS1) for general helminth defense. We interpret the largely differentiated gene expression response among parasite species as general redundancy of the vertebrate immune system, which was also visible in genotype-specific responses among the different D. pseudospathaceum infections. The present study provides the first evidence that IL4-mediated activation of T-helper lymphocyte cells is also important in anti-helminthic immune responses of teleost fish.
Dohmen, Elias; Kremer, Lukas P. M.; Bornberg-Bauer, Erich; Kemena, Carsten
DOGMA: domain-based transcriptome and proteome quality assessment Journal Article
In: Bioinformatics, vol. 32, no. 17, pp. 2577-2581, 2016.
@article{Dohmen2016,
title = {DOGMA: domain-based transcriptome and proteome quality assessment},
author = {Elias Dohmen and Lukas P. M. Kremer and Erich Bornberg-Bauer and Carsten Kemena},
url = {https://bornberglab.org/wp-content/uploads/2021/04/dohmen2016.pdf, Download},
doi = {https://doi.org/10.1093/bioinformatics/btw231},
year = {2016},
date = {2016-05-05},
journal = {Bioinformatics},
volume = {32},
number = {17},
pages = {2577-2581},
abstract = {Motivation: Genome studies have become cheaper and easier than ever before, due to the decreased costs of high-throughput sequencing and the free availability of analysis software. However, the quality of genome or transcriptome assemblies can vary a lot. Therefore, quality assessment of assemblies and annotations are crucial aspects of genome analysis pipelines.
Results: We developed DOGMA, a program for fast and easy quality assessment of transcriptome and proteome data based on conserved protein domains. DOGMA measures the completeness of a given transcriptome or proteome and provides information about domain content for further analysis. DOGMA provides a very fast way to do quality assessment within seconds.
Availability and Implementation: DOGMA is implemented in Python and published under GNU GPL v.3 license. The source code is available on https://ebbgit.uni-muenster.de/domainWorld/DOGMA/ .},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Motivation: Genome studies have become cheaper and easier than ever before, due to the decreased costs of high-throughput sequencing and the free availability of analysis software. However, the quality of genome or transcriptome assemblies can vary a lot. Therefore, quality assessment of assemblies and annotations are crucial aspects of genome analysis pipelines.
Results: We developed DOGMA, a program for fast and easy quality assessment of transcriptome and proteome data based on conserved protein domains. DOGMA measures the completeness of a given transcriptome or proteome and provides information about domain content for further analysis. DOGMA provides a very fast way to do quality assessment within seconds.
Availability and Implementation: DOGMA is implemented in Python and published under GNU GPL v.3 license. The source code is available on https://ebbgit.uni-muenster.de/domainWorld/DOGMA/ .
Results: We developed DOGMA, a program for fast and easy quality assessment of transcriptome and proteome data based on conserved protein domains. DOGMA measures the completeness of a given transcriptome or proteome and provides information about domain content for further analysis. DOGMA provides a very fast way to do quality assessment within seconds.
Availability and Implementation: DOGMA is implemented in Python and published under GNU GPL v.3 license. The source code is available on https://ebbgit.uni-muenster.de/domainWorld/DOGMA/ .
Olsen, Jeanine L.; Rouzé, Pierre; Verhelst, Bram; Lin, Yao-Cheng; Bayer, Till; Collen, Jonas; Dattolo, Emanuela; Paoli, Emanuele De; Dittami, Simon; Maumus, Florian; Michel, Gurvan; Kersting, Anna R.; Lauritano, Chiara; Lohaus, Rolf; Töpel, Mats; Tonon, Thierry; Vanneste, Kevin; Amirebrahimi, Mojgan; Brakel, Janina; Boström, Christoffer; Chovatia, Mansi; Grimwood, Jane; Jenkins, Jerry W.; Jueterbock, Alexander; Mraz, Amy; Stam, Wytze T.; Tice, Hope; Bornberg-Bauer, Erich; Green, Pamela J.; Pearson, Gareth A.; Procaccini, Gabriele; Duarte, Carlos M.; Schmutz, Jeremy; Reusch, Thorsten B. H.; Peer, Yves Van
The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea Journal Article
In: Nature, vol. 530, pp. 331–335, 2016.
@article{Olsen2016,
title = {The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea},
author = {Jeanine L. Olsen and Pierre Rouzé and Bram Verhelst and Yao-Cheng Lin and Till Bayer and Jonas Collen and Emanuela Dattolo and Emanuele De Paoli and Simon Dittami and Florian Maumus and Gurvan Michel and Anna R. Kersting and Chiara Lauritano and Rolf Lohaus and Mats Töpel and Thierry Tonon and Kevin Vanneste and Mojgan Amirebrahimi and Janina Brakel and Christoffer Boström and Mansi Chovatia and Jane Grimwood and Jerry W. Jenkins and Alexander Jueterbock and Amy Mraz and Wytze T. Stam and Hope Tice and Erich Bornberg-Bauer and Pamela J. Green and Gareth A. Pearson and Gabriele Procaccini and Carlos M. Duarte and Jeremy Schmutz and Thorsten B. H. Reusch and Yves Van Peer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/olsen2016.pdf, Download},
doi = {doi:10.1038/nature16548},
year = {2016},
date = {2016-01-27},
journal = {Nature},
volume = {530},
pages = {331–335},
abstract = {Seagrasses colonized the sea on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet. Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae and that is important for ion homoeostasis, nutrient uptake and O2/CO2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Seagrasses colonized the sea on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet. Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae and that is important for ion homoeostasis, nutrient uptake and O2/CO2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants.
Huang, Yun; Chain, Frédéric J. J.; Panchal, Mahesh; Eizaguirre, Christophe; Kalbe, Martin; Lenz, Tobias L.; Samonte, Irene E.; Stoll, Monika; Bornberg-Bauer, Erich; Reusch, Thorsten B. H.; Milinski, Manfred; Feulner, Philine G. D.
Transcriptome profiling of immune tissues revealshabitat-specific gene expression between lake and riversticklebacks Journal Article
In: Molecular Ecology, vol. 25, pp. 943–958, 2016.
@article{Huang2016,
title = {Transcriptome profiling of immune tissues revealshabitat-specific gene expression between lake and riversticklebacks},
author = {Yun Huang and Frédéric J. J. Chain and Mahesh Panchal and Christophe Eizaguirre and Martin Kalbe and Tobias L. Lenz and Irene E. Samonte and Monika Stoll and Erich Bornberg-Bauer and Thorsten B. H. Reusch and Manfred Milinski and Philine G. D. Feulner},
url = {https://bornberglab.org/wp-content/uploads/2021/04/huang2016.pdf, Download},
doi = {https://doi.org/10.1111/mec.13520},
year = {2016},
date = {2016-01-07},
journal = {Molecular Ecology},
volume = {25},
pages = {943–958},
abstract = {The observation of habitat‐specific phenotypes suggests the action of natural selection. The three‐spined stickleback (Gasterosteus aculeatus) has repeatedly colonized and adapted to diverse freshwater habitats across the northern hemisphere since the last glaciation, while giving rise to recurring phenotypes associated with specific habitats. Parapatric lake and river populations of sticklebacks harbour distinct parasite communities, a factor proposed to contribute to adaptive differentiation between these ecotypes. However, little is known about the transcriptional response to the distinct parasite pressure of those fish in a natural setting. Here, we sampled wild‐caught sticklebacks across four geographical locations from lake and river habitats differing in their parasite load. We compared gene expression profiles between lake and river populations using 77 whole‐transcriptome libraries from two immune‐relevant tissues, the head kidney and the spleen. Differential expression analyses revealed 139 genes with habitat‐specific expression patterns across the sampled population pairs. Among the 139 differentially expressed genes, eight are annotated with an immune function and 42 have been identified as differentially expressed in previous experimental studies in which fish have been immune challenged. Together, these findings reinforce the hypothesis that parasites contribute to adaptation of sticklebacks in lake and river habitats.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The observation of habitat‐specific phenotypes suggests the action of natural selection. The three‐spined stickleback (Gasterosteus aculeatus) has repeatedly colonized and adapted to diverse freshwater habitats across the northern hemisphere since the last glaciation, while giving rise to recurring phenotypes associated with specific habitats. Parapatric lake and river populations of sticklebacks harbour distinct parasite communities, a factor proposed to contribute to adaptive differentiation between these ecotypes. However, little is known about the transcriptional response to the distinct parasite pressure of those fish in a natural setting. Here, we sampled wild‐caught sticklebacks across four geographical locations from lake and river habitats differing in their parasite load. We compared gene expression profiles between lake and river populations using 77 whole‐transcriptome libraries from two immune‐relevant tissues, the head kidney and the spleen. Differential expression analyses revealed 139 genes with habitat‐specific expression patterns across the sampled population pairs. Among the 139 differentially expressed genes, eight are annotated with an immune function and 42 have been identified as differentially expressed in previous experimental studies in which fish have been immune challenged. Together, these findings reinforce the hypothesis that parasites contribute to adaptation of sticklebacks in lake and river habitats.
2015
Bornberg-Bauer, Erich; Schmitz, Jonathan F.; Heberlein, Magdalena
Emergence of de novo proteins from "dark genomic matter" by "grow slow and moult" Journal Article
In: Biochemical Society Transactions, vol. 43, no. 5, pp. 867–873, 2015.
@article{Bornberg-Bauer2015,
title = {Emergence of de novo proteins from "dark genomic matter" by "grow slow and moult"},
author = {Erich Bornberg-Bauer and Jonathan F. Schmitz and Magdalena Heberlein},
url = {https://bornberglab.org/wp-content/uploads/2021/04/bornberg-bauer2015.pdf, Download},
doi = {https://doi.org/10.1042/BST20150089},
year = {2015},
date = {2015-10-09},
journal = {Biochemical Society Transactions},
volume = {43},
number = {5},
pages = {867–873},
abstract = {Proteins are the workhorses of the cell and, over billions of years, they have evolved an amazing plethora of extremely diverse and versatile structures with equally diverse functions. Evolutionary emergence of new proteins and transitions between existing ones are believed to be rare or even impossible. However, recent advances in comparative genomics have repeatedly called some 10%–30% of all genes without any detectable similarity to existing proteins. Even after careful scrutiny, some of those orphan genes contain protein coding reading frames with detectable transcription and translation. Thus some proteins seem to have emerged from previously non-coding ‘dark genomic matter’. These ‘de novo’ proteins tend to be disordered, fast evolving, weakly expressed but also rapidly assuming novel and physiologically important functions. Here we review mechanisms by which ‘de novo’ proteins might be created, under which circumstances they may become fixed and why they are elusive. We propose a ‘grow slow and moult’ model in which first a reading frame is extended, coding for an initially disordered and non-globular appendage which, over time, becomes more structured and may also become associated with other proteins.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Proteins are the workhorses of the cell and, over billions of years, they have evolved an amazing plethora of extremely diverse and versatile structures with equally diverse functions. Evolutionary emergence of new proteins and transitions between existing ones are believed to be rare or even impossible. However, recent advances in comparative genomics have repeatedly called some 10%–30% of all genes without any detectable similarity to existing proteins. Even after careful scrutiny, some of those orphan genes contain protein coding reading frames with detectable transcription and translation. Thus some proteins seem to have emerged from previously non-coding ‘dark genomic matter’. These ‘de novo’ proteins tend to be disordered, fast evolving, weakly expressed but also rapidly assuming novel and physiologically important functions. Here we review mechanisms by which ‘de novo’ proteins might be created, under which circumstances they may become fixed and why they are elusive. We propose a ‘grow slow and moult’ model in which first a reading frame is extended, coding for an initially disordered and non-globular appendage which, over time, becomes more structured and may also become associated with other proteins.
Haase, David; Rieger, Jennifer K.; Witten, Anika; Stoll, Monika; Bornberg-Bauer, Erich; Kalbe, Martin; Reusch, Thorsten B. H.
Immunity comes first: The effect of parasite genotypes on adaptive immunity and immunization in three-spined sticklebacks Journal Article
In: Developmental and Comparative Immunology, vol. 54, no. 1, pp. 137-144, 2015.
@article{Haase2015,
title = {Immunity comes first: The effect of parasite genotypes on adaptive immunity and immunization in three-spined sticklebacks},
author = {David Haase and Jennifer K. Rieger and Anika Witten and Monika Stoll and Erich Bornberg-Bauer and Martin Kalbe and Thorsten B. H. Reusch},
url = {https://bornberglab.org/wp-content/uploads/2021/10/haase2015.pdf, Download},
doi = {https://doi.org/10.1016/j.dci.2015.09.008},
year = {2015},
date = {2015-09-21},
journal = {Developmental and Comparative Immunology},
volume = {54},
number = {1},
pages = {137-144},
abstract = {Adaptive immunity in vertebrates can confer increased resistance against invading pathogens upon reinfection. But how specific parasite genotypes affect the temporal transition from innate to adaptive immunity under continual exposure to parasites is poorly understood. Here, we investigated the effects of homologous and heterologous exposures of genetically distinct parasite lineages of the eye fluke Diplostomum pseudospathaceum on gene expression patterns of adaptive immunity in sticklebacks (Gasterosteus aculeatus). Observable differences in gene expression were largely attributable to final exposures while there was no transcription pattern characteristic for a general response to repeated infections with D. pseudospathaceum. None of the final exposure treatments was able to erase the distinct expression patterns resulting from a heterologous pre-exposed fish. Interestingly, heterologous final exposures showed similarities between different treatment groups subjected to homologous reexposure. The observed pattern was supported by parasite infection rates and suggests that host immunization was optimized towards an adaptive immune response that favored effectiveness against parasite diversity over specificity.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Adaptive immunity in vertebrates can confer increased resistance against invading pathogens upon reinfection. But how specific parasite genotypes affect the temporal transition from innate to adaptive immunity under continual exposure to parasites is poorly understood. Here, we investigated the effects of homologous and heterologous exposures of genetically distinct parasite lineages of the eye fluke Diplostomum pseudospathaceum on gene expression patterns of adaptive immunity in sticklebacks (Gasterosteus aculeatus). Observable differences in gene expression were largely attributable to final exposures while there was no transcription pattern characteristic for a general response to repeated infections with D. pseudospathaceum. None of the final exposure treatments was able to erase the distinct expression patterns resulting from a heterologous pre-exposed fish. Interestingly, heterologous final exposures showed similarities between different treatment groups subjected to homologous reexposure. The observed pattern was supported by parasite infection rates and suggests that host immunization was optimized towards an adaptive immune response that favored effectiveness against parasite diversity over specificity.
Smith, Chris R.; Cahan, Sara Helms; Kemena, Carsten; Brady, Seán G.; Yang, Wei; Bornberg-Bauer, Erich; Eriksson, Ti; Gadau, Jürgen; Helmkampf, Martin; Gotzek, Dietrich; Miyakawa, Misato Okamoto; Suarez, Andrew V.; Mikheyev, Alexander
How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites Journal Article
In: Molecular Biology and Evolution, vol. 32, no. 11, pp. 2919–2931, 2015.
@article{Smith2015,
title = {How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites},
author = {Chris R. Smith and Sara Helms Cahan and Carsten Kemena and Seán G. Brady and Wei Yang and Erich Bornberg-Bauer and Ti Eriksson and Jürgen Gadau and Martin Helmkampf and Dietrich Gotzek and Misato Okamoto Miyakawa and Andrew V. Suarez and Alexander Mikheyev},
url = {https://bornberglab.org/wp-content/uploads/2021/04/smith2015.pdf, Download},
doi = {https://doi.org/10.1093/molbev/msv165},
year = {2015},
date = {2015-07-29},
journal = {Molecular Biology and Evolution},
volume = {32},
number = {11},
pages = {2919–2931},
abstract = {A central goal of biology is to uncover the genetic basis for the origin of new phenotypes. A particularly effective approach is to examine the genomic architecture of species that have secondarily lost a phenotype with respect to their close relatives. In the eusocial Hymenoptera, queens and workers have divergent phenotypes that may be produced via either expression of alternative sets of caste-specific genes and pathways or differences in expression patterns of a shared set of multifunctional genes. To distinguish between these two hypotheses, we investigated how secondary loss of the worker phenotype in workerless ant social parasites impacted genome evolution across two independent origins of social parasitism in the ant genera Pogonomyrmex and Vollenhovia. We sequenced the genomes of three social parasites and their most-closely related eusocial host species and compared gene losses in social parasites with gene expression differences between host queens and workers. Virtually all annotated genes were expressed to some degree in both castes of the host, with most shifting in queen-worker bias across developmental stages. As a result, despite >1 My of divergence from the last common ancestor that had workers, the social parasites showed strikingly little evidence of gene loss, damaging mutations, or shifts in selection regime resulting from loss of the worker caste. This suggests that regulatory changes within a multifunctional genome, rather than sequence differences, have played a predominant role in the evolution of social parasitism, and perhaps also in the many gains and losses of phenotypes in the social insects.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
A central goal of biology is to uncover the genetic basis for the origin of new phenotypes. A particularly effective approach is to examine the genomic architecture of species that have secondarily lost a phenotype with respect to their close relatives. In the eusocial Hymenoptera, queens and workers have divergent phenotypes that may be produced via either expression of alternative sets of caste-specific genes and pathways or differences in expression patterns of a shared set of multifunctional genes. To distinguish between these two hypotheses, we investigated how secondary loss of the worker phenotype in workerless ant social parasites impacted genome evolution across two independent origins of social parasitism in the ant genera Pogonomyrmex and Vollenhovia. We sequenced the genomes of three social parasites and their most-closely related eusocial host species and compared gene losses in social parasites with gene expression differences between host queens and workers. Virtually all annotated genes were expressed to some degree in both castes of the host, with most shifting in queen-worker bias across developmental stages. As a result, despite >1 My of divergence from the last common ancestor that had workers, the social parasites showed strikingly little evidence of gene loss, damaging mutations, or shifts in selection regime resulting from loss of the worker caste. This suggests that regulatory changes within a multifunctional genome, rather than sequence differences, have played a predominant role in the evolution of social parasitism, and perhaps also in the many gains and losses of phenotypes in the social insects.
Schüler, Andreas; Schmitz, Gregor; Reft, Abigail; Özbek, Suat; Thurm, Ulrich; Bornberg-Bauer, Erich
The rise and fall of TRP-N, an ancient family of mechanogated ion channels, in metazoan Journal Article
In: Genome Biology and Evolution, vol. 7, no. 6, pp. 1713–1727, 2015.
@article{Schüler2015,
title = {The rise and fall of TRP-N, an ancient family of mechanogated ion channels, in metazoan},
author = {Andreas Schüler and Gregor Schmitz and Abigail Reft and Suat Özbek and Ulrich Thurm and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Schuler2015.pdf, Download},
doi = {https://doi.org/10.1093/gbe/evv091},
year = {2015},
date = {2015-06-22},
journal = {Genome Biology and Evolution},
volume = {7},
number = {6},
pages = {1713–1727},
abstract = {Mechanoreception, the sensing of mechanical forces, is an ancient means of orientation and communication and tightly linked to the evolution of motile animals. In flies, the transient-receptor-potential N protein (TRP-N) was found to be a cilia-associated mechanoreceptor. TRP-N belongs to a large and diverse family of ion channels. Its unusually long N-terminal repeat of 28 ankyrin domains presumably acts as the gating spring by which mechanical energy induces channel gating. We analyzed the evolutionary origins and possible diversification of TRP-N. Using a custom-made set of highly discriminative sequence profiles we scanned a representative set of metazoan genomes and subsequently corrected several gene models. We find that, contrary to other ion channel families, TRP-N is remarkably conserved in its domain arrangements and copy number (1) in all Bilateria except for amniotes, even in the wake of several whole-genome duplications. TRP-N is absent in Porifera but present in Ctenophora and Placozoa. Exceptional multiplications of TRP-N occurred in Cnidaria, independently along the Hydra and the Nematostella lineage. Molecular signals of subfunctionalization can be attributed to different mechanisms of activation of the gating spring. In Hydra this is further supported by in situ hybridization and immune staining, suggesting that at least three paralogs adapted to nematocyte discharge, which is key for predation and defense. We propose that these new candidate proteins help explain the sensory complexity of Cnidaria which has been previously observed but so far has lacked a molecular underpinning. Also, the ancient appearance of TRP-N supports a common origin of important components of the nervous systems in Ctenophores, Cnidaria, and Bilateria.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Mechanoreception, the sensing of mechanical forces, is an ancient means of orientation and communication and tightly linked to the evolution of motile animals. In flies, the transient-receptor-potential N protein (TRP-N) was found to be a cilia-associated mechanoreceptor. TRP-N belongs to a large and diverse family of ion channels. Its unusually long N-terminal repeat of 28 ankyrin domains presumably acts as the gating spring by which mechanical energy induces channel gating. We analyzed the evolutionary origins and possible diversification of TRP-N. Using a custom-made set of highly discriminative sequence profiles we scanned a representative set of metazoan genomes and subsequently corrected several gene models. We find that, contrary to other ion channel families, TRP-N is remarkably conserved in its domain arrangements and copy number (1) in all Bilateria except for amniotes, even in the wake of several whole-genome duplications. TRP-N is absent in Porifera but present in Ctenophora and Placozoa. Exceptional multiplications of TRP-N occurred in Cnidaria, independently along the Hydra and the Nematostella lineage. Molecular signals of subfunctionalization can be attributed to different mechanisms of activation of the gating spring. In Hydra this is further supported by in situ hybridization and immune staining, suggesting that at least three paralogs adapted to nematocyte discharge, which is key for predation and defense. We propose that these new candidate proteins help explain the sensory complexity of Cnidaria which has been previously observed but so far has lacked a molecular underpinning. Also, the ancient appearance of TRP-N supports a common origin of important components of the nervous systems in Ctenophores, Cnidaria, and Bilateria.
Masri, Leila; Branca, Antoine; Sheppard, Anna E.; Papkou, Andrei; Laehnemann, David; Guenther, Patrick S.; Prahl, Swantje; Saebelfeld, Manja; Hollensteiner, Jacqueline; Liesegang, Heiko; Brzuszkiewicz, Elzbieta; Daniel, Rolf; Michiels, Nicolaas K.; Schulte, Rebecca D.; Kurtz, Joachim; Rosenstiel, Philip; Telschow, Arndt; Bornberg-Bauer, Erich; Schulenburg, Hinrich
Host-Pathogen Coevolution: The Selective Advantage of Bacillus thuringiensis Virulence and Its Cry Toxin Genes Journal Article
In: PLOS Biology, vol. 13, no. 6, 2015.
@article{Masri2015,
title = {Host-Pathogen Coevolution: The Selective Advantage of Bacillus thuringiensis Virulence and Its Cry Toxin Genes},
author = {Leila Masri and Antoine Branca and Anna E. Sheppard and Andrei Papkou and David Laehnemann and Patrick S. Guenther and Swantje Prahl and Manja Saebelfeld and Jacqueline Hollensteiner and Heiko Liesegang and Elzbieta Brzuszkiewicz and Rolf Daniel and Nicolaas K. Michiels and Rebecca D. Schulte and Joachim Kurtz and Philip Rosenstiel and Arndt Telschow and Erich Bornberg-Bauer and Hinrich Schulenburg},
url = {https://bornberglab.org/wp-content/uploads/2023/01/Masri2015.pdf, Download},
doi = {https://doi.org/10.1371/journal.pbio.1002169},
year = {2015},
date = {2015-06-04},
urldate = {2015-06-04},
journal = {PLOS Biology},
volume = {13},
number = {6},
abstract = {Reciprocal coevolution between host and pathogen is widely seen as a major driver of evolution and biological innovation. Yet, to date, the underlying genetic mechanisms and associated trait functions that are unique to rapid coevolutionary change are generally unknown. We here combined experimental evolution of the bacterial biocontrol agent Bacillus thuringiensis and its nematode host Caenorhabditis elegans with large-scale phenotyping, whole genome analysis, and functional genetics to demonstrate the selective benefit of pathogen virulence and the underlying toxin genes during the adaptation process. We show that: (i) high virulence was specifically favoured during pathogen–host coevolution rather than pathogen one-sided adaptation to a nonchanging host or to an environment without host; (ii) the pathogen genotype BT-679 with known nematocidal toxin genes and high virulence specifically swept to fixation in all of the independent replicate populations under coevolution but only some under one-sided adaptation; (iii) high virulence in the BT-679-dominated populations correlated with elevated copy numbers of the plasmid containing the nematocidal toxin genes; (iv) loss of virulence in a toxin-plasmid lacking BT-679 isolate was reconstituted by genetic reintroduction or external addition of the toxins. We conclude that sustained coevolution is distinct from unidirectional selection in shaping the pathogen's genome and life history characteristics. To our knowledge, this study is the first to characterize the pathogen genes involved in coevolutionary adaptation in an animal host–pathogen interaction system.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Reciprocal coevolution between host and pathogen is widely seen as a major driver of evolution and biological innovation. Yet, to date, the underlying genetic mechanisms and associated trait functions that are unique to rapid coevolutionary change are generally unknown. We here combined experimental evolution of the bacterial biocontrol agent Bacillus thuringiensis and its nematode host Caenorhabditis elegans with large-scale phenotyping, whole genome analysis, and functional genetics to demonstrate the selective benefit of pathogen virulence and the underlying toxin genes during the adaptation process. We show that: (i) high virulence was specifically favoured during pathogen–host coevolution rather than pathogen one-sided adaptation to a nonchanging host or to an environment without host; (ii) the pathogen genotype BT-679 with known nematocidal toxin genes and high virulence specifically swept to fixation in all of the independent replicate populations under coevolution but only some under one-sided adaptation; (iii) high virulence in the BT-679-dominated populations correlated with elevated copy numbers of the plasmid containing the nematocidal toxin genes; (iv) loss of virulence in a toxin-plasmid lacking BT-679 isolate was reconstituted by genetic reintroduction or external addition of the toxins. We conclude that sustained coevolution is distinct from unidirectional selection in shaping the pathogen's genome and life history characteristics. To our knowledge, this study is the first to characterize the pathogen genes involved in coevolutionary adaptation in an animal host–pathogen interaction system.
Bitard-Feildel, Tristan; Kemena, Carsten; Greenwood, Jenny M.; Bornberg-Bauer, Erich
Domain similarity based orthology detection Journal Article
In: BMC Bioinformatics, vol. 16, no. 154, pp. 1-11, 2015.
@article{Bitard-Feildel2015,
title = {Domain similarity based orthology detection},
author = {Tristan Bitard-Feildel and Carsten Kemena and Jenny M. Greenwood and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Feildel2015.pdf, Download},
doi = {DOI 10.1186/s12859-015-0570-8},
year = {2015},
date = {2015-05-13},
urldate = {2015-05-13},
journal = {BMC Bioinformatics},
volume = {16},
number = {154},
pages = {1-11},
abstract = {Background
Orthologous protein detection software mostly uses pairwise comparisons of amino-acid sequences to assert whether two proteins are orthologous or not. Accordingly, when the number of sequences for comparison increases, the number of comparisons to compute grows in a quadratic order. A current challenge of bioinformatic research, especially when taking into account the increasing number of sequenced organisms available, is to make this ever-growing number of comparisons computationally feasible in a reasonable amount of time. We propose to speed up the detection of orthologous proteins by using strings of domains to characterize the proteins.
Results
We present two new protein similarity measures, a cosine and a maximal weight matching score based on domain content similarity, and new software, named porthoDom. The qualities of the cosine and the maximal weight matching similarity measures are compared against curated datasets. The measures show that domain content similarities are able to correctly group proteins into their families. Accordingly, the cosine similarity measure is used inside porthoDom, the wrapper developed for proteinortho. porthoDom makes use of domain content similarity measures to group proteins together before searching for orthologs. By using domains instead of amino acid sequences, the reduction of the search space decreases the computational complexity of an all-against-all sequence comparison.
Conclusion
We demonstrate that representing and comparing proteins as strings of discrete domains, i.e. as a concatenation of their unique identifiers, allows a drastic simplification of search space. porthoDom has the advantage of speeding up orthology detection while maintaining a degree of accuracy similar to proteinortho. The implementation of porthoDom is released using python and C++ languages and is available under the GNU GPL licence 3 at http://www.bornberglab.org/pages/porthoda.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
Orthologous protein detection software mostly uses pairwise comparisons of amino-acid sequences to assert whether two proteins are orthologous or not. Accordingly, when the number of sequences for comparison increases, the number of comparisons to compute grows in a quadratic order. A current challenge of bioinformatic research, especially when taking into account the increasing number of sequenced organisms available, is to make this ever-growing number of comparisons computationally feasible in a reasonable amount of time. We propose to speed up the detection of orthologous proteins by using strings of domains to characterize the proteins.
Results
We present two new protein similarity measures, a cosine and a maximal weight matching score based on domain content similarity, and new software, named porthoDom. The qualities of the cosine and the maximal weight matching similarity measures are compared against curated datasets. The measures show that domain content similarities are able to correctly group proteins into their families. Accordingly, the cosine similarity measure is used inside porthoDom, the wrapper developed for proteinortho. porthoDom makes use of domain content similarity measures to group proteins together before searching for orthologs. By using domains instead of amino acid sequences, the reduction of the search space decreases the computational complexity of an all-against-all sequence comparison.
Conclusion
We demonstrate that representing and comparing proteins as strings of discrete domains, i.e. as a concatenation of their unique identifiers, allows a drastic simplification of search space. porthoDom has the advantage of speeding up orthology detection while maintaining a degree of accuracy similar to proteinortho. The implementation of porthoDom is released using python and C++ languages and is available under the GNU GPL licence 3 at http://www.bornberglab.org/pages/porthoda.
Orthologous protein detection software mostly uses pairwise comparisons of amino-acid sequences to assert whether two proteins are orthologous or not. Accordingly, when the number of sequences for comparison increases, the number of comparisons to compute grows in a quadratic order. A current challenge of bioinformatic research, especially when taking into account the increasing number of sequenced organisms available, is to make this ever-growing number of comparisons computationally feasible in a reasonable amount of time. We propose to speed up the detection of orthologous proteins by using strings of domains to characterize the proteins.
Results
We present two new protein similarity measures, a cosine and a maximal weight matching score based on domain content similarity, and new software, named porthoDom. The qualities of the cosine and the maximal weight matching similarity measures are compared against curated datasets. The measures show that domain content similarities are able to correctly group proteins into their families. Accordingly, the cosine similarity measure is used inside porthoDom, the wrapper developed for proteinortho. porthoDom makes use of domain content similarity measures to group proteins together before searching for orthologs. By using domains instead of amino acid sequences, the reduction of the search space decreases the computational complexity of an all-against-all sequence comparison.
Conclusion
We demonstrate that representing and comparing proteins as strings of discrete domains, i.e. as a concatenation of their unique identifiers, allows a drastic simplification of search space. porthoDom has the advantage of speeding up orthology detection while maintaining a degree of accuracy similar to proteinortho. The implementation of porthoDom is released using python and C++ languages and is available under the GNU GPL licence 3 at http://www.bornberglab.org/pages/porthoda.
Sadd, Ben M; Barribeau, Seth M; Bloch, Guy; Graaf, Dirk C; Dearden, Peter; Elsik, Christine G; Gadau, Jürgen; Grimmelikhuijzen, Cornelis JP; Hasselmann, Martin; Lozier, Jeffrey D; Robertson, Hugh M; Smagghe, Guy; Stolle, Eckart; Vaerenbergh, Matthias Van; Waterhouse, Robert M; Bornberg-Bauer, Erich; Klasberg, Steffen; Bennett, Anna K; Câmara, Francisco; Guigó, Roderic; Hoff, Katharina; Mariotti, Marco; Munoz-Torres, Monica; Murphy, Terence; Santesmasses, Didac; Amdam, Gro V; Beckers, Matthew; Beye, Martin; Biewer, Matthias; Bitondi, Márcia MG; Blaxter, Mark L; Bourke, Andrew FG; Brown, Mark JF; Buechel, Severine D; Cameron, Rossanah; Cappelle, Kaat; Carolan, James C; Christiaens, Olivier; Ciborowski, Kate L; Clarke, David F; Colgan, Thomas J; Collins, David H; Cridge, Andrew G; Dalmay, Tamas; Dreier, Stephanie; Plessis, Louis; Duncan, Elizabeth; Erler, Silvio; Evans, Jay; Falcon, Tiago; Flores, Kevin; Freitas, Flávia CP; Fuchikawa, Taro; Gempe, Tanja; Hartfelder, Klaus; Hauser, Frank; Helbing, Sophie; Humann, Fernanda C; Irvine, Frano; Jermiin, Lars S; Johnson, Claire E; Johnson, Reed M; Jones, Andrew K; Kadowaki, Tatsuhiko; Kidner, Jonathan H; Koch, Vasco; Köhler, Arian; Kraus, F Bernhard; Lattorff, H Michael G; Leask, Megan; Lockett, Gabrielle A; Mallon, Eamonn B; Antonio, David S Marco; Marxer, Monika; Meeus, Ivan; Moritz, Robin FA; Nair, Ajay; Näpflin, Kathrin; Nissen, Inga; Niu, Jinzhi; Nunes, Francis MF; Oakeshott, John G; Osborne, Amy; Otte, Marianne; Pinheiro, Daniel G; Rossié, Nina; Rueppell, Olav; Santos, Carolina G; Schmid-Hempel, Regula; Schmitt, Björn D; Schulte, Christina; Simões, Zilá LP; Soares, Michelle PM; Swevers, Luc; Winnebeck, Eva C; Wolschin, Florian; Yu, Na; Zdobnov, Evgeny M; Aqrawi, Peshtewani K; Blankenburg, Kerstin P; Coyle, Marcus; Francisco, Liezl; Hernandez, Alvaro G; Holder, Michael; Hudson, Matthew E; Jackson, LaRonda; Jayaseelan, Joy; Joshi, Vandita; Kovar, Christie; Lee, Sandra L; Mata, Robert; Mathew, Tittu; Newsham, Irene F; Ngo, Robin; Okwuonu, Geoffrey; Pham, Christopher; Pu, Ling-Ling; Saada, Nehad; Santibanez, Jireh; Simmons, DeNard; Thornton, Rebecca; Venkat, Aarti; Walden, Kimberly KO; Wu, Yuan-Qing; Debyser, Griet; Devreese, Bart; Asher, Claire; Blommaert, Julie; Chipman, Ariel D; Chittka, Lars; Fouks, Bertrand; Liu, Jisheng; O’Neill, Meaghan P; Sumner, Seirian; Puiu, Daniela; Qu, Jiaxin; Salzberg, Steven L; Scherer, Steven E; Muzny, Donna M; Richards, Stephen; Robinson, Gene E; Gibbs, Richard A; Schmid-Hempel, Paul; Worley, Kim C
The genomes of two key bumblebee species with primitive eusocial organization Journal Article
In: Genome Biology, vol. 16, no. 76, pp. 1-32, 2015.
@article{Sadd2015,
title = {The genomes of two key bumblebee species with primitive eusocial organization},
author = {Ben M Sadd and Seth M Barribeau and Guy Bloch and Dirk C Graaf and Peter Dearden and Christine G Elsik and Jürgen Gadau and Cornelis JP Grimmelikhuijzen and Martin Hasselmann and Jeffrey D Lozier and Hugh M Robertson and Guy Smagghe and Eckart Stolle and Matthias Van Vaerenbergh and Robert M Waterhouse and Erich Bornberg-Bauer and Steffen Klasberg and Anna K Bennett and Francisco Câmara and Roderic Guigó and Katharina Hoff and Marco Mariotti and Monica Munoz-Torres and Terence Murphy and Didac Santesmasses and Gro V Amdam and Matthew Beckers and Martin Beye and Matthias Biewer and Márcia MG Bitondi and Mark L Blaxter and Andrew FG Bourke and Mark JF Brown and Severine D Buechel and Rossanah Cameron and Kaat Cappelle and James C Carolan and Olivier Christiaens and Kate L Ciborowski and David F Clarke and Thomas J Colgan and David H Collins and Andrew G Cridge and Tamas Dalmay and Stephanie Dreier and Louis Plessis and Elizabeth Duncan and Silvio Erler and Jay Evans and Tiago Falcon and Kevin Flores and Flávia CP Freitas and Taro Fuchikawa and Tanja Gempe and Klaus Hartfelder and Frank Hauser and Sophie Helbing and Fernanda C Humann and Frano Irvine and Lars S Jermiin and Claire E Johnson and Reed M Johnson and Andrew K Jones and Tatsuhiko Kadowaki and Jonathan H Kidner and Vasco Koch and Arian Köhler and F Bernhard Kraus and H Michael G Lattorff and Megan Leask and Gabrielle A Lockett and Eamonn B Mallon and David S Marco Antonio and Monika Marxer and Ivan Meeus and Robin FA Moritz and Ajay Nair and Kathrin Näpflin and Inga Nissen and Jinzhi Niu and Francis MF Nunes and John G Oakeshott and Amy Osborne and Marianne Otte and Daniel G Pinheiro and Nina Rossié and Olav Rueppell and Carolina G Santos and Regula Schmid-Hempel and Björn D Schmitt and Christina Schulte and Zilá LP Simões and Michelle PM Soares and Luc Swevers and Eva C Winnebeck and Florian Wolschin and Na Yu and Evgeny M Zdobnov and Peshtewani K Aqrawi and Kerstin P Blankenburg and Marcus Coyle and Liezl Francisco and Alvaro G Hernandez and Michael Holder and Matthew E Hudson and LaRonda Jackson and Joy Jayaseelan and Vandita Joshi and Christie Kovar and Sandra L Lee and Robert Mata and Tittu Mathew and Irene F Newsham and Robin Ngo and Geoffrey Okwuonu and Christopher Pham and Ling-Ling Pu and Nehad Saada and Jireh Santibanez and DeNard Simmons and Rebecca Thornton and Aarti Venkat and Kimberly KO Walden and Yuan-Qing Wu and Griet Debyser and Bart Devreese and Claire Asher and Julie Blommaert and Ariel D Chipman and Lars Chittka and Bertrand Fouks and Jisheng Liu and Meaghan P O’Neill and Seirian Sumner and Daniela Puiu and Jiaxin Qu and Steven L Salzberg and Steven E Scherer and Donna M Muzny and Stephen Richards and Gene E Robinson and Richard A Gibbs and Paul Schmid-Hempel and Kim C Worley},
url = {https://bornberglab.org/wp-content/uploads/2021/04/sadd2015.pdf, Download},
doi = {DOI 10.1186/s13059-015-0623-3},
year = {2015},
date = {2015-04-24},
urldate = {2015-04-24},
journal = {Genome Biology},
volume = {16},
number = {76},
pages = {1-32},
abstract = {Background
The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats.
Results
We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits.
Conclusions
These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats.
Results
We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits.
Conclusions
These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.
The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats.
Results
We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits.
Conclusions
These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.
Bitard-Feildel, Tristan; Heberlein, Magdalena; Bornberg-Bauer, Erich; Callebaut, Isabelle
Detection of Orphan Domains in Drosophila using "Hydrophobic clustering analysis" Journal Article
In: Biochimie, vol. 119, pp. 244-253, 2015.
@article{Bitard-Feildel2015b,
title = {Detection of Orphan Domains in Drosophila using "Hydrophobic clustering analysis"},
author = {Tristan Bitard-Feildel and Magdalena Heberlein and Erich Bornberg-Bauer and Isabelle Callebaut},
url = {https://bornberglab.org/wp-content/uploads/2021/10/feildel20152.pdf, Download},
doi = {https://doi.org/10.1016/j.biochi.2015.02.019},
year = {2015},
date = {2015-02-28},
journal = {Biochimie},
volume = {119},
pages = {244-253},
abstract = {Introduction
Comparative genomics has become an important strategy in life science research. While many genes, and the proteins they code for, can be well characterized by assigning orthologs, a significant amount of proteins or domains remain obscure “orphans”. Some orphans are overlooked by current computational methods because they rapidly diverged, others emerged relatively recently (de novo). Recent research has demonstrated the importance of orphans, and of de novo proteins and domains for development of new phenotypic traits and adaptation. New approaches for detecting novel domains are thus of paramount importance.
Results
The hydrophobic cluster analysis (HCA) method delineates globular-like domains from the information of a protein sequence and thereby allows bypassing some of the established methods limitations based on conserved sequence similarity. In this study, HCA is tested for orphan domain detection on 12 Drosophila genomes. After their detection, the oprhan domains are classified into two categories, depending on their presence/absence in distantly related species. The two categories show significantly different physico-chemical properties when compared to previously characterized domains from the Pfam database. The newly detected domains have a higher degree of intrinsic disorder and a particular hydrophobic cluster composition. The older the domains are, the more similar their hydrophobic cluster content is to the cluster content of Pfam domains. The results suggest that, over time, newly created domains acquire a canonical set of hydrophobic clusters but conserve some features of intrinsically disordered regions.
Conclusion
Our results agree with previous findings on orphan domains and suggest that the physico-chemical properties of domains change over evolutionary long time scale. The presented HCA-based method is able to detect domains with unusual properties without relying on prior knowledge, such as the availability of homologs. Therefore, the method has large potential for complementing existing strategies to annotate genomes, and for better understanding how molecular features emerge.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Introduction
Comparative genomics has become an important strategy in life science research. While many genes, and the proteins they code for, can be well characterized by assigning orthologs, a significant amount of proteins or domains remain obscure “orphans”. Some orphans are overlooked by current computational methods because they rapidly diverged, others emerged relatively recently (de novo). Recent research has demonstrated the importance of orphans, and of de novo proteins and domains for development of new phenotypic traits and adaptation. New approaches for detecting novel domains are thus of paramount importance.
Results
The hydrophobic cluster analysis (HCA) method delineates globular-like domains from the information of a protein sequence and thereby allows bypassing some of the established methods limitations based on conserved sequence similarity. In this study, HCA is tested for orphan domain detection on 12 Drosophila genomes. After their detection, the oprhan domains are classified into two categories, depending on their presence/absence in distantly related species. The two categories show significantly different physico-chemical properties when compared to previously characterized domains from the Pfam database. The newly detected domains have a higher degree of intrinsic disorder and a particular hydrophobic cluster composition. The older the domains are, the more similar their hydrophobic cluster content is to the cluster content of Pfam domains. The results suggest that, over time, newly created domains acquire a canonical set of hydrophobic clusters but conserve some features of intrinsically disordered regions.
Conclusion
Our results agree with previous findings on orphan domains and suggest that the physico-chemical properties of domains change over evolutionary long time scale. The presented HCA-based method is able to detect domains with unusual properties without relying on prior knowledge, such as the availability of homologs. Therefore, the method has large potential for complementing existing strategies to annotate genomes, and for better understanding how molecular features emerge.
Comparative genomics has become an important strategy in life science research. While many genes, and the proteins they code for, can be well characterized by assigning orthologs, a significant amount of proteins or domains remain obscure “orphans”. Some orphans are overlooked by current computational methods because they rapidly diverged, others emerged relatively recently (de novo). Recent research has demonstrated the importance of orphans, and of de novo proteins and domains for development of new phenotypic traits and adaptation. New approaches for detecting novel domains are thus of paramount importance.
Results
The hydrophobic cluster analysis (HCA) method delineates globular-like domains from the information of a protein sequence and thereby allows bypassing some of the established methods limitations based on conserved sequence similarity. In this study, HCA is tested for orphan domain detection on 12 Drosophila genomes. After their detection, the oprhan domains are classified into two categories, depending on their presence/absence in distantly related species. The two categories show significantly different physico-chemical properties when compared to previously characterized domains from the Pfam database. The newly detected domains have a higher degree of intrinsic disorder and a particular hydrophobic cluster composition. The older the domains are, the more similar their hydrophobic cluster content is to the cluster content of Pfam domains. The results suggest that, over time, newly created domains acquire a canonical set of hydrophobic clusters but conserve some features of intrinsically disordered regions.
Conclusion
Our results agree with previous findings on orphan domains and suggest that the physico-chemical properties of domains change over evolutionary long time scale. The presented HCA-based method is able to detect domains with unusual properties without relying on prior knowledge, such as the availability of homologs. Therefore, the method has large potential for complementing existing strategies to annotate genomes, and for better understanding how molecular features emerge.
Feulner, Philine G. D.; Chain, Frédéric J. J.; Panchal, Mahesh; Huang, Yun; Eizaguirre, Christophe; Kalbe, Martin; Lenz, Tobias L.; Samonte, Irene E.; Stoll, Monika; Bornberg-Bauer, Erich; Reusch, Thorsten B. H.; Milinski, Manfred
Genomics of Divergence along a Continuum of Parapatric Population Differentiation Journal Article
In: PLOS Genetics, vol. 11, no. 7, 2015.
@article{Feulner2015,
title = {Genomics of Divergence along a Continuum of Parapatric Population Differentiation},
author = {Philine G. D. Feulner and Frédéric J. J. Chain and Mahesh Panchal and Yun Huang and Christophe Eizaguirre and Martin Kalbe and Tobias L. Lenz and Irene E. Samonte and Monika Stoll and Erich Bornberg-Bauer and Thorsten B. H. Reusch and Manfred Milinski},
url = {https://bornberglab.org/wp-content/uploads/2023/01/Feulner2015.pdf, Download},
doi = {https://doi.org/10.1371/journal.pgen.1005414},
year = {2015},
date = {2015-02-13},
urldate = {2015-02-13},
journal = {PLOS Genetics},
volume = {11},
number = {7},
abstract = {The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation.
Kemena, Carsten; Bitard-Feildel, Tristan; Bornberg-Bauer, Erich
MDAT- Aligning multiple domain arrangements Journal Article
In: BMC Bioinformatics, vol. 16, no. 19, pp. 1-7, 2015.
@article{Kemena2015,
title = {MDAT- Aligning multiple domain arrangements},
author = {Carsten Kemena and Tristan Bitard-Feildel and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Kemena2015.pdf, Download},
doi = {DOI 10.1186/s12859-014-0442-7},
year = {2015},
date = {2015-01-28},
urldate = {2015-01-28},
journal = {BMC Bioinformatics},
volume = {16},
number = {19},
pages = {1-7},
abstract = {Background
Proteins are composed of domains, protein segments that fold independently from the rest of the protein and have a specific function. During evolution the arrangement of domains can change: domains are gained, lost or their order is rearranged. To facilitate the analysis of these changes we propose the use of multiple domain alignments.
Results
We developed an alignment program, called MDAT, which aligns multiple domain arrangements. MDAT extends earlier programs which perform pairwise alignments of domain arrangements. MDAT uses a domain similarity matrix to score domain pairs and aligns the domain arrangements using a consistency supported progressive alignment method.
Conclusion
MDAT will be useful for analysing changes in domain arrangements within and between protein families and will thus provide valuable insights into the evolution of proteins and their domains. MDAT is coded in C++, and the source code is freely available for download at http://www.bornberglab.org/pages/mdat.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
Proteins are composed of domains, protein segments that fold independently from the rest of the protein and have a specific function. During evolution the arrangement of domains can change: domains are gained, lost or their order is rearranged. To facilitate the analysis of these changes we propose the use of multiple domain alignments.
Results
We developed an alignment program, called MDAT, which aligns multiple domain arrangements. MDAT extends earlier programs which perform pairwise alignments of domain arrangements. MDAT uses a domain similarity matrix to score domain pairs and aligns the domain arrangements using a consistency supported progressive alignment method.
Conclusion
MDAT will be useful for analysing changes in domain arrangements within and between protein families and will thus provide valuable insights into the evolution of proteins and their domains. MDAT is coded in C++, and the source code is freely available for download at http://www.bornberglab.org/pages/mdat.
Proteins are composed of domains, protein segments that fold independently from the rest of the protein and have a specific function. During evolution the arrangement of domains can change: domains are gained, lost or their order is rearranged. To facilitate the analysis of these changes we propose the use of multiple domain alignments.
Results
We developed an alignment program, called MDAT, which aligns multiple domain arrangements. MDAT extends earlier programs which perform pairwise alignments of domain arrangements. MDAT uses a domain similarity matrix to score domain pairs and aligns the domain arrangements using a consistency supported progressive alignment method.
Conclusion
MDAT will be useful for analysing changes in domain arrangements within and between protein families and will thus provide valuable insights into the evolution of proteins and their domains. MDAT is coded in C++, and the source code is freely available for download at http://www.bornberglab.org/pages/mdat.
2014
Schrader, Lukas; Kim, Jay W.; Ence, Daniel; Zimin, Aleksey; Klein, Antonia; Wyschetzki, Katharina; Weichselgartner, Tobias; Kemena, Carsten; Stökl, Johannes; Schultner, Eva; Wurm, Yannick; Smith, Christopher D.; Yandell, Mark; Heinze, Jürgen; Gadau, Jürgen; Oettler, Jan
Transposable element islands facilitate adaptation to novel environments in an invasive species Journal Article
In: Nature Communications, vol. 5, no. 5495, pp. 1-10, 2014.
@article{Schrader2014,
title = {Transposable element islands facilitate adaptation to novel environments in an invasive species},
author = {Lukas Schrader and Jay W. Kim and Daniel Ence and Aleksey Zimin and Antonia Klein and Katharina Wyschetzki and Tobias Weichselgartner and Carsten Kemena and Johannes Stökl and Eva Schultner and Yannick Wurm and Christopher D. Smith and Mark Yandell and Jürgen Heinze and Jürgen Gadau and Jan Oettler},
url = {https://bornberglab.org/wp-content/uploads/2021/04/schrader2014.pdf, Download},
doi = {10.1038/ncomms6495},
year = {2014},
date = {2014-12-16},
urldate = {2014-12-16},
journal = {Nature Communications},
volume = {5},
number = {5495},
pages = {1-10},
abstract = {Adaptation requires genetic variation, but founder populations are generally genetically depleted. Here we sequence two populations of an inbred ant that diverge in phenotype to determine how variability is generated. Cardiocondyla obscurior has the smallest of the sequenced ant genomes and its structure suggests a fundamental role of transposable elements (TEs) in adaptive evolution. Accumulations of TEs (TE islands) comprising 7.18% of the genome evolve faster than other regions with regard to single-nucleotide variants, gene/exon duplications and deletions and gene homology. A non-random distribution of gene families, larvae/adult specific gene expression and signs of differential methylation in TE islands indicate intragenomic differences in regulation, evolutionary rates and coalescent effective population size. Our study reveals a tripartite interplay between TEs, life history and adaptation in an invasive species.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Adaptation requires genetic variation, but founder populations are generally genetically depleted. Here we sequence two populations of an inbred ant that diverge in phenotype to determine how variability is generated. Cardiocondyla obscurior has the smallest of the sequenced ant genomes and its structure suggests a fundamental role of transposable elements (TEs) in adaptive evolution. Accumulations of TEs (TE islands) comprising 7.18% of the genome evolve faster than other regions with regard to single-nucleotide variants, gene/exon duplications and deletions and gene homology. A non-random distribution of gene families, larvae/adult specific gene expression and signs of differential methylation in TE islands indicate intragenomic differences in regulation, evolutionary rates and coalescent effective population size. Our study reveals a tripartite interplay between TEs, life history and adaptation in an invasive species.
Kersting, Anna R.; Mizrachi, Eshchar; Bornberg-Bauer, Erich; Myburg, Alexander A.
Protein domain evolution is associated with reproductive diversification and adaptive radiation in the basal rosid Eucalyptus grandis Journal Article
In: New Phytologist, vol. 206, no. 4, pp. 1328-1336, 2014.
@article{Kersting2014,
title = {Protein domain evolution is associated with reproductive diversification and adaptive radiation in the basal rosid Eucalyptus grandis},
author = {Anna R. Kersting and Eshchar Mizrachi and Erich Bornberg-Bauer and Alexander A. Myburg},
url = {https://bornberglab.org/wp-content/uploads/2021/04/kersting2014.pdf, Download},
doi = {https://doi.org/10.1111/nph.13211},
year = {2014},
date = {2014-12-11},
journal = {New Phytologist},
volume = {206},
number = {4},
pages = {1328-1336},
abstract = {Eucalyptus is a pivotal genus within the rosid order Myrtales with distinct geographic history and adaptations. Comparative analysis of protein domain evolution in the newly sequenced Eucalyptus grandis genome and other rosid lineages sheds light on the adaptive mechanisms integral to the success of this genus of woody perennials.
We reconstructed the ancestral domain content to elucidate the gain, loss and expansion of protein domains and domain arrangements in Eucalyptus in the context of rosid phylogeny. We used functional gene ontology (GO) annotation of genes to investigate the possible biological and evolutionary consequences of protein domain expansion.
We found that protein modulation within the angiosperms occurred primarily on the level of expansion of certain domains and arrangements. Using RNA‐Seq data from E. grandis, we showed that domain expansions have contributed to tissue‐specific expression of tandemly duplicated genes.
Our results indicate that tandem duplication of genes, a key feature of the Eucalyptus genome, has played an important role in the expansion of domains, particularly in proteins related to the specialization of reproduction and biotic and abiotic interactions affecting root and floral biology, and that tissue‐specific expression of proteins with expanded domains has facilitated subfunctionalization in domain families.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Eucalyptus is a pivotal genus within the rosid order Myrtales with distinct geographic history and adaptations. Comparative analysis of protein domain evolution in the newly sequenced Eucalyptus grandis genome and other rosid lineages sheds light on the adaptive mechanisms integral to the success of this genus of woody perennials.
We reconstructed the ancestral domain content to elucidate the gain, loss and expansion of protein domains and domain arrangements in Eucalyptus in the context of rosid phylogeny. We used functional gene ontology (GO) annotation of genes to investigate the possible biological and evolutionary consequences of protein domain expansion.
We found that protein modulation within the angiosperms occurred primarily on the level of expansion of certain domains and arrangements. Using RNA‐Seq data from E. grandis, we showed that domain expansions have contributed to tissue‐specific expression of tandemly duplicated genes.
Our results indicate that tandem duplication of genes, a key feature of the Eucalyptus genome, has played an important role in the expansion of domains, particularly in proteins related to the specialization of reproduction and biotic and abiotic interactions affecting root and floral biology, and that tissue‐specific expression of proteins with expanded domains has facilitated subfunctionalization in domain families.
We reconstructed the ancestral domain content to elucidate the gain, loss and expansion of protein domains and domain arrangements in Eucalyptus in the context of rosid phylogeny. We used functional gene ontology (GO) annotation of genes to investigate the possible biological and evolutionary consequences of protein domain expansion.
We found that protein modulation within the angiosperms occurred primarily on the level of expansion of certain domains and arrangements. Using RNA‐Seq data from E. grandis, we showed that domain expansions have contributed to tissue‐specific expression of tandemly duplicated genes.
Our results indicate that tandem duplication of genes, a key feature of the Eucalyptus genome, has played an important role in the expansion of domains, particularly in proteins related to the specialization of reproduction and biotic and abiotic interactions affecting root and floral biology, and that tissue‐specific expression of proteins with expanded domains has facilitated subfunctionalization in domain families.
Chain, Frédéric J. J.; Feulner, Philine G. D.; Panchal, Mahesh; Eizaguirre, Christophe; Samonte, Irene E.; Kalbe, Martin; Lenz, Tobias L.; Stoll, Monika; Bornberg-Bauer, Erich; Milinski, Manfred; Reusch, Thorsten B. H.
Extensive Copy-Number Variation of Young Genes across Stickleback Populations Journal Article
In: PLOS Genetics, vol. 10, no. 12, 2014.
@article{Chain2014,
title = {Extensive Copy-Number Variation of Young Genes across Stickleback Populations},
author = {Frédéric J. J. Chain and Philine G. D. Feulner and Mahesh Panchal and Christophe Eizaguirre and Irene E. Samonte and Martin Kalbe and Tobias L. Lenz and Monika Stoll and Erich Bornberg-Bauer and Manfred Milinski and Thorsten B. H. Reusch},
url = {https://bornberglab.org/wp-content/uploads/2023/01/Chain2014.pdf, Download},
doi = {https://doi.org/10.1371/journal.pgen.1004830},
year = {2014},
date = {2014-12-04},
urldate = {2014-12-04},
journal = {PLOS Genetics},
volume = {10},
number = {12},
abstract = {Duplicate genes emerge as copy-number variations (CNVs) at the population level, and remain copy-number polymorphic until they are fixed or lost. The successful establishment of such structural polymorphisms in the genome plays an important role in evolution by promoting genetic diversity, complexity and innovation. To characterize the early evolutionary stages of duplicate genes and their potential adaptive benefits, we combine comparative genomics with population genomics analyses to evaluate the distribution and impact of CNVs across natural populations of an eco-genomic model, the three-spined stickleback. With whole genome sequences of 66 individuals from populations inhabiting three distinct habitats, we find that CNVs generally occur at low frequencies and are often only found in one of the 11 populations surveyed. A subset of CNVs, however, displays copy-number differentiation between populations, showing elevated within-population frequencies consistent with local adaptation. By comparing teleost genomes to identify lineage-specific genes and duplications in sticklebacks, we highlight rampant gene content differences among individuals in which over 30% of young duplicate genes are CNVs. These CNV genes are evolving rapidly at the molecular level and are enriched with functional categories associated with environmental interactions, depicting the dynamic early copy-number polymorphic stage of genes during},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Duplicate genes emerge as copy-number variations (CNVs) at the population level, and remain copy-number polymorphic until they are fixed or lost. The successful establishment of such structural polymorphisms in the genome plays an important role in evolution by promoting genetic diversity, complexity and innovation. To characterize the early evolutionary stages of duplicate genes and their potential adaptive benefits, we combine comparative genomics with population genomics analyses to evaluate the distribution and impact of CNVs across natural populations of an eco-genomic model, the three-spined stickleback. With whole genome sequences of 66 individuals from populations inhabiting three distinct habitats, we find that CNVs generally occur at low frequencies and are often only found in one of the 11 populations surveyed. A subset of CNVs, however, displays copy-number differentiation between populations, showing elevated within-population frequencies consistent with local adaptation. By comparing teleost genomes to identify lineage-specific genes and duplications in sticklebacks, we highlight rampant gene content differences among individuals in which over 30% of young duplicate genes are CNVs. These CNV genes are evolving rapidly at the molecular level and are enriched with functional categories associated with environmental interactions, depicting the dynamic early copy-number polymorphic stage of genes during
Haase, David; Rieger, Jennifer K.; Witten, Anika; Stoll, Monika; Bornberg-Bauer, Erich; Kalbe, Martin; Reusch, Thorsten B. H.
Specific Gene Expression Responses to Parasite Genotypes Reveal Redundancy of Innate Immunity in Vertebrates Journal Article
In: PLOS One, vol. 9, no. 9, 2014.
@article{Haase2014,
title = {Specific Gene Expression Responses to Parasite Genotypes Reveal Redundancy of Innate Immunity in Vertebrates},
author = {David Haase and Jennifer K. Rieger and Anika Witten and Monika Stoll and Erich Bornberg-Bauer and Martin Kalbe and Thorsten B. H. Reusch},
url = {https://bornberglab.org/wp-content/uploads/2021/04/haase2014.pdf, Download},
doi = {https://doi.org/10.1371/journal.pone.0108001},
year = {2014},
date = {2014-09-25},
journal = {PLOS One},
volume = {9},
number = {9},
abstract = {Vertebrate innate immunity is the first line of defense against an invading pathogen and has long been assumed to be largely unspecific with respect to parasite/pathogen species. However, recent phenotypic evidence suggests that immunogenetic variation, i.e. allelic variability in genes associated with the immune system, results in host-parasite genotype-by-genotype interactions and thus specific innate immune responses. Immunogenetic variation is common in all vertebrate taxa and this reflects an effective immunological function in complex environments. However, the underlying variability in host gene expression patterns as response of innate immunity to within-species genetic diversity of macroparasites in vertebrates is unknown. We hypothesized that intra-specific variation among parasite genotypes must be reflected in host gene expression patterns. Here we used high-throughput RNA-sequencing to examine the effect of parasite genotypes on gene expression patterns of a vertebrate host, the three-spined stickleback (Gasterosteus aculeatus). By infecting naïve fish with distinct trematode genotypes of the species Diplostomum pseudospathaceum we show that gene activity of innate immunity in three-spined sticklebacks depended on the identity of an infecting macroparasite genotype. In addition to a suite of genes indicative for a general response against the trematode we also find parasite-strain specific gene expression, in particular in the complement system genes, despite similar infection rates of single clone treatments. The observed discrepancy between infection rates and gene expression indicates the presence of alternative pathways which execute similar functions. This suggests that the innate immune system can induce redundant responses specific to parasite genotypes.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Vertebrate innate immunity is the first line of defense against an invading pathogen and has long been assumed to be largely unspecific with respect to parasite/pathogen species. However, recent phenotypic evidence suggests that immunogenetic variation, i.e. allelic variability in genes associated with the immune system, results in host-parasite genotype-by-genotype interactions and thus specific innate immune responses. Immunogenetic variation is common in all vertebrate taxa and this reflects an effective immunological function in complex environments. However, the underlying variability in host gene expression patterns as response of innate immunity to within-species genetic diversity of macroparasites in vertebrates is unknown. We hypothesized that intra-specific variation among parasite genotypes must be reflected in host gene expression patterns. Here we used high-throughput RNA-sequencing to examine the effect of parasite genotypes on gene expression patterns of a vertebrate host, the three-spined stickleback (Gasterosteus aculeatus). By infecting naïve fish with distinct trematode genotypes of the species Diplostomum pseudospathaceum we show that gene activity of innate immunity in three-spined sticklebacks depended on the identity of an infecting macroparasite genotype. In addition to a suite of genes indicative for a general response against the trematode we also find parasite-strain specific gene expression, in particular in the complement system genes, despite similar infection rates of single clone treatments. The observed discrepancy between infection rates and gene expression indicates the presence of alternative pathways which execute similar functions. This suggests that the innate immune system can induce redundant responses specific to parasite genotypes.
Myburg, Alexander A.; Grattapaglia, Dario; Tuskan, Gerald A.; Hellsten, Uffe; Hayes, Richard D.; Grimwood, Jane; Jenkins, Jerry; Lindquist, Erika; Tice, Hope; Bauer, Diane; Goodstein, David M.; Dubchak, Inna; Poliakov, Alexandre; Mizrachi, Eshchar; Kullan, Anand R. K.; Hussey, Steven G.; Pinard, Desre; Merwe, Karen; Singh, Pooja; Jaarsveld, Ida; Silva-Junior, Orzenil B.; Togawa, Roberto C.; Pappas, Marilia R.; Faria, Danielle A.; Sansaloni, Carolina P.; Petroli, Cesar D.; Yang, Xiaohan; Ranjan, Priya; Tschaplinski, Timothy J.; Ye, Chu-Yu; Li, Ting; Sterck, Lieven; Vanneste, Kevin; Murat, Florent; Soler, Marçal; Clemente, Hélène San; Saidi, Naijib; Cassan-Wang, Hua; Dunand, Christophe; Hefer, Charles A.; Bornberg-Bauer, Erich; Kersting, Anna R.; Vining, Kelly; Amarasinghe, Vindhya; Ranik, Martin; Naithani, Sushma; Elser, Justin; Boyd, Alexander E.; Liston, Aaron; Spatafora, Joseph W.; Dharmwardhana, Palitha; Raja, Rajani; Sullivan, Christopher; Romanel, Elisson; Alves-Ferreira, Marcio; Külheim, Carsten; Foley, William; Carocha, Victor; Paiva, Jorge; Kudrna, David; Brommonschenkel, Sergio H.; Pasquali, Giancarlo; Byrne, Margaret; Rigault, Philippe; Tibbits, Josquin; Spokevicius, Antanas; Jones, Rebecca C.; Steane, Dorothy A.; Vaillancourt, René E.; Potts, Brad M.; Joubert, Fourie; Barry, Kerrie; Pappas, Georgios J.; Strauss, Steven H.; Jaiswal, Pankaj; Grima-Pettenati, Jacqueline; Salse, Jérôme; Peer, Yves Van; Rokhsar, Daniel S.; Schmutz, Jeremy
The genome of Eucalyptus grandis Journal Article
In: Nature, vol. 510, pp. 356–362, 2014.
@article{Myburg2014,
title = {The genome of Eucalyptus grandis},
author = {Alexander A. Myburg and Dario Grattapaglia and Gerald A. Tuskan and Uffe Hellsten and Richard D. Hayes and Jane Grimwood and Jerry Jenkins and Erika Lindquist and Hope Tice and Diane Bauer and David M. Goodstein and Inna Dubchak and Alexandre Poliakov and Eshchar Mizrachi and Anand R. K. Kullan and Steven G. Hussey and Desre Pinard and Karen Merwe and Pooja Singh and Ida Jaarsveld and Orzenil B. Silva-Junior and Roberto C. Togawa and Marilia R. Pappas and Danielle A. Faria and Carolina P. Sansaloni and Cesar D. Petroli and Xiaohan Yang and Priya Ranjan and Timothy J. Tschaplinski and Chu-Yu Ye and Ting Li and Lieven Sterck and Kevin Vanneste and Florent Murat and Marçal Soler and Hélène San Clemente and Naijib Saidi and Hua Cassan-Wang and Christophe Dunand and Charles A. Hefer and Erich Bornberg-Bauer and Anna R. Kersting and Kelly Vining and Vindhya Amarasinghe and Martin Ranik and Sushma Naithani and Justin Elser and Alexander E. Boyd and Aaron Liston and Joseph W. Spatafora and Palitha Dharmwardhana and Rajani Raja and Christopher Sullivan and Elisson Romanel and Marcio Alves-Ferreira and Carsten Külheim and William Foley and Victor Carocha and Jorge Paiva and David Kudrna and Sergio H. Brommonschenkel and Giancarlo Pasquali and Margaret Byrne and Philippe Rigault and Josquin Tibbits and Antanas Spokevicius and Rebecca C. Jones and Dorothy A. Steane and René E. Vaillancourt and Brad M. Potts and Fourie Joubert and Kerrie Barry and Georgios J. Pappas and Steven H. Strauss and Pankaj Jaiswal and Jacqueline Grima-Pettenati and Jérôme Salse and Yves Van Peer and Daniel S. Rokhsar and Jeremy Schmutz},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Myburg2014.pdf, Download},
doi = {10.1038/nature13308},
year = {2014},
date = {2014-06-11},
journal = {Nature},
volume = {510},
pages = {356–362},
abstract = {Eucalypts are the world’s most widely planted hardwood trees. Their outstanding diversity, adaptability and growth have made them a global renewable resource of fibre and energy. We sequenced and assembled >94% of the 640-megabase genome of Eucalyptus grandis. Of 36,376 predicted protein-coding genes, 34% occur in tandem duplications, the largest proportion thus far in plant genomes. Eucalyptus also shows the highest diversity of genes for specialized metabolites such as terpenes that act as chemical defence and provide unique pharmaceutical oils. Genome sequencing of the E. grandis sister species E. globulus and a set of inbred E. grandis tree genomes reveals dynamic genome evolution and hotspots of inbreeding depression. The E. grandis genome is the first reference for the eudicot order Myrtales and is placed here sister to the eurosids. This resource expands our understanding of the unique biology of large woody perennials and provides a powerful tool to accelerate comparative biology, breeding and biotechnology.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Eucalypts are the world’s most widely planted hardwood trees. Their outstanding diversity, adaptability and growth have made them a global renewable resource of fibre and energy. We sequenced and assembled >94% of the 640-megabase genome of Eucalyptus grandis. Of 36,376 predicted protein-coding genes, 34% occur in tandem duplications, the largest proportion thus far in plant genomes. Eucalyptus also shows the highest diversity of genes for specialized metabolites such as terpenes that act as chemical defence and provide unique pharmaceutical oils. Genome sequencing of the E. grandis sister species E. globulus and a set of inbred E. grandis tree genomes reveals dynamic genome evolution and hotspots of inbreeding depression. The E. grandis genome is the first reference for the eudicot order Myrtales and is placed here sister to the eurosids. This resource expands our understanding of the unique biology of large woody perennials and provides a powerful tool to accelerate comparative biology, breeding and biotechnology.
Behrens, Sarah; Peuß, Robert; Milutinović, Barbara; Eggert, Hendrik; Esser, Daniela; Rosenstiel, Philip; Schulenburg, Hinrich; Bornberg-Bauer, Erich; Kurtz, Joachim
Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis Journal Article
In: BMC Genomics, vol. 15, no. 445, pp. 1-17, 2014.
@article{Behrens2014,
title = {Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis},
author = {Sarah Behrens and Robert Peuß and Barbara Milutinović and Hendrik Eggert and Daniela Esser and Philip Rosenstiel and Hinrich Schulenburg and Erich Bornberg-Bauer and Joachim Kurtz},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Behrens2014.pdf, Download},
doi = {10.1186/1471-2164-15-445},
year = {2014},
date = {2014-06-07},
urldate = {2014-06-07},
journal = {BMC Genomics},
volume = {15},
number = {445},
pages = {1-17},
abstract = {Background
Pathogens can infect their hosts through different routes. For studying the consequences for host resistance, we here used the entomopathogen Bacillus thuringiensis and the red flour beetle Tribolium castaneum for oral and systemic (i. e. pricking the cuticle) experimental infection. In order to characterize the molecular mechanisms underpinning the two different infection routes, the transcriptomes of beetles of two different T. castaneum populations – one recently collected population (Cro1) and a commonly used laboratory strain (SB) – were analyzed using a next generation RNA sequencing approach.
Results
The genetically more diverse population Cro1 showed a significantly larger number of differentially expressed genes. While both populations exhibited similar reactions to pricking, their expression patterns in response to oral infection differed remarkably. In particular, the Cro1 population showed a strong response of cuticular proteins and developmental genes, which might indicate an adaptive developmental flexibility that was lost in the SB population presumably as a result of inbreeding. The immune response of SB was primarily based on antimicrobial peptides, while Cro1 relied on responses mediated by phenoloxidase and reactive oxygen species, which may explain the higher resistance of this strain against oral infection.
Conclusions
Our data demonstrate that immunological and physiological processes underpinning the two different routes of infection are clearly distinct, and that host populations particularly differ in responses to oral infection. Furthermore, gene expression upon pricking infection entailed a strong signal of wounding, highlighting the importance of pricking controls in future infection studies.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
Pathogens can infect their hosts through different routes. For studying the consequences for host resistance, we here used the entomopathogen Bacillus thuringiensis and the red flour beetle Tribolium castaneum for oral and systemic (i. e. pricking the cuticle) experimental infection. In order to characterize the molecular mechanisms underpinning the two different infection routes, the transcriptomes of beetles of two different T. castaneum populations – one recently collected population (Cro1) and a commonly used laboratory strain (SB) – were analyzed using a next generation RNA sequencing approach.
Results
The genetically more diverse population Cro1 showed a significantly larger number of differentially expressed genes. While both populations exhibited similar reactions to pricking, their expression patterns in response to oral infection differed remarkably. In particular, the Cro1 population showed a strong response of cuticular proteins and developmental genes, which might indicate an adaptive developmental flexibility that was lost in the SB population presumably as a result of inbreeding. The immune response of SB was primarily based on antimicrobial peptides, while Cro1 relied on responses mediated by phenoloxidase and reactive oxygen species, which may explain the higher resistance of this strain against oral infection.
Conclusions
Our data demonstrate that immunological and physiological processes underpinning the two different routes of infection are clearly distinct, and that host populations particularly differ in responses to oral infection. Furthermore, gene expression upon pricking infection entailed a strong signal of wounding, highlighting the importance of pricking controls in future infection studies.
Pathogens can infect their hosts through different routes. For studying the consequences for host resistance, we here used the entomopathogen Bacillus thuringiensis and the red flour beetle Tribolium castaneum for oral and systemic (i. e. pricking the cuticle) experimental infection. In order to characterize the molecular mechanisms underpinning the two different infection routes, the transcriptomes of beetles of two different T. castaneum populations – one recently collected population (Cro1) and a commonly used laboratory strain (SB) – were analyzed using a next generation RNA sequencing approach.
Results
The genetically more diverse population Cro1 showed a significantly larger number of differentially expressed genes. While both populations exhibited similar reactions to pricking, their expression patterns in response to oral infection differed remarkably. In particular, the Cro1 population showed a strong response of cuticular proteins and developmental genes, which might indicate an adaptive developmental flexibility that was lost in the SB population presumably as a result of inbreeding. The immune response of SB was primarily based on antimicrobial peptides, while Cro1 relied on responses mediated by phenoloxidase and reactive oxygen species, which may explain the higher resistance of this strain against oral infection.
Conclusions
Our data demonstrate that immunological and physiological processes underpinning the two different routes of infection are clearly distinct, and that host populations particularly differ in responses to oral infection. Furthermore, gene expression upon pricking infection entailed a strong signal of wounding, highlighting the importance of pricking controls in future infection studies.
Terrapon, Nicolas; Li, Cai; Robertson, Hugh M.; Ji, Lu; Meng, Xuehong; Booth, Warren; Chen, Zhensheng; Childers, Christopher P.; Glastad, Karl M.; Gokhale, Kaustubh; Gowin, Johannes; Gronenberg, Wulfila; Hermansen, Russell A.; Hu, Haofu; Hunt, Brendan G.; Huylmans, Ann K.; Khalil, Sayed M. S.; Mitchell, Robert D.; Munoz-Torres, Monica C.; Mustard, Julie A.; Pan, Hailin; Reese, Justin T.; Scharf, Michael E.; Sun, Fengming; Vogel, Heiko; Xiao, Jin; Yang, Wei; Yang, Zhikai; Yang, Zuoquan; Zhou, Jiajian; Zhu, Jiwei; Brent, Colin S.; Elsik, Christine G.; Goodisman, Michael A. D.; Liberles, David A.; Roe, R. Michael; Vargo, Edward L.; Vilcinskas, Andreas; Wang, Jun; Bornberg-Bauer, Erich; Korb, Judith; Zhang, Guojie; Liebig, Jürgen
Molecular traces of alternative social organization in a termite genome Journal Article
In: Nature Communications, vol. 5, no. 3636, pp. 1-12, 2014.
@article{Terrapon2014b,
title = {Molecular traces of alternative social organization in a termite genome},
author = {Nicolas Terrapon and Cai Li and Hugh M. Robertson and Lu Ji and Xuehong Meng and Warren Booth and Zhensheng Chen and Christopher P. Childers and Karl M. Glastad and Kaustubh Gokhale and Johannes Gowin and Wulfila Gronenberg and Russell A. Hermansen and Haofu Hu and Brendan G. Hunt and Ann K. Huylmans and Sayed M. S. Khalil and Robert D. Mitchell and Monica C. Munoz-Torres and Julie A. Mustard and Hailin Pan and Justin T. Reese and Michael E. Scharf and Fengming Sun and Heiko Vogel and Jin Xiao and Wei Yang and Zhikai Yang and Zuoquan Yang and Jiajian Zhou and Jiwei Zhu and Colin S. Brent and Christine G. Elsik and Michael A. D. Goodisman and David A. Liberles and R. Michael Roe and Edward L. Vargo and Andreas Vilcinskas and Jun Wang and Erich Bornberg-Bauer and Judith Korb and Guojie Zhang and Jürgen Liebig},
url = {https://bornberglab.org/wp-content/uploads/2021/10/terrapon20142.pdf, Download},
doi = {10.1038/ncomms4636},
year = {2014},
date = {2014-05-20},
urldate = {2014-05-20},
journal = {Nature Communications},
volume = {5},
number = {3636},
pages = {1-12},
abstract = {Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation.
Franssen, Susanne U.; Gu, Jenny; Winters, Gidon; Huylmans, Ann K.; Wienpahl, Isabell; Sparwel, Maximiliane; Coyer, James A.; Olsen, Jeanine L.; Reusch, Thorsten B. H.; Bornberg-Bauer, Erich
Genome-wide transcriptomic responses of the seagrasses Zostera marina and Nanozostera noltii under a simulated heatwave confirm functional types Journal Article
In: Marine Genomics, vol. 15, pp. 65-73, 2014.
@article{Franssen2014,
title = {Genome-wide transcriptomic responses of the seagrasses Zostera marina and Nanozostera noltii under a simulated heatwave confirm functional types},
author = {Susanne U. Franssen and Jenny Gu and Gidon Winters and Ann K. Huylmans and Isabell Wienpahl and Maximiliane Sparwel and James A. Coyer and Jeanine L. Olsen and Thorsten B. H. Reusch and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/franssen2014.pdf, Download},
doi = {https://doi.org/10.1016/j.margen.2014.03.004},
year = {2014},
date = {2014-04-03},
urldate = {2014-04-03},
journal = {Marine Genomics},
volume = {15},
pages = {65-73},
abstract = {Genome-wide transcription analysis between related species occurring in overlapping ranges can provide insights into the molecular basis underlying different ecological niches. The co-occurring seagrass species, Zostera marina and Nanozostera noltii, are found in marine coastal environments throughout the northern hemisphere. Z. marina is often dominant in subtidal environments and subjected to fewer temperature extremes compared to the predominately intertidal and more stress-tolerant N. noltii.
We exposed plants of both species to a realistic heat wave scenario in a common-stress-garden experiment. Using RNA-seq (~ 7 million reads/library), four Z. marina and four N. noltii libraries were compared representing northern (Denmark) and southern (Italy) locations within the co-occurring range of the species' European distribution.
A total of 8977 expressed genes were identified, of which 78 were directly related to heat stress. As predicted, both species were negatively affected by the heat wave, but showed markedly different molecular responses. In Z. marina the heat response was similar across locations in response to the heatwave at 26 °C, with a complex response in functions related to protein folding, synthesis of ribosomal chloroplast proteins, proteins involved in cell wall modification and heat shock proteins (HSPs). In N. noltii the heat response markedly differed between locations, while HSP genes were not induced in either population.
Our results suggest that as coastal seawater temperatures increase, Z. marina will disappear along its southern most ranges, whereas N. noltii will continue to move north. As a consequence, sub- and intertidal habitat partitioning may weaken in more northern regions because the higher thermal tolerance of N. noltii provides a competitive advantage in both habitats. Although previous studies have focused on HSPs, the present study clearly demonstrates that a broader examination of stress related genes is necessary.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Genome-wide transcription analysis between related species occurring in overlapping ranges can provide insights into the molecular basis underlying different ecological niches. The co-occurring seagrass species, Zostera marina and Nanozostera noltii, are found in marine coastal environments throughout the northern hemisphere. Z. marina is often dominant in subtidal environments and subjected to fewer temperature extremes compared to the predominately intertidal and more stress-tolerant N. noltii.
We exposed plants of both species to a realistic heat wave scenario in a common-stress-garden experiment. Using RNA-seq (~ 7 million reads/library), four Z. marina and four N. noltii libraries were compared representing northern (Denmark) and southern (Italy) locations within the co-occurring range of the species' European distribution.
A total of 8977 expressed genes were identified, of which 78 were directly related to heat stress. As predicted, both species were negatively affected by the heat wave, but showed markedly different molecular responses. In Z. marina the heat response was similar across locations in response to the heatwave at 26 °C, with a complex response in functions related to protein folding, synthesis of ribosomal chloroplast proteins, proteins involved in cell wall modification and heat shock proteins (HSPs). In N. noltii the heat response markedly differed between locations, while HSP genes were not induced in either population.
Our results suggest that as coastal seawater temperatures increase, Z. marina will disappear along its southern most ranges, whereas N. noltii will continue to move north. As a consequence, sub- and intertidal habitat partitioning may weaken in more northern regions because the higher thermal tolerance of N. noltii provides a competitive advantage in both habitats. Although previous studies have focused on HSPs, the present study clearly demonstrates that a broader examination of stress related genes is necessary.
We exposed plants of both species to a realistic heat wave scenario in a common-stress-garden experiment. Using RNA-seq (~ 7 million reads/library), four Z. marina and four N. noltii libraries were compared representing northern (Denmark) and southern (Italy) locations within the co-occurring range of the species' European distribution.
A total of 8977 expressed genes were identified, of which 78 were directly related to heat stress. As predicted, both species were negatively affected by the heat wave, but showed markedly different molecular responses. In Z. marina the heat response was similar across locations in response to the heatwave at 26 °C, with a complex response in functions related to protein folding, synthesis of ribosomal chloroplast proteins, proteins involved in cell wall modification and heat shock proteins (HSPs). In N. noltii the heat response markedly differed between locations, while HSP genes were not induced in either population.
Our results suggest that as coastal seawater temperatures increase, Z. marina will disappear along its southern most ranges, whereas N. noltii will continue to move north. As a consequence, sub- and intertidal habitat partitioning may weaken in more northern regions because the higher thermal tolerance of N. noltii provides a competitive advantage in both habitats. Although previous studies have focused on HSPs, the present study clearly demonstrates that a broader examination of stress related genes is necessary.
Moore, Andrew D.; Held, Andreas; Terrapon, Nicolas; Weiner, January; Bornberg-Bauer, Erich
DoMosaics: Software for domain arrangement visualization and domain-centric analysis of proteins. Journal Article
In: Bioinformatics, vol. 30, no. 2, pp. 282–283, 2014.
@article{Moore2014,
title = {DoMosaics: Software for domain arrangement visualization and domain-centric analysis of proteins.},
author = {Andrew D. Moore and Andreas Held and Nicolas Terrapon and January Weiner and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/moore2014.pdf, Download},
doi = {https://doi.org/10.1093/bioinformatics/btt640},
year = {2014},
date = {2014-01-15},
journal = {Bioinformatics},
volume = {30},
number = {2},
pages = {282–283},
abstract = {Summary: DoMosaics is an application that unifies protein domain annotation, domain arrangement analysis and visualization in a single tool. It simplifies the analysis of protein families by consolidating disjunct procedures based on often inconvenient command-line applications and complex analysis tools. It provides a simple user interface with access to domain annotation services such as InterProScan or a local HMMER installation, and can be used to compare, analyze and visualize the evolution of domain architectures.
Availability and implementation: DoMosaics is licensed under the Apache License, Version 2.0, and binaries can be freely obtained from www.domosaics.net.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Summary: DoMosaics is an application that unifies protein domain annotation, domain arrangement analysis and visualization in a single tool. It simplifies the analysis of protein families by consolidating disjunct procedures based on often inconvenient command-line applications and complex analysis tools. It provides a simple user interface with access to domain annotation services such as InterProScan or a local HMMER installation, and can be used to compare, analyze and visualize the evolution of domain architectures.
Availability and implementation: DoMosaics is licensed under the Apache License, Version 2.0, and binaries can be freely obtained from www.domosaics.net.
Availability and implementation: DoMosaics is licensed under the Apache License, Version 2.0, and binaries can be freely obtained from www.domosaics.net.
Terrapon, Nicolas; Weiner, January; Grath, Sonja; Moore, Andrew D.; Bornberg-Bauer, Erich
Rapid similarity search of proteins using alignments of domain arrangements Journal Article
In: Bioinformatics, vol. 30, no. 2, pp. 274–281, 2014.
@article{Terrapon2014,
title = {Rapid similarity search of proteins using alignments of domain arrangements},
author = {Nicolas Terrapon and January Weiner and Sonja Grath and Andrew D. Moore and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/terrapon2014.pdf, Download},
doi = {https://doi.org/10.1093/bioinformatics/btt379},
year = {2014},
date = {2014-01-15},
journal = {Bioinformatics},
volume = {30},
number = {2},
pages = {274–281},
abstract = {Motivation: Homology search methods are dominated by the central paradigm that sequence similarity is a proxy for common ancestry and, by extension, functional similarity. For determining sequence similarity in proteins, most widely used methods use models of sequence evolution and compare amino-acid strings in search for conserved linear stretches. Probabilistic models or sequence profiles capture the position-specific variation in an alignment of homologous sequences and can identify conserved motifs or domains. While profile-based search methods are generally more accurate than simple sequence comparison methods, they tend to be computationally more demanding. In recent years, several methods have emerged that perform protein similarity searches based on domain composition. However, few methods have considered the linear arrangements of domains when conducting similarity searches, despite strong evidence that domain order can harbour considerable functional and evolutionary signal.
Results: Here, we introduce an alignment scheme that uses a classical dynamic programming approach to the global alignment of domains. We illustrate that representing proteins as strings of domains (domain arrangements) and comparing these strings globally allows for a both fast and sensitive homology search. Further, we demonstrate that the presented methods complement existing methods by finding similar proteins missed by popular amino-acid–based comparison methods.
Availability: An implementation of the presented algorithms, a web-based interface as well as a command-line program for batch searching against the UniProt database can be found at http://rads.uni-muenster.de. Furthermore, we provide a JAVA API for programmatic access to domain-string–based search methods.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Motivation: Homology search methods are dominated by the central paradigm that sequence similarity is a proxy for common ancestry and, by extension, functional similarity. For determining sequence similarity in proteins, most widely used methods use models of sequence evolution and compare amino-acid strings in search for conserved linear stretches. Probabilistic models or sequence profiles capture the position-specific variation in an alignment of homologous sequences and can identify conserved motifs or domains. While profile-based search methods are generally more accurate than simple sequence comparison methods, they tend to be computationally more demanding. In recent years, several methods have emerged that perform protein similarity searches based on domain composition. However, few methods have considered the linear arrangements of domains when conducting similarity searches, despite strong evidence that domain order can harbour considerable functional and evolutionary signal.
Results: Here, we introduce an alignment scheme that uses a classical dynamic programming approach to the global alignment of domains. We illustrate that representing proteins as strings of domains (domain arrangements) and comparing these strings globally allows for a both fast and sensitive homology search. Further, we demonstrate that the presented methods complement existing methods by finding similar proteins missed by popular amino-acid–based comparison methods.
Availability: An implementation of the presented algorithms, a web-based interface as well as a command-line program for batch searching against the UniProt database can be found at http://rads.uni-muenster.de. Furthermore, we provide a JAVA API for programmatic access to domain-string–based search methods.
Results: Here, we introduce an alignment scheme that uses a classical dynamic programming approach to the global alignment of domains. We illustrate that representing proteins as strings of domains (domain arrangements) and comparing these strings globally allows for a both fast and sensitive homology search. Further, we demonstrate that the presented methods complement existing methods by finding similar proteins missed by popular amino-acid–based comparison methods.
Availability: An implementation of the presented algorithms, a web-based interface as well as a command-line program for batch searching against the UniProt database can be found at http://rads.uni-muenster.de. Furthermore, we provide a JAVA API for programmatic access to domain-string–based search methods.
2013
Guo, Baocheng; Chain, Frédéric J. J.; Bornberg-Bauer, Erich; Leder, Erica H; Merilä, Juha
Genomic divergence between nine- and three-spined sticklebacks Journal Article
In: BMC Genomics, vol. 6, no. 756, pp. 1-11, 2013.
@article{Guo2013,
title = {Genomic divergence between nine- and three-spined sticklebacks},
author = {Baocheng Guo and Frédéric J. J. Chain and Erich Bornberg-Bauer and Erica H Leder and Juha Merilä},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Guo2013.pdf, Download},
doi = {10.1186/1471-2164-14-756},
year = {2013},
date = {2013-11-05},
urldate = {2013-11-05},
journal = {BMC Genomics},
volume = {6},
number = {756},
pages = {1-11},
abstract = {Background
Comparative genomics approaches help to shed light on evolutionary processes that shape differentiation between lineages. The nine-spined stickleback (Pungitius pungitius) is a closely related species of the ecological ‘supermodel’ three-spined stickleback (Gasterosteus aculeatus). It is an emerging model system for evolutionary biology research but has garnered less attention and lacks extensive genomic resources. To expand on these resources and aid the study of sticklebacks in a phylogenetic framework, we characterized nine-spined stickleback transcriptomes from brain and liver using deep sequencing.
Results
We obtained nearly eight thousand assembled transcripts, of which 3,091 were assigned as putative one-to-one orthologs to genes found in the three-spined stickleback. These sequences were used for evaluating overall differentiation and substitution rates between nine- and three-spined sticklebacks, and to identify genes that are putatively evolving under positive selection. The synonymous substitution rate was estimated to be 7.1 × 10-9 per site per year between the two species, and a total of 165 genes showed patterns of adaptive evolution in one or both species. A few nine-spined stickleback contigs lacked an obvious ortholog in three-spined sticklebacks but were found to match genes in other fish species, suggesting several gene losses within 13 million years since the divergence of the two stickleback species. We identified 47 SNPs in 25 different genes that differentiate pond and marine ecotypes. We also identified 468 microsatellites that could be further developed as genetic markers in nine-spined sticklebacks.
Conclusion
With deep sequencing of nine-spined stickleback cDNA libraries, our study provides a significant increase in the number of gene sequences and microsatellite markers for this species, and identifies a number of genes showing patterns of adaptive evolution between nine- and three-spined sticklebacks. We also report several candidate genes that might be involved in differential adaptation between marine and freshwater nine-spined sticklebacks. This study provides a valuable resource for future studies aiming to identify candidate genes underlying ecological adaptation in this and other stickleback species.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
Comparative genomics approaches help to shed light on evolutionary processes that shape differentiation between lineages. The nine-spined stickleback (Pungitius pungitius) is a closely related species of the ecological ‘supermodel’ three-spined stickleback (Gasterosteus aculeatus). It is an emerging model system for evolutionary biology research but has garnered less attention and lacks extensive genomic resources. To expand on these resources and aid the study of sticklebacks in a phylogenetic framework, we characterized nine-spined stickleback transcriptomes from brain and liver using deep sequencing.
Results
We obtained nearly eight thousand assembled transcripts, of which 3,091 were assigned as putative one-to-one orthologs to genes found in the three-spined stickleback. These sequences were used for evaluating overall differentiation and substitution rates between nine- and three-spined sticklebacks, and to identify genes that are putatively evolving under positive selection. The synonymous substitution rate was estimated to be 7.1 × 10-9 per site per year between the two species, and a total of 165 genes showed patterns of adaptive evolution in one or both species. A few nine-spined stickleback contigs lacked an obvious ortholog in three-spined sticklebacks but were found to match genes in other fish species, suggesting several gene losses within 13 million years since the divergence of the two stickleback species. We identified 47 SNPs in 25 different genes that differentiate pond and marine ecotypes. We also identified 468 microsatellites that could be further developed as genetic markers in nine-spined sticklebacks.
Conclusion
With deep sequencing of nine-spined stickleback cDNA libraries, our study provides a significant increase in the number of gene sequences and microsatellite markers for this species, and identifies a number of genes showing patterns of adaptive evolution between nine- and three-spined sticklebacks. We also report several candidate genes that might be involved in differential adaptation between marine and freshwater nine-spined sticklebacks. This study provides a valuable resource for future studies aiming to identify candidate genes underlying ecological adaptation in this and other stickleback species.
Comparative genomics approaches help to shed light on evolutionary processes that shape differentiation between lineages. The nine-spined stickleback (Pungitius pungitius) is a closely related species of the ecological ‘supermodel’ three-spined stickleback (Gasterosteus aculeatus). It is an emerging model system for evolutionary biology research but has garnered less attention and lacks extensive genomic resources. To expand on these resources and aid the study of sticklebacks in a phylogenetic framework, we characterized nine-spined stickleback transcriptomes from brain and liver using deep sequencing.
Results
We obtained nearly eight thousand assembled transcripts, of which 3,091 were assigned as putative one-to-one orthologs to genes found in the three-spined stickleback. These sequences were used for evaluating overall differentiation and substitution rates between nine- and three-spined sticklebacks, and to identify genes that are putatively evolving under positive selection. The synonymous substitution rate was estimated to be 7.1 × 10-9 per site per year between the two species, and a total of 165 genes showed patterns of adaptive evolution in one or both species. A few nine-spined stickleback contigs lacked an obvious ortholog in three-spined sticklebacks but were found to match genes in other fish species, suggesting several gene losses within 13 million years since the divergence of the two stickleback species. We identified 47 SNPs in 25 different genes that differentiate pond and marine ecotypes. We also identified 468 microsatellites that could be further developed as genetic markers in nine-spined sticklebacks.
Conclusion
With deep sequencing of nine-spined stickleback cDNA libraries, our study provides a significant increase in the number of gene sequences and microsatellite markers for this species, and identifies a number of genes showing patterns of adaptive evolution between nine- and three-spined sticklebacks. We also report several candidate genes that might be involved in differential adaptation between marine and freshwater nine-spined sticklebacks. This study provides a valuable resource for future studies aiming to identify candidate genes underlying ecological adaptation in this and other stickleback species.
Simola, Daniel F.; Wissler, Lothar; Donahue, Greg; Waterhouse, Robert M.; Helmkampf, Martin; Roux, Julien; Nygaard, Sanne; Glastad, Karl M.; Hagen, Darren E.; Viljakainen, Lumi; Reese, Justin T.; Hunt, Brendan G.; Graur, Dan; Elhaik, Eran; Kriventseva, Evgenia V.; Wen, Jiayu; Parker, Brian J.; Cash, Elizabeth; Privman, Eyal; Childers, Christopher P.; Muñoz-Torres, Monica C.; Boomsma, Jacobus J.; Bornberg-Bauer, Erich; Currie, Cameron R.; Elsik, Christine G.; Suen, Garret; Goodisman, Michael A. D.; Keller, Laurent; Liebig, Jürgen; Rawls, Alan; Reinberg, Danny; Smith, Chris D.; Smith, Chris R.; Tsutsui, Neil; Wurm, Yannick; Zdobnov, Evgeny M.; Berger, Shelley L.; Gadau, Jürgen
Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality Journal Article
In: Genome Research, vol. 23, pp. 1235-1247, 2013.
@article{Simola2013,
title = {Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality},
author = {Daniel F. Simola and Lothar Wissler and Greg Donahue and Robert M. Waterhouse and Martin Helmkampf and Julien Roux and Sanne Nygaard and Karl M. Glastad and Darren E. Hagen and Lumi Viljakainen and Justin T. Reese and Brendan G. Hunt and Dan Graur and Eran Elhaik and Evgenia V. Kriventseva and Jiayu Wen and Brian J. Parker and Elizabeth Cash and Eyal Privman and Christopher P. Childers and Monica C. Muñoz-Torres and Jacobus J. Boomsma and Erich Bornberg-Bauer and Cameron R. Currie and Christine G. Elsik and Garret Suen and Michael A. D. Goodisman and Laurent Keller and Jürgen Liebig and Alan Rawls and Danny Reinberg and Chris D. Smith and Chris R. Smith and Neil Tsutsui and Yannick Wurm and Evgeny M. Zdobnov and Shelley L. Berger and Jürgen Gadau},
url = {https://bornberglab.org/wp-content/uploads/2021/04/simola2013.pdf, Download},
doi = {10.1101/gr.155408.113},
year = {2013},
date = {2013-05-01},
journal = {Genome Research},
volume = {23},
pages = {1235-1247},
abstract = {Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor–binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb) and trans (e.g., fork head) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila. Thus, while the “socio-genomes” of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor–binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb) and trans (e.g., fork head) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila. Thus, while the “socio-genomes” of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations.
Bornberg-Bauer, Erich; Albà, M Mar
Dynamics and Adaptive Benefits of Modular Protein Evolution Journal Article
In: Current Opinion in Structural Biology, vol. 23, no. 3, pp. 459-466, 2013.
@article{Bornberg-Bauer2013,
title = {Dynamics and Adaptive Benefits of Modular Protein Evolution},
author = {Erich Bornberg-Bauer and M Mar Albà},
url = {https://bornberglab.org/wp-content/uploads/2021/04/bornberg-bauer2013.pdf, Download},
doi = {10.1016/j.sbi.2013.02.012},
year = {2013},
date = {2013-04-03},
journal = {Current Opinion in Structural Biology},
volume = {23},
number = {3},
pages = {459-466},
abstract = {During protein evolution, novel domain arrangements are continuously formed. Rearrangements are important for the creation of molecular biodiversity and for functional molecular changes which underlie developmental shifts in the bauplan of organisms. Here we review the mechanisms by which new arrangements arise and the potential benefits of rearrangements. We concentrate on how new domains emerge and why they rapidly spread across genomes, gaining higher copy numbers than older, more established domains. This spread is most likely a consequence of their high adaptive potential but is unlikely to make up on its own for the drastic loss of domains, which is observed across different taxa. We show that a significant portion of the recently emerged domains, especially those in multidomain families, are highly disordered and speculate about the significance of these findings for the evolvability of novel genetic material.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
During protein evolution, novel domain arrangements are continuously formed. Rearrangements are important for the creation of molecular biodiversity and for functional molecular changes which underlie developmental shifts in the bauplan of organisms. Here we review the mechanisms by which new arrangements arise and the potential benefits of rearrangements. We concentrate on how new domains emerge and why they rapidly spread across genomes, gaining higher copy numbers than older, more established domains. This spread is most likely a consequence of their high adaptive potential but is unlikely to make up on its own for the drastic loss of domains, which is observed across different taxa. We show that a significant portion of the recently emerged domains, especially those in multidomain families, are highly disordered and speculate about the significance of these findings for the evolvability of novel genetic material.
Moore, Andrew D.; Grath, Sonja; Schüler, Andreas; Huylmans, Ann K.; Bornberg-Bauer, Erich
Quantification and Functional Analysis of Modular Protein Evolution in a Dense Phylogenetic Tree Journal Article
In: Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, vol. 1834, no. 5, pp. 898-907, 2013.
@article{Moore2013,
title = {Quantification and Functional Analysis of Modular Protein Evolution in a Dense Phylogenetic Tree},
author = {Andrew D. Moore and Sonja Grath and Andreas Schüler and Ann K. Huylmans and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Moore2013.pdf, Download},
doi = {10.1016/j.bbapap.2013.01.007},
year = {2013},
date = {2013-02-01},
urldate = {2013-02-01},
journal = {Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics},
volume = {1834},
number = {5},
pages = {898-907},
abstract = {Modularity is a hallmark of molecular evolution. Whether considering gene regulation, the components of metabolic pathways or signaling cascades, the ability to reuse autonomous modules in different molecular contexts can expedite evolutionary innovation. Similarly, protein domains are the modules of proteins, and modular domain rearrangements can create diversity with seemingly few operations in turn allowing for swift changes to an organism's functional repertoire. Here, we assess the patterns and functional effects of modular rearrangements at high resolution. Using a well resolved and diverse group of pancrustaceans, we illustrate arrangement diversity within closely related organisms, estimate arrangement turnover frequency and establish, for the first time, branch-specific rate estimates for fusion, fission, domain addition and terminal loss. Our results show that roughly 16 new arrangements arise per million years and that between 64% and 81% of these can be explained by simple, single-step modular rearrangement events. We find evidence that the frequencies of fission and terminal deletion events increase over time, and that modular rearrangements impact all levels of the cellular signaling apparatus and thus may have strong adaptive potential. Novel arrangements that cannot be explained by simple modular rearrangements contain a significant amount of repeat domains that occur in complex patterns which we term “supra-repeats”. Furthermore, these arrangements are significantly longer than those with a single-step rearrangement solution, suggesting that such arrangements may result from multi-step events. In summary, our analysis provides an integrated view and initial quantification of the patterns and functional impact of modular protein evolution in a well resolved phylogenetic tree. This article is part of a Special Issue entitled: The emerging dynamic view of proteins: Protein plasticity in allostery, evolution and self-assembly.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Modularity is a hallmark of molecular evolution. Whether considering gene regulation, the components of metabolic pathways or signaling cascades, the ability to reuse autonomous modules in different molecular contexts can expedite evolutionary innovation. Similarly, protein domains are the modules of proteins, and modular domain rearrangements can create diversity with seemingly few operations in turn allowing for swift changes to an organism's functional repertoire. Here, we assess the patterns and functional effects of modular rearrangements at high resolution. Using a well resolved and diverse group of pancrustaceans, we illustrate arrangement diversity within closely related organisms, estimate arrangement turnover frequency and establish, for the first time, branch-specific rate estimates for fusion, fission, domain addition and terminal loss. Our results show that roughly 16 new arrangements arise per million years and that between 64% and 81% of these can be explained by simple, single-step modular rearrangement events. We find evidence that the frequencies of fission and terminal deletion events increase over time, and that modular rearrangements impact all levels of the cellular signaling apparatus and thus may have strong adaptive potential. Novel arrangements that cannot be explained by simple modular rearrangements contain a significant amount of repeat domains that occur in complex patterns which we term “supra-repeats”. Furthermore, these arrangements are significantly longer than those with a single-step rearrangement solution, suggesting that such arrangements may result from multi-step events. In summary, our analysis provides an integrated view and initial quantification of the patterns and functional impact of modular protein evolution in a well resolved phylogenetic tree. This article is part of a Special Issue entitled: The emerging dynamic view of proteins: Protein plasticity in allostery, evolution and self-assembly.
Wissler, Lothar; Gadau, Jürgen; Simola, Daniel F.; Helmkampf, Martin; Bornberg-Bauer, Erich
Mechanisms and dynamics of orphan gene emergence in insect genomes Journal Article
In: Genome Biology and Evolution, vol. 5, no. 2, pp. 439–455, 2013.
@article{Wissler2013,
title = {Mechanisms and dynamics of orphan gene emergence in insect genomes},
author = {Lothar Wissler and Jürgen Gadau and Daniel F. Simola and Martin Helmkampf and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/wissler2013.pdf, Download},
doi = {10.1093/gbe/evt009},
year = {2013},
date = {2013-01-24},
journal = {Genome Biology and Evolution},
volume = {5},
number = {2},
pages = {439–455},
abstract = {Orphan genes are defined as genes that lack detectable similarity to genes in other species and therefore no clear signals of common descent (i.e., homology) can be inferred. Orphans are an enigmatic portion of the genome because their origin and function are mostly unknown and they typically make up 10% to 30% of all genes in a genome. Several case studies demonstrated that orphans can contribute to lineage-specific adaptation. Here, we study orphan genes by comparing 30 arthropod genomes, focusing in particular on seven recently sequenced ant genomes. This setup allows analyzing a major metazoan taxon and a comparison between social Hymenoptera (ants and bees) and nonsocial Diptera (flies and mosquitoes). First, we find that recently split lineages undergo accelerated genomic reorganization, including the rapid gain of many orphan genes. Second, between the two insect orders Hymenoptera and Diptera, orphan genes are more abundant and emerge more rapidly in Hymenoptera, in particular, in leaf-cutter ants. With respect to intragenomic localization, we find that ant orphan genes show little clustering, which suggests that orphan genes in ants are scattered uniformly over the genome and between nonorphan genes. Finally, our results indicate that the genetic mechanisms creating orphan genes—such as gene duplication, frame-shift fixation, creation of overlapping genes, horizontal gene transfer, and exaptation of transposable elements—act at different rates in insects, primates, and plants. In Formicidae, the majority of orphan genes has their origin in intergenic regions, pointing to a high rate of de novo gene formation or generalized gene loss, and support a recently proposed dynamic model of frequent gene birth and death.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Orphan genes are defined as genes that lack detectable similarity to genes in other species and therefore no clear signals of common descent (i.e., homology) can be inferred. Orphans are an enigmatic portion of the genome because their origin and function are mostly unknown and they typically make up 10% to 30% of all genes in a genome. Several case studies demonstrated that orphans can contribute to lineage-specific adaptation. Here, we study orphan genes by comparing 30 arthropod genomes, focusing in particular on seven recently sequenced ant genomes. This setup allows analyzing a major metazoan taxon and a comparison between social Hymenoptera (ants and bees) and nonsocial Diptera (flies and mosquitoes). First, we find that recently split lineages undergo accelerated genomic reorganization, including the rapid gain of many orphan genes. Second, between the two insect orders Hymenoptera and Diptera, orphan genes are more abundant and emerge more rapidly in Hymenoptera, in particular, in leaf-cutter ants. With respect to intragenomic localization, we find that ant orphan genes show little clustering, which suggests that orphan genes in ants are scattered uniformly over the genome and between nonorphan genes. Finally, our results indicate that the genetic mechanisms creating orphan genes—such as gene duplication, frame-shift fixation, creation of overlapping genes, horizontal gene transfer, and exaptation of transposable elements—act at different rates in insects, primates, and plants. In Formicidae, the majority of orphan genes has their origin in intergenic regions, pointing to a high rate of de novo gene formation or generalized gene loss, and support a recently proposed dynamic model of frequent gene birth and death.
2012
Sikosek, Tobias; Bornberg-Bauer, Erich; Chan, Hue Sun
Evolutionary Dynamics on Protein Bi-stability Landscapes can Potentially Resolve Adaptive Conflicts Journal Article
In: PLOS Computational Biology, vol. 8, no. 9, 2012.
@article{Sikosek2012,
title = {Evolutionary Dynamics on Protein Bi-stability Landscapes can Potentially Resolve Adaptive Conflicts},
author = {Tobias Sikosek and Erich Bornberg-Bauer and Hue Sun Chan},
url = {https://bornberglab.org/wp-content/uploads/2023/01/sikosek2012.pdf, Download},
doi = {10.1371/journal.pcbi.1002659},
year = {2012},
date = {2012-09-13},
urldate = {2012-09-13},
journal = {PLOS Computational Biology},
volume = {8},
number = {9},
abstract = {Experimental studies have shown that some proteins exist in two alternative native-state conformations. It has been proposed that such bi-stable proteins can potentially function as evolutionary bridges at the interface between two neutral networks of protein sequences that fold uniquely into the two different native conformations. Under adaptive conflict scenarios, bi-stable proteins may be of particular advantage if they simultaneously provide two beneficial biological functions. However, computational models that simulate protein structure evolution do not yet recognize the importance of bi-stability. Here we use a biophysical model to analyze sequence space to identify bi-stable or multi-stable proteins with two or more equally stable native-state structures. The inclusion of such proteins enhances phenotype connectivity between neutral networks in sequence space. Consideration of the sequence space neighborhood of bridge proteins revealed that bi-stability decreases gradually with each mutation that takes the sequence further away from an exactly bi-stable protein. With relaxed selection pressures, we found that bi-stable proteins in our model are highly successful under simulated adaptive conflict. Inspired by these model predictions, we developed a method to identify real proteins in the PDB with bridge-like properties, and have verified a clear bi-stability gradient for a series of mutants studied by Alexander et al. (Proc Nat Acad Sci USA 2009, 106:21149–21154) that connect two sequences that fold uniquely into two different native structures via a bridge-like intermediate mutant sequence. Based on these findings, new testable predictions for future studies on protein bi-stability and evolution are discussed.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Experimental studies have shown that some proteins exist in two alternative native-state conformations. It has been proposed that such bi-stable proteins can potentially function as evolutionary bridges at the interface between two neutral networks of protein sequences that fold uniquely into the two different native conformations. Under adaptive conflict scenarios, bi-stable proteins may be of particular advantage if they simultaneously provide two beneficial biological functions. However, computational models that simulate protein structure evolution do not yet recognize the importance of bi-stability. Here we use a biophysical model to analyze sequence space to identify bi-stable or multi-stable proteins with two or more equally stable native-state structures. The inclusion of such proteins enhances phenotype connectivity between neutral networks in sequence space. Consideration of the sequence space neighborhood of bridge proteins revealed that bi-stability decreases gradually with each mutation that takes the sequence further away from an exactly bi-stable protein. With relaxed selection pressures, we found that bi-stable proteins in our model are highly successful under simulated adaptive conflict. Inspired by these model predictions, we developed a method to identify real proteins in the PDB with bridge-like properties, and have verified a clear bi-stability gradient for a series of mutants studied by Alexander et al. (Proc Nat Acad Sci USA 2009, 106:21149–21154) that connect two sequences that fold uniquely into two different native structures via a bridge-like intermediate mutant sequence. Based on these findings, new testable predictions for future studies on protein bi-stability and evolution are discussed.
Sikosek, Tobias; Chan, Hue Sun; Bornberg-Bauer, Erich
Escape from Adaptive Conflict follows from weak functional trade-offs and mutational robustness Journal Article
In: PNAS, vol. 109, no. 37, pp. 14888-14893, 2012.
@article{Sikosek2012b,
title = {Escape from Adaptive Conflict follows from weak functional trade-offs and mutational robustness},
author = {Tobias Sikosek and Hue Sun Chan and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/10/sikosek20122.pdf, Download},
doi = {10.1073/pnas.1115620109},
year = {2012},
date = {2012-09-11},
journal = {PNAS},
volume = {109},
number = {37},
pages = {14888-14893},
abstract = {A fundamental question in molecular evolution is how proteins can adapt to new functions while being conserved for an existing function at the same time. Several theoretical models have been put forward to explain this apparent paradox. The most popular models include neofunctionalization, subfunctionalization (SUBF) by degenerative mutations, and dosage models. All of these models focus on adaptation after gene duplication. A newly proposed model named “Escape from Adaptive Conflict” (EAC) includes adaptive processes before and after gene duplication that lead to multifunctional proteins, and divergence (SUBF). Support for the importance of multifunctionality for the evolution of new protein functions comes from two experimental observations. First, many enzymes have highly evolvable promiscuous side activities. Second, different structural states of the same protein can be associated with different functions. How these observations may be related to the EAC model, under which conditions EAC is possible, and how the different models relate to each other is still unclear. Here, we present a theoretical framework that uses biophysical principles to infer the roles of functional promiscuity, gene dosage, gene duplication, point mutations, and selection pressures in the evolution of proteins. We find that selection pressures can determine whether neofunctionalization or SUBF is the more likely evolutionary process. Multifunctional proteins, arising during EAC evolution, allow rapid adaptation independent of gene duplication. This becomes a crucial advantage when gene duplications are rare. Finally, we propose that an increase in mutational robustness, not necessarily functional optimization, can be the sole driving force behind SUBF.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
A fundamental question in molecular evolution is how proteins can adapt to new functions while being conserved for an existing function at the same time. Several theoretical models have been put forward to explain this apparent paradox. The most popular models include neofunctionalization, subfunctionalization (SUBF) by degenerative mutations, and dosage models. All of these models focus on adaptation after gene duplication. A newly proposed model named “Escape from Adaptive Conflict” (EAC) includes adaptive processes before and after gene duplication that lead to multifunctional proteins, and divergence (SUBF). Support for the importance of multifunctionality for the evolution of new protein functions comes from two experimental observations. First, many enzymes have highly evolvable promiscuous side activities. Second, different structural states of the same protein can be associated with different functions. How these observations may be related to the EAC model, under which conditions EAC is possible, and how the different models relate to each other is still unclear. Here, we present a theoretical framework that uses biophysical principles to infer the roles of functional promiscuity, gene dosage, gene duplication, point mutations, and selection pressures in the evolution of proteins. We find that selection pressures can determine whether neofunctionalization or SUBF is the more likely evolutionary process. Multifunctional proteins, arising during EAC evolution, allow rapid adaptation independent of gene duplication. This becomes a crucial advantage when gene duplications are rare. Finally, we propose that an increase in mutational robustness, not necessarily functional optimization, can be the sole driving force behind SUBF.
Niehuis, Oliver; Hartig, Gerrit; Grath, Sonja; Pohl, Hans; Lehmann, Jörg; Tafer, Hakim; Donath, Alexander; Krauss, Veiko; Eisenhardt, Carina; Hertel, Jana; Petersen, Malte; Mayer, Christoph; Meusemann, Karen; Peters, Ralph S.; Stadler, Peter F.; Beutel, Rolf G.; Bornberg-Bauer, Erich; McKenna, Duane D.; Misof, Bernhard
Genomic and Morphological Evidence Converge to Resolve the Enigma of Strepsiptera Journal Article
In: Current Biology, vol. 22, no. 14, pp. 1309-1313, 2012.
@article{Niehuis2012,
title = {Genomic and Morphological Evidence Converge to Resolve the Enigma of Strepsiptera},
author = {Oliver Niehuis and Gerrit Hartig and Sonja Grath and Hans Pohl and Jörg Lehmann and Hakim Tafer and Alexander Donath and Veiko Krauss and Carina Eisenhardt and Jana Hertel and Malte Petersen and Christoph Mayer and Karen Meusemann and Ralph S. Peters and Peter F. Stadler and Rolf G. Beutel and Erich Bornberg-Bauer and Duane D. McKenna and Bernhard Misof},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Niehuis2012.pdf, Download},
doi = {10.1016/j.cub.2012.05.018},
year = {2012},
date = {2012-07-24},
journal = {Current Biology},
volume = {22},
number = {14},
pages = {1309-1313},
abstract = {The phylogeny of insects, one of the most spectacular radiations of life on earth, has received considerable attention [1, 2, 3]. However, the evolutionary roots of one intriguing group of insects, the twisted-wing parasites (Strepsiptera), remain unclear despite centuries of study and debate [1, 2, 4, 5, 6, 7, 8, 9, 10, 11]. Strepsiptera exhibit exceptional larval developmental features, consistent with a predicted step from direct (hemimetabolous) larval development to complete metamorphosis that could have set the stage for the spectacular radiation of metamorphic (holometabolous) insects [1, 12, 13]. Here we report the sequencing of a Strepsiptera genome and show that the analysis of sequence-based genomic data (comprising more than 18 million nucleotides from nearly 4,500 genes obtained from a total of 13 insect genomes), along with genomic metacharacters, clarifies the phylogenetic origin of Strepsiptera and sheds light on the evolution of holometabolous insect development. Our results provide overwhelming support for Strepsiptera as the closest living relatives of beetles (Coleoptera). They demonstrate that the larval developmental features of Strepsiptera, reminiscent of those of hemimetabolous insects, are the result of convergence. Our analyses solve the long-standing enigma of the evolutionary roots of Strepsiptera and reveal that the holometabolous mode of insect development is more malleable than previously thought.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The phylogeny of insects, one of the most spectacular radiations of life on earth, has received considerable attention [1, 2, 3]. However, the evolutionary roots of one intriguing group of insects, the twisted-wing parasites (Strepsiptera), remain unclear despite centuries of study and debate [1, 2, 4, 5, 6, 7, 8, 9, 10, 11]. Strepsiptera exhibit exceptional larval developmental features, consistent with a predicted step from direct (hemimetabolous) larval development to complete metamorphosis that could have set the stage for the spectacular radiation of metamorphic (holometabolous) insects [1, 12, 13]. Here we report the sequencing of a Strepsiptera genome and show that the analysis of sequence-based genomic data (comprising more than 18 million nucleotides from nearly 4,500 genes obtained from a total of 13 insect genomes), along with genomic metacharacters, clarifies the phylogenetic origin of Strepsiptera and sheds light on the evolution of holometabolous insect development. Our results provide overwhelming support for Strepsiptera as the closest living relatives of beetles (Coleoptera). They demonstrate that the larval developmental features of Strepsiptera, reminiscent of those of hemimetabolous insects, are the result of convergence. Our analyses solve the long-standing enigma of the evolutionary roots of Strepsiptera and reveal that the holometabolous mode of insect development is more malleable than previously thought.
Feulner, Philine G. D.; Chain, Frederic J. J.; Panchal, Mahesh; Eizaguirre, Christophe; Kalbe, Martin; Lenz, Tobias L.; Mundry, Marvin; Samonte, Irene E.; Stoll, Monika; Milinski, Manfred; Reusch, Thorsten B. H.; Bornberg-Bauer, Erich
Genome‐wide patterns of standing genetic variation in a marine population of three‐spined sticklebacks Journal Article
In: Molecular Ecology, vol. 22, no. 3, pp. 635-649, 2012.
@article{FEULNER2012,
title = {Genome‐wide patterns of standing genetic variation in a marine population of three‐spined sticklebacks},
author = {Philine G. D. Feulner and Frederic J. J. Chain and Mahesh Panchal and Christophe Eizaguirre and Martin Kalbe and Tobias L. Lenz and Marvin Mundry and Irene E. Samonte and Monika Stoll and Manfred Milinski and Thorsten B. H. Reusch and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/feulner2012.pdf, Download},
doi = {10.1111/j.1365-294X.2012.05680.x},
year = {2012},
date = {2012-07-03},
urldate = {2012-07-03},
journal = {Molecular Ecology},
volume = {22},
number = {3},
pages = {635-649},
abstract = {Since the end of the Pleistocene, the three‐spined stickleback (Gasterosteus aculeatus) has repeatedly colonized and adapted to various freshwater habitats probably originating from ancestral marine populations. Standing genetic variation and the underlying genomic architecture both have been speculated to contribute to recent adaptive radiations of sticklebacks. Here, we expand on the current genomic resources of this fish by providing extensive genome‐wide variation data from six individuals from a marine (North Sea) stickleback population. Using next‐generation sequencing and a combination of paired‐end and mate‐pair libraries, we detected a wide size range of genetic variation. Among the six individuals, we found more than 7% of the genome is polymorphic, consisting of 2 599 111 SNPs, 233 464 indels and structural variation (SV) (>50 bp) such as 1054 copy‐number variable regions (deletions and duplications) and 48 inversions. Many of these polymorphisms affect gene and coding sequences. Based on SNP diversity, we determined outlier regions concordant with signatures expected under adaptive evolution. As some of these outliers overlap with pronounced regions of copy‐number variation, we propose the consideration of such SV when analysing SNP data from re‐sequencing approaches. We further discuss the value of this resource on genome‐wide variation for further investigation upon the relative contribution of standing variation on the parallel evolution of sticklebacks and the importance of the genomic architecture in adaptive radiation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Since the end of the Pleistocene, the three‐spined stickleback (Gasterosteus aculeatus) has repeatedly colonized and adapted to various freshwater habitats probably originating from ancestral marine populations. Standing genetic variation and the underlying genomic architecture both have been speculated to contribute to recent adaptive radiations of sticklebacks. Here, we expand on the current genomic resources of this fish by providing extensive genome‐wide variation data from six individuals from a marine (North Sea) stickleback population. Using next‐generation sequencing and a combination of paired‐end and mate‐pair libraries, we detected a wide size range of genetic variation. Among the six individuals, we found more than 7% of the genome is polymorphic, consisting of 2 599 111 SNPs, 233 464 indels and structural variation (SV) (>50 bp) such as 1054 copy‐number variable regions (deletions and duplications) and 48 inversions. Many of these polymorphisms affect gene and coding sequences. Based on SNP diversity, we determined outlier regions concordant with signatures expected under adaptive evolution. As some of these outliers overlap with pronounced regions of copy‐number variation, we propose the consideration of such SV when analysing SNP data from re‐sequencing approaches. We further discuss the value of this resource on genome‐wide variation for further investigation upon the relative contribution of standing variation on the parallel evolution of sticklebacks and the importance of the genomic architecture in adaptive radiation.
Wissler, Lothar; Godmann, Lars; Bornberg-Bauer, Erich
Evolutionary dynamics of simple sequence repeats across long evolutionary time in genus Drosophila Journal Article
In: Trends in Evolutionary Biology, vol. 4, no. 7, 2012.
@article{Wissler2012,
title = {Evolutionary dynamics of simple sequence repeats across long evolutionary time in genus Drosophila},
author = {Lothar Wissler and Lars Godmann and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/wissler2012.pdf, Download},
doi = {10.4081/eb.2012.e7},
year = {2012},
date = {2012-06-21},
journal = {Trends in Evolutionary Biology},
volume = {4},
number = {7},
abstract = {Repetitive DNA is among the fastest evolving types of genomic DNA, which includes simple sequence repeats (SSRs), short regions of tandemly repeated one to six nucleotides long motifs. SSRs are found most frequently in noncoding regions. Repeat number variation occurs rapidly and is presumably neutral such that polymorphic SSRs are frequently used as genetic markers to characterize and classify populations. Despite their rapid evolution, recent reports suggested that SSR loci can be retained over hundreds of millions of years. We here investigate the dynamics and genomic features of SSR evolution in syntenic regions conserved across twelve Drosophila species and within a D. melanogaster population dataset. We find that SSR loci decay exponentially with time, the percentage of retained SSRs mostly reflects species relationships and correlates well with the sequence similarity of neighboring genes. About 47% of repeat loci within syntenic regions may share common ancestry due to predicted conservation in at least two species from the Drosophila subgenera Sophophora and Drosophila respectively, i.e. after 80 million years of divergence time. Since loci which are highly polymorphic at the population level also decay faster across species, SSR evolution appears to be a gradual process in which conservation pressure may act at relatively constant rates across time scales. A higher proportion of SSR loci are retained among Drosophila subgenus species considering their evolutionary distance and the expected decay rate estimated across all Drosophila species. This prolonged SSR retention might be caused by a higher SSR mutation rate and a lower nucleotide substitution rate in the Drosophila subgenus compared to Sophophora species. SSRs in exons and on autosomes evolve more slowly than SSRs located outside of exons or on the sex chromosome, respectively, both within and across species. SSR variability and phylogenetic conservation thus varies depending on the genomic location. These findings provide new insights into the dynamics of SSRs at both micro- and macro-evolutionary scales. The development of robust models of SSR long-term evolution will facilitate more in-depth analyses in general and the prediction of neutrally evolving SSRs and SSRs evolving under purifying selection, extending our knowledge of the functional impact of SSRs in genome evolution.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Repetitive DNA is among the fastest evolving types of genomic DNA, which includes simple sequence repeats (SSRs), short regions of tandemly repeated one to six nucleotides long motifs. SSRs are found most frequently in noncoding regions. Repeat number variation occurs rapidly and is presumably neutral such that polymorphic SSRs are frequently used as genetic markers to characterize and classify populations. Despite their rapid evolution, recent reports suggested that SSR loci can be retained over hundreds of millions of years. We here investigate the dynamics and genomic features of SSR evolution in syntenic regions conserved across twelve Drosophila species and within a D. melanogaster population dataset. We find that SSR loci decay exponentially with time, the percentage of retained SSRs mostly reflects species relationships and correlates well with the sequence similarity of neighboring genes. About 47% of repeat loci within syntenic regions may share common ancestry due to predicted conservation in at least two species from the Drosophila subgenera Sophophora and Drosophila respectively, i.e. after 80 million years of divergence time. Since loci which are highly polymorphic at the population level also decay faster across species, SSR evolution appears to be a gradual process in which conservation pressure may act at relatively constant rates across time scales. A higher proportion of SSR loci are retained among Drosophila subgenus species considering their evolutionary distance and the expected decay rate estimated across all Drosophila species. This prolonged SSR retention might be caused by a higher SSR mutation rate and a lower nucleotide substitution rate in the Drosophila subgenus compared to Sophophora species. SSRs in exons and on autosomes evolve more slowly than SSRs located outside of exons or on the sex chromosome, respectively, both within and across species. SSR variability and phylogenetic conservation thus varies depending on the genomic location. These findings provide new insights into the dynamics of SSRs at both micro- and macro-evolutionary scales. The development of robust models of SSR long-term evolution will facilitate more in-depth analyses in general and the prediction of neutrally evolving SSRs and SSRs evolving under purifying selection, extending our knowledge of the functional impact of SSRs in genome evolution.
Liberles, David A.; Teichmann, Sarah A.; Bahar, Ivet; Bastolla, Ugo; Bloom, Jesse; Bornberg-Bauer, Erich; Colwell, Lucy J.; Koning, A. P. Jason; Dokholyan, Nikolay V.; Echave, Julian; Elofsson, Arne; Gerloff, Dietlind L.; Goldstein, Richard A.; Grahnen, Johan A.; Holder, Mark T.; Lakner, Clemens; Lartillot, Nicholas; Lovell, Simon C.; Naylor, Gavin; Perica, Tina; Pollock, David D.; Pupko, Tal; Regan, Lynne; Roger, Andrew; Rubinstein, Nimrod; Shakhnovich, Eugene; Sjölander, Kimmen; Sunyaev, Shamil; Teufel, Ashley I.; Thorne, Jeffrey L.; Thornton, Joseph W.; Weinreich, Daniel M.; Whelan, Simon
The interface of protein structure, protein biophysics, and molecular evolution Journal Article
In: Protein Science, vol. 21, no. 6, pp. 769-785, 2012.
@article{Liberles2012,
title = {The interface of protein structure, protein biophysics, and molecular evolution},
author = {David A. Liberles and Sarah A. Teichmann and Ivet Bahar and Ugo Bastolla and Jesse Bloom and Erich Bornberg-Bauer and Lucy J. Colwell and A. P. Jason Koning and Nikolay V. Dokholyan and Julian Echave and Arne Elofsson and Dietlind L. Gerloff and Richard A. Goldstein and Johan A. Grahnen and Mark T. Holder and Clemens Lakner and Nicholas Lartillot and Simon C. Lovell and Gavin Naylor and Tina Perica and David D. Pollock and Tal Pupko and Lynne Regan and Andrew Roger and Nimrod Rubinstein and Eugene Shakhnovich and Kimmen Sjölander and Shamil Sunyaev and Ashley I. Teufel and Jeffrey L. Thorne and Joseph W. Thornton and Daniel M. Weinreich and Simon Whelan},
url = {https://bornberglab.org/wp-content/uploads/2021/04/liberles2012.pdf, Download},
doi = {10.1002/pro.2071},
year = {2012},
date = {2012-03-30},
journal = {Protein Science},
volume = {21},
number = {6},
pages = {769-785},
abstract = {Abstract The interface of protein structural biology, protein biophysics, molecular evolution, and molecular population genetics forms the foundations for a mechanistic understanding of many aspects of protein biochemistry. Current efforts in interdisciplinary protein modeling are in their infancy and the state‐of‐the art of such models is described. Beyond the relationship between amino acid substitution and static protein structure, protein function, and corresponding organismal fitness, other considerations are also discussed. More complex mutational processes such as insertion and deletion and domain rearrangements and even circular permutations should be evaluated. The role of intrinsically disordered proteins is still controversial, but may be increasingly important to consider. Protein geometry and protein dynamics as a deviation from static considerations of protein structure are also important. Protein expression level is known to be a major determinant of evolutionary rate and several considerations including selection at the mRNA level and the role of interaction specificity are discussed. Lastly, the relationship between modeling and needed high‐throughput experimental data as well as experimental examination of protein evolution using ancestral sequence resurrection and in vitro biochemistry are presented, towards an aim of ultimately generating better models for biological inference and prediction.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Abstract The interface of protein structural biology, protein biophysics, molecular evolution, and molecular population genetics forms the foundations for a mechanistic understanding of many aspects of protein biochemistry. Current efforts in interdisciplinary protein modeling are in their infancy and the state‐of‐the art of such models is described. Beyond the relationship between amino acid substitution and static protein structure, protein function, and corresponding organismal fitness, other considerations are also discussed. More complex mutational processes such as insertion and deletion and domain rearrangements and even circular permutations should be evaluated. The role of intrinsically disordered proteins is still controversial, but may be increasingly important to consider. Protein geometry and protein dynamics as a deviation from static considerations of protein structure are also important. Protein expression level is known to be a major determinant of evolutionary rate and several considerations including selection at the mRNA level and the role of interaction specificity are discussed. Lastly, the relationship between modeling and needed high‐throughput experimental data as well as experimental examination of protein evolution using ancestral sequence resurrection and in vitro biochemistry are presented, towards an aim of ultimately generating better models for biological inference and prediction.
Balasubramanian, Prakash G.; Beckmann, Anna; Warnken, Uwe; Schnölzer, Martina; Schüler, Andreas; Bornberg-Bauer, Erich; Holstein, Thomas W.; SuatÖzbek,
Proteome of Hydra Nematocyst Journal Article
In: Journal of Biological Chemistry, vol. 287, no. 13, pp. 9672-9681, 2012.
@article{Balasubramanian2012,
title = {Proteome of Hydra Nematocyst},
author = {Prakash G. Balasubramanian and Anna Beckmann and Uwe Warnken and Martina Schnölzer and Andreas Schüler and Erich Bornberg-Bauer and Thomas W. Holstein and SuatÖzbek},
url = {https://bornberglab.org/wp-content/uploads/2021/04/balasubramanian2012.pdf, Download},
doi = {10.1074/jbc.M111.328203},
year = {2012},
date = {2012-03-23},
journal = {Journal of Biological Chemistry},
volume = {287},
number = {13},
pages = {9672-9681},
abstract = {Stinging cells or nematocytes of jellyfish and other cnidarians represent one of the most poisonous and sophisticated cellular inventions in animal evolution. This ancient cell type is unique in containing a giant secretory vesicle derived from the Golgi apparatus. The organelle structure within the vesicle comprises an elastically stretched capsule (nematocyst) to which a long tubule is attached. During exocytosis, the barbed part of the tubule is accelerated with >5 million g in <700 ns, enabling a harpoon-like discharge (Nüchter, T., Benoit, M., Engel, U., Ozbek, S., and Holstein, T. W. (2006) Curr. Biol. 16, R316–R318). Hitherto, the molecular components responsible for the organelle's biomechanical properties were largely unknown. Here, we describe the proteome of nematocysts from the freshwater polyp Hydra magnipapillata. Our analysis revealed an unexpectedly complex secretome of 410 proteins with venomous and lytic but also adhesive or fibrous properties. In particular, the insoluble fraction of the nematocyst represents a functional extracellular matrix structure of collagenous and elastic nature. This finding suggests an evolutionary scenario in which exocytic vesicles harboring a venomous secretome assembled a sophisticated predatory structure from extracellular matrix motif proteins.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Stinging cells or nematocytes of jellyfish and other cnidarians represent one of the most poisonous and sophisticated cellular inventions in animal evolution. This ancient cell type is unique in containing a giant secretory vesicle derived from the Golgi apparatus. The organelle structure within the vesicle comprises an elastically stretched capsule (nematocyst) to which a long tubule is attached. During exocytosis, the barbed part of the tubule is accelerated with >5 million g in <700 ns, enabling a harpoon-like discharge (Nüchter, T., Benoit, M., Engel, U., Ozbek, S., and Holstein, T. W. (2006) Curr. Biol. 16, R316–R318). Hitherto, the molecular components responsible for the organelle's biomechanical properties were largely unknown. Here, we describe the proteome of nematocysts from the freshwater polyp Hydra magnipapillata. Our analysis revealed an unexpectedly complex secretome of 410 proteins with venomous and lytic but also adhesive or fibrous properties. In particular, the insoluble fraction of the nematocyst represents a functional extracellular matrix structure of collagenous and elastic nature. This finding suggests an evolutionary scenario in which exocytic vesicles harboring a venomous secretome assembled a sophisticated predatory structure from extracellular matrix motif proteins.
Gu, Jenny; Weber, Katrin; Klemp, Elisabeth; Winters, Gidon; Franssen, Susanne U.; Wienpahl, Isabell; Huylmans, Ann K.; Zecher, Karsten; Reusch, Thorsten B. H.; Bornberg-Bauer, Erich; Weber, Andreas P. M.
Identifying core features of adaptive metabolic mechanisms for chronic heat stress attenuation contributing to systems robustness Journal Article
In: Integrative Biology, vol. 4, no. 5, pp. 480-493, 2012.
@article{Gu2012,
title = {Identifying core features of adaptive metabolic mechanisms for chronic heat stress attenuation contributing to systems robustness},
author = {Jenny Gu and Katrin Weber and Elisabeth Klemp and Gidon Winters and Susanne U. Franssen and Isabell Wienpahl and Ann K. Huylmans and Karsten Zecher and Thorsten B. H. Reusch and Erich Bornberg-Bauer and Andreas P. M. Weber},
url = {https://bornberglab.org/wp-content/uploads/2021/04/gu2012.pdf, Download},
doi = {10.1039/c2ib00109h},
year = {2012},
date = {2012-03-08},
urldate = {2012-03-08},
journal = {Integrative Biology},
volume = {4},
number = {5},
pages = {480-493},
abstract = {The contribution of metabolism to heat stress may play a significant role in defining robustness and recovery of systems; either by providing the energy and metabolites required for cellular homeostasis, or through the generation of protective osmolytes. However, the mechanisms by which heat stress attenuation could be adapted through metabolic processes as a stabilizing strategy against thermal stress are still largely unclear. We address this issue through metabolomic and transcriptomic profiles for populations along a thermal cline where two seagrass species, Zostera marina and Zostera noltii, were found in close proximity. Significant changes captured by these profile comparisons could be detected, with a larger response magnitude observed in northern populations to heat stress. Sucrose, fructose, and myo-inositol were identified to be the most responsive of the 29 analyzed organic metabolites. Many key enzymes in the Calvin cycle, glycolysis and pentose phosphate pathways also showed significant differential expression. The reported comparison suggests that adaptive mechanisms are involved through metabolic pathways to dampen the impacts of heat stress, and interactions between the metabolome and proteome should be further investigated in systems biology to understand robust design features against abiotic stress.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The contribution of metabolism to heat stress may play a significant role in defining robustness and recovery of systems; either by providing the energy and metabolites required for cellular homeostasis, or through the generation of protective osmolytes. However, the mechanisms by which heat stress attenuation could be adapted through metabolic processes as a stabilizing strategy against thermal stress are still largely unclear. We address this issue through metabolomic and transcriptomic profiles for populations along a thermal cline where two seagrass species, Zostera marina and Zostera noltii, were found in close proximity. Significant changes captured by these profile comparisons could be detected, with a larger response magnitude observed in northern populations to heat stress. Sucrose, fructose, and myo-inositol were identified to be the most responsive of the 29 analyzed organic metabolites. Many key enzymes in the Calvin cycle, glycolysis and pentose phosphate pathways also showed significant differential expression. The reported comparison suggests that adaptive mechanisms are involved through metabolic pathways to dampen the impacts of heat stress, and interactions between the metabolome and proteome should be further investigated in systems biology to understand robust design features against abiotic stress.
Mundry, Marvin; Bornberg-Bauer, Erich; Sammeth, Michael; Feulner, Philine G. D.
Evaluating Characteristics of De Novo Assembly Software on 454 Transcriptome Data: A Simulation Approach Journal Article
In: PLOS One, vol. 7, no. 2, 2012.
@article{Mundry2012,
title = {Evaluating Characteristics of De Novo Assembly Software on 454 Transcriptome Data: A Simulation Approach},
author = {Marvin Mundry and Erich Bornberg-Bauer and Michael Sammeth and Philine G. D. Feulner},
url = {https://bornberglab.org/wp-content/uploads/2021/04/mundry2012.pdf, Download},
doi = {10.1371/journal.pone.0031410},
year = {2012},
date = {2012-02-27},
journal = {PLOS One},
volume = {7},
number = {2},
abstract = {Background
The quantity of transcriptome data is rapidly increasing for non-model organisms. As sequencing technology advances, focus shifts towards solving bioinformatic challenges, of which sequence read assembly is the first task. Recent studies have compared the performance of different software to establish a best practice for transcriptome assembly. Here, we adapted a simulation approach to evaluate specific features of assembly programs on 454 data. The novelty of our study is that the simulation allows us to calculate a model assembly as reference point for comparison.
Findings
The simulation approach allows us to compare basic metrics of assemblies computed by different software applications (CAP3, MIRA, Newbler, and Oases) to a known optimal solution. We found MIRA and CAP3 are conservative in merging reads. This resulted in comparably high number of short contigs. In contrast, Newbler more readily merged reads into longer contigs, while Oases produced the overall shortest assembly. Due to the simulation approach, reads could be traced back to their correct placement within the transcriptome. Together with mapping reads onto the assembled contigs, we were able to evaluate ambiguity in the assemblies. This analysis further supported the conservative nature of MIRA and CAP3, which resulted in low proportions of chimeric contigs, but high redundancy. Newbler produced less redundancy, but the proportion of chimeric contigs was higher.
Conclusion
Our evaluation of four assemblers suggested that MIRA and Newbler slightly outperformed the other programs, while showing contrasting characteristics. Oases did not perform very well on the 454 reads. Our evaluation indicated that the software was either conservative (MIRA) or liberal (Newbler) about merging reads into contigs. This suggested that in choosing an assembly program researchers should carefully consider their follow up analysis and consequences of the chosen approach to gain an assembly.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
The quantity of transcriptome data is rapidly increasing for non-model organisms. As sequencing technology advances, focus shifts towards solving bioinformatic challenges, of which sequence read assembly is the first task. Recent studies have compared the performance of different software to establish a best practice for transcriptome assembly. Here, we adapted a simulation approach to evaluate specific features of assembly programs on 454 data. The novelty of our study is that the simulation allows us to calculate a model assembly as reference point for comparison.
Findings
The simulation approach allows us to compare basic metrics of assemblies computed by different software applications (CAP3, MIRA, Newbler, and Oases) to a known optimal solution. We found MIRA and CAP3 are conservative in merging reads. This resulted in comparably high number of short contigs. In contrast, Newbler more readily merged reads into longer contigs, while Oases produced the overall shortest assembly. Due to the simulation approach, reads could be traced back to their correct placement within the transcriptome. Together with mapping reads onto the assembled contigs, we were able to evaluate ambiguity in the assemblies. This analysis further supported the conservative nature of MIRA and CAP3, which resulted in low proportions of chimeric contigs, but high redundancy. Newbler produced less redundancy, but the proportion of chimeric contigs was higher.
Conclusion
Our evaluation of four assemblers suggested that MIRA and Newbler slightly outperformed the other programs, while showing contrasting characteristics. Oases did not perform very well on the 454 reads. Our evaluation indicated that the software was either conservative (MIRA) or liberal (Newbler) about merging reads into contigs. This suggested that in choosing an assembly program researchers should carefully consider their follow up analysis and consequences of the chosen approach to gain an assembly.
The quantity of transcriptome data is rapidly increasing for non-model organisms. As sequencing technology advances, focus shifts towards solving bioinformatic challenges, of which sequence read assembly is the first task. Recent studies have compared the performance of different software to establish a best practice for transcriptome assembly. Here, we adapted a simulation approach to evaluate specific features of assembly programs on 454 data. The novelty of our study is that the simulation allows us to calculate a model assembly as reference point for comparison.
Findings
The simulation approach allows us to compare basic metrics of assemblies computed by different software applications (CAP3, MIRA, Newbler, and Oases) to a known optimal solution. We found MIRA and CAP3 are conservative in merging reads. This resulted in comparably high number of short contigs. In contrast, Newbler more readily merged reads into longer contigs, while Oases produced the overall shortest assembly. Due to the simulation approach, reads could be traced back to their correct placement within the transcriptome. Together with mapping reads onto the assembled contigs, we were able to evaluate ambiguity in the assemblies. This analysis further supported the conservative nature of MIRA and CAP3, which resulted in low proportions of chimeric contigs, but high redundancy. Newbler produced less redundancy, but the proportion of chimeric contigs was higher.
Conclusion
Our evaluation of four assemblers suggested that MIRA and Newbler slightly outperformed the other programs, while showing contrasting characteristics. Oases did not perform very well on the 454 reads. Our evaluation indicated that the software was either conservative (MIRA) or liberal (Newbler) about merging reads into contigs. This suggested that in choosing an assembly program researchers should carefully consider their follow up analysis and consequences of the chosen approach to gain an assembly.
Kersting, Anna R.; Bornberg-Bauer, Erich; Moore, Andrew D.; Grath, Sonja
Dynamics and Adaptive Benefits of Protein Domain Emergence and Arrangements during Plant Genome Evolution Journal Article
In: Genome Biology and Evolution, vol. 4, no. 3, pp. 316–329, 2012.
@article{Kersting2012,
title = {Dynamics and Adaptive Benefits of Protein Domain Emergence and Arrangements during Plant Genome Evolution},
author = {Anna R. Kersting and Erich Bornberg-Bauer and Andrew D. Moore and Sonja Grath},
url = {https://bornberglab.org/wp-content/uploads/2021/04/kersting2012.pdf, Download},
doi = {10.1093/gbe/evs004},
year = {2012},
date = {2012-01-16},
journal = {Genome Biology and Evolution},
volume = {4},
number = {3},
pages = {316–329},
abstract = {Plant genomes are generally very large, mostly paleopolyploid, and have numerous gene duplicates and complex genomic features such as repeats and transposable elements. Many of these features have been hypothesized to enable plants, which cannot easily escape environmental challenges, to rapidly adapt. Another mechanism, which has recently been well described as a major facilitator of rapid adaptation in bacteria, animals, and fungi but not yet for plants, is modular rearrangement of protein-coding genes. Due to the high precision of profile-based methods, rearrangements can be well captured at the protein level by characterizing the emergence, loss, and rearrangements of protein domains, their structural, functional, and evolutionary building blocks. Here, we study the dynamics of domain rearrangements and explore their adaptive benefit in 27 plant and 3 algal genomes. We use a phylogenomic approach by which we can explain the formation of 88% of all arrangements by single-step events, such as fusion, fission, and terminal loss of domains. We find many domains are lost along every lineage, but at least 500 domains are novel, that is, they are unique to green plants and emerged more or less recently. These novel domains duplicate and rearrange more readily within their genomes than ancient domains and are overproportionally involved in stress response and developmental innovations. Novel domains more often affect regulatory proteins and show a higher degree of structural disorder than ancient domains. Whereas a relatively large and well-conserved core set of single-domain proteins exists, long multi-domain arrangements tend to be species-specific. We find that duplicated genes are more often involved in rearrangements. Although fission events typically impact metabolic proteins, fusion events often create new signaling proteins essential for environmental sensing. Taken together, the high volatility of single domains and complex arrangements in plant genomes demonstrate the importance of modularity for environmental adaptability of plants.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Plant genomes are generally very large, mostly paleopolyploid, and have numerous gene duplicates and complex genomic features such as repeats and transposable elements. Many of these features have been hypothesized to enable plants, which cannot easily escape environmental challenges, to rapidly adapt. Another mechanism, which has recently been well described as a major facilitator of rapid adaptation in bacteria, animals, and fungi but not yet for plants, is modular rearrangement of protein-coding genes. Due to the high precision of profile-based methods, rearrangements can be well captured at the protein level by characterizing the emergence, loss, and rearrangements of protein domains, their structural, functional, and evolutionary building blocks. Here, we study the dynamics of domain rearrangements and explore their adaptive benefit in 27 plant and 3 algal genomes. We use a phylogenomic approach by which we can explain the formation of 88% of all arrangements by single-step events, such as fusion, fission, and terminal loss of domains. We find many domains are lost along every lineage, but at least 500 domains are novel, that is, they are unique to green plants and emerged more or less recently. These novel domains duplicate and rearrange more readily within their genomes than ancient domains and are overproportionally involved in stress response and developmental innovations. Novel domains more often affect regulatory proteins and show a higher degree of structural disorder than ancient domains. Whereas a relatively large and well-conserved core set of single-domain proteins exists, long multi-domain arrangements tend to be species-specific. We find that duplicated genes are more often involved in rearrangements. Although fission events typically impact metabolic proteins, fusion events often create new signaling proteins essential for environmental sensing. Taken together, the high volatility of single domains and complex arrangements in plant genomes demonstrate the importance of modularity for environmental adaptability of plants.
Terrapon, Nicolas; Grath, Sonja; Weiner, January; Moore, Andrew D.; Bornberg-Bauer, Erich
Fast Homology Search Using Domain-Architecture Alignment Proceedings
2012.
@proceedings{TERRAPON2012,
title = {Fast Homology Search Using Domain-Architecture Alignment},
author = {Nicolas Terrapon and Sonja Grath and January Weiner and Andrew D. Moore and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/10/terrapon_revision2012.pdf, Download},
year = {2012},
date = {2012-01-01},
urldate = {2012-01-01},
abstract = {Homology detection, i.e. the identification of genes that share common ancestry, is key
to understanding the evolutionary history of gene families. However, homology detection using
local sequence similarity alone (such as employed by BLAST) can be problematic when applied to
multi-domain proteins, as true homology can be masked by local similarity of domain sequences.
Here, we present a new approach for detecting homology that is based on the global alignment
of domain arrangements. It combines the ability of global alignments to capture homology across
the entire sequence with the efficiency and sensitivity of local alignments.},
keywords = {},
pubstate = {published},
tppubtype = {proceedings}
}
Homology detection, i.e. the identification of genes that share common ancestry, is key
to understanding the evolutionary history of gene families. However, homology detection using
local sequence similarity alone (such as employed by BLAST) can be problematic when applied to
multi-domain proteins, as true homology can be masked by local similarity of domain sequences.
Here, we present a new approach for detecting homology that is based on the global alignment
of domain arrangements. It combines the ability of global alignments to capture homology across
the entire sequence with the efficiency and sensitivity of local alignments.
to understanding the evolutionary history of gene families. However, homology detection using
local sequence similarity alone (such as employed by BLAST) can be problematic when applied to
multi-domain proteins, as true homology can be masked by local similarity of domain sequences.
Here, we present a new approach for detecting homology that is based on the global alignment
of domain arrangements. It combines the ability of global alignments to capture homology across
the entire sequence with the efficiency and sensitivity of local alignments.
2011
Grbić, Miodrag; Leeuwen, Thomas Van; Clark, Richard M.; Rombauts, Stephane; Rouzé, Pierre; Grbić, Vojislava; Osborne, Edward J.; Dermauw, Wannes; Ngoc, Phuong Cao Thi; Ortego, Félix; Hernández-Crespo, Pedro; Diaz, Isabel; Martinez, Manuel; Navajas, Maria; Sucena, Élio; Magalhães, Sara; Nagy, Lisa; Pace, Ryan M.; Djuranović, Sergej; Smagghe, Guy; Iga, Masatoshi; Christiaens, Olivier; Veenstra, Jan A.; Ewer, John; Villalobos, Rodrigo Mancilla; Hutter, Jeffrey L.; Hudson, Stephen D.; Velez, Marisela; Yi, Soojin V.; Zeng, Jia; Pires-daSilva, Andre; Roch, Fernando; Cazaux, Marc; Navarro, Marie; Zhurov, Vladimir; Acevedo, Gustavo; Bjelica, Anica; Fawcett, Jeffrey A.; Bonnet, Eric; Martens, Cindy; Baele, Guy; Wissler, Lothar; Sanchez-Rodriguez, Aminael; Tirry, Luc; Blais, Catherine; Demeestere, Kristof; Henz, Stefan R.; Gregory, T. Ryan; Mathieu, Johannes; Verdon, Lou; Farinelli, Laurent; Schmutz, Jeremy; Lindquist, Erika; Feyereisen, René; Peer, Yves Van
The genome of Tetranychus urticae reveals herbivorous pest adaptations Journal Article
In: Nature, vol. 479, pp. 487–492, 2011.
@article{Grbić2011,
title = {The genome of Tetranychus urticae reveals herbivorous pest adaptations},
author = {Miodrag Grbić and Thomas Van Leeuwen and Richard M. Clark and Stephane Rombauts and Pierre Rouzé and Vojislava Grbić and Edward J. Osborne and Wannes Dermauw and Phuong Cao Thi Ngoc and Félix Ortego and Pedro Hernández-Crespo and Isabel Diaz and Manuel Martinez and Maria Navajas and Élio Sucena and Sara Magalhães and Lisa Nagy and Ryan M. Pace and Sergej Djuranović and Guy Smagghe and Masatoshi Iga and Olivier Christiaens and Jan A. Veenstra and John Ewer and Rodrigo Mancilla Villalobos and Jeffrey L. Hutter and Stephen D. Hudson and Marisela Velez and Soojin V. Yi and Jia Zeng and Andre Pires-daSilva and Fernando Roch and Marc Cazaux and Marie Navarro and Vladimir Zhurov and Gustavo Acevedo and Anica Bjelica and Jeffrey A. Fawcett and Eric Bonnet and Cindy Martens and Guy Baele and Lothar Wissler and Aminael Sanchez-Rodriguez and Luc Tirry and Catherine Blais and Kristof Demeestere and Stefan R. Henz and T. Ryan Gregory and Johannes Mathieu and Lou Verdon and Laurent Farinelli and Jeremy Schmutz and Erika Lindquist and René Feyereisen and Yves Van Peer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Grbic2011.pdf, Download},
doi = {10.1038/nature10640},
year = {2011},
date = {2011-11-23},
journal = {Nature},
volume = {479},
pages = {487–492},
abstract = {The spider mite Tetranychus urticae is a cosmopolitan agricultural pest with an extensive host plant range and an extreme record of pesticide resistance. Here we present the completely sequenced and annotated spider mite genome, representing the first complete chelicerate genome. At 90 megabases T. urticae has the smallest sequenced arthropod genome. Compared with other arthropods, the spider mite genome shows unique changes in the hormonal environment and organization of the Hox complex, and also reveals evolutionary innovation of silk production. We find strong signatures of polyphagy and detoxification in gene families associated with feeding on different hosts and in new gene families acquired by lateral gene transfer. Deep transcriptome analysis of mites feeding on different plants shows how this pest responds to a changing host environment. The T. urticae genome thus offers new insights into arthropod evolution and plant–herbivore interactions, and provides unique opportunities for developing novel plant protection strategies.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The spider mite Tetranychus urticae is a cosmopolitan agricultural pest with an extensive host plant range and an extreme record of pesticide resistance. Here we present the completely sequenced and annotated spider mite genome, representing the first complete chelicerate genome. At 90 megabases T. urticae has the smallest sequenced arthropod genome. Compared with other arthropods, the spider mite genome shows unique changes in the hormonal environment and organization of the Hox complex, and also reveals evolutionary innovation of silk production. We find strong signatures of polyphagy and detoxification in gene families associated with feeding on different hosts and in new gene families acquired by lateral gene transfer. Deep transcriptome analysis of mites feeding on different plants shows how this pest responds to a changing host environment. The T. urticae genome thus offers new insights into arthropod evolution and plant–herbivore interactions, and provides unique opportunities for developing novel plant protection strategies.
Franssen, Susanne U.; Gu, Jenny; Bergmann, Nina; Winters, Gidon; Klostermeier, Ulrich C.; Rosenstiel, Philip; Bornberg-Bauer, Erich; Reusch, Thorsten B. H.
Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species Journal Article
In: Proceedings of the National Academy of Sciences, no. 48, pp. 19276-8, 2011.
@article{Franssen2011,
title = {Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species},
author = {Susanne U. Franssen and Jenny Gu and Nina Bergmann and Gidon Winters and Ulrich C. Klostermeier and Philip Rosenstiel and Erich Bornberg-Bauer and Thorsten B. H. Reusch},
url = {https://bornberglab.org/wp-content/uploads/2021/04/franssen2011.pdf, Download},
doi = {10.1073/pnas.1107680108},
year = {2011},
date = {2011-11-14},
journal = {Proceedings of the National Academy of Sciences},
number = {48},
pages = {19276-8},
abstract = {Large-scale transcription profiling via direct cDNA sequencing
provides important insights as to how foundation species cope
with increasing climatic extremes predicted under global warming.
Species distributed along a thermal cline, such as the ecologically
important seagrass Zostera marina, provide an opportunity to as-
sess temperature effects on gene expression as a function of their
long-term adaptation to heat stress. We exposed a southern and
northern European population of Zostera marina from contrasting
thermal environments to a realistic heat wave in a common-stress
garden. In a fully crossed experiment, eight cDNA libraries, each
comprising ∼125 000 reads, were obtained during and after a sim-
ulated heat wave, along with nonstressed control treatments. Al-
though gene-expression patterns during stress were similar in
both populations and were dominated by classical heat-shock pro-
teins, transcription profiles diverged after the heat wave. Gene-
expression patterns in southern genotypes returned to control
values immediately, but genotypes from the northern site failed
to recover and revealed the induction of genes involved in protein
degradation, indicating failed metabolic compensation to high
sea-surface temperature. We conclude that the return of gene-
expression patterns during recovery provides critical information
on thermal adaptation in aquatic habitats under climatic stress. As
a unifying concept for ecological genomics, we propose transcrip-
tomic resilience, analogous to ecological resilience, as an impor-
tant measure to predict the tolerance of individuals and hence the
fate of local populations in the face of global warming.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Large-scale transcription profiling via direct cDNA sequencing
provides important insights as to how foundation species cope
with increasing climatic extremes predicted under global warming.
Species distributed along a thermal cline, such as the ecologically
important seagrass Zostera marina, provide an opportunity to as-
sess temperature effects on gene expression as a function of their
long-term adaptation to heat stress. We exposed a southern and
northern European population of Zostera marina from contrasting
thermal environments to a realistic heat wave in a common-stress
garden. In a fully crossed experiment, eight cDNA libraries, each
comprising ∼125 000 reads, were obtained during and after a sim-
ulated heat wave, along with nonstressed control treatments. Al-
though gene-expression patterns during stress were similar in
both populations and were dominated by classical heat-shock pro-
teins, transcription profiles diverged after the heat wave. Gene-
expression patterns in southern genotypes returned to control
values immediately, but genotypes from the northern site failed
to recover and revealed the induction of genes involved in protein
degradation, indicating failed metabolic compensation to high
sea-surface temperature. We conclude that the return of gene-
expression patterns during recovery provides critical information
on thermal adaptation in aquatic habitats under climatic stress. As
a unifying concept for ecological genomics, we propose transcrip-
tomic resilience, analogous to ecological resilience, as an impor-
tant measure to predict the tolerance of individuals and hence the
fate of local populations in the face of global warming.
provides important insights as to how foundation species cope
with increasing climatic extremes predicted under global warming.
Species distributed along a thermal cline, such as the ecologically
important seagrass Zostera marina, provide an opportunity to as-
sess temperature effects on gene expression as a function of their
long-term adaptation to heat stress. We exposed a southern and
northern European population of Zostera marina from contrasting
thermal environments to a realistic heat wave in a common-stress
garden. In a fully crossed experiment, eight cDNA libraries, each
comprising ∼125 000 reads, were obtained during and after a sim-
ulated heat wave, along with nonstressed control treatments. Al-
though gene-expression patterns during stress were similar in
both populations and were dominated by classical heat-shock pro-
teins, transcription profiles diverged after the heat wave. Gene-
expression patterns in southern genotypes returned to control
values immediately, but genotypes from the northern site failed
to recover and revealed the induction of genes involved in protein
degradation, indicating failed metabolic compensation to high
sea-surface temperature. We conclude that the return of gene-
expression patterns during recovery provides critical information
on thermal adaptation in aquatic habitats under climatic stress. As
a unifying concept for ecological genomics, we propose transcrip-
tomic resilience, analogous to ecological resilience, as an impor-
tant measure to predict the tolerance of individuals and hence the
fate of local populations in the face of global warming.
Moore, Andrew D.; Bornberg-Bauer, Erich
The Dynamics and Evolutionary Potential of Domain Loss and Emergence Journal Article
In: Molecular Biology and Evolution, vol. 29, no. 2, pp. 787–796, 2011.
@article{Moore2011,
title = {The Dynamics and Evolutionary Potential of Domain Loss and Emergence},
author = {Andrew D. Moore and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/moore2011.pdf, Download},
doi = {10.1093/molbev/msr250},
year = {2011},
date = {2011-10-19},
journal = {Molecular Biology and Evolution},
volume = {29},
number = {2},
pages = {787–796},
abstract = {The wealth of available genomic data presents an unrivaled opportunity to study the molecular basis of evolution. Studies on gene family expansions and site-dependent analyses have already helped establish important insights into how proteins facilitate adaptation. However, efforts to conduct full-scale cross-genomic comparisons between species are challenged by both growing amounts of data and the inherent difficulty in accurately inferring homology between deeply rooted species. Proteins, in comparison, evolve by means of domain rearrangements, a process more amenable to study given the strength of profile-based homology inference and the lower rates with which rearrangements occur. However, adapting to a constantly changing environment can require molecular modulations beyond reach of rearrangement alone. Here, we explore rates and functional implications of novel domain emergence in contrast to domain gain and loss in 20 arthropod species of the pancrustacean clade. Emerging domains are more likely disordered in structure and spread more rapidly within their genomes than established domains. Furthermore, although domain turnover occurs at lower rates than gene family turnover, we find strong evidence that the emergence of novel domains is foremost associated with environmental adaptation such as abiotic stress response. The results presented here illustrate the simplicity with which domain-based analyses can unravel key players of nature's adaptational machinery, complementing the classical site-based analyses of adaptation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The wealth of available genomic data presents an unrivaled opportunity to study the molecular basis of evolution. Studies on gene family expansions and site-dependent analyses have already helped establish important insights into how proteins facilitate adaptation. However, efforts to conduct full-scale cross-genomic comparisons between species are challenged by both growing amounts of data and the inherent difficulty in accurately inferring homology between deeply rooted species. Proteins, in comparison, evolve by means of domain rearrangements, a process more amenable to study given the strength of profile-based homology inference and the lower rates with which rearrangements occur. However, adapting to a constantly changing environment can require molecular modulations beyond reach of rearrangement alone. Here, we explore rates and functional implications of novel domain emergence in contrast to domain gain and loss in 20 arthropod species of the pancrustacean clade. Emerging domains are more likely disordered in structure and spread more rapidly within their genomes than established domains. Furthermore, although domain turnover occurs at lower rates than gene family turnover, we find strong evidence that the emergence of novel domains is foremost associated with environmental adaptation such as abiotic stress response. The results presented here illustrate the simplicity with which domain-based analyses can unravel key players of nature's adaptational machinery, complementing the classical site-based analyses of adaptation.
Hartig, G; Niehuis, O; Grath, Sonja; Pohl, H; Donath, A; Eisenhart, C; Hertel, J; Krauss, V; Lehmann, J; Mayer, C; Tafer, H; Meusemann, K; Peters, RS; Beutel, RG; Stadler, P; Bornberg-Bauer, Erich; Misof, B
The first genome of a twisted wing parasite (Insectae: strepsiptera) and its phylogenetic implications Journal Article
In: Zitteliana, pp. 30-32, 2011.
@article{G2011,
title = {The first genome of a twisted wing parasite (Insectae: strepsiptera) and its phylogenetic implications},
author = {G Hartig and O Niehuis and Sonja Grath and H Pohl and A Donath and C Eisenhart and J Hertel and V Krauss and J Lehmann and C Mayer and H Tafer and K Meusemann and RS Peters and RG Beutel and P Stadler and Erich Bornberg-Bauer and B Misof},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Hartig2011.pdf, Download},
year = {2011},
date = {2011-10-11},
urldate = {2011-10-11},
journal = {Zitteliana},
pages = {30-32},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Reineke, Anna R.; Bornberg-Bauer, Erich; Gu, Jenny
Evolutionary divergence and limits of conserved non-coding sequence detection in plant genomes Journal Article
In: Nucleic Acids Research, vol. 39, no. 14, pp. 6029–6043, 2011.
@article{Reineke2011,
title = {Evolutionary divergence and limits of conserved non-coding sequence detection in plant genomes},
author = {Anna R. Reineke and Erich Bornberg-Bauer and Jenny Gu},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Reineke2011.pdf, Download},
doi = {10.1093/nar/gkr179},
year = {2011},
date = {2011-08-01},
journal = {Nucleic Acids Research},
volume = {39},
number = {14},
pages = {6029–6043},
abstract = {The discovery of regulatory motifs embedded in upstream regions of plants is a particularly challenging bioinformatics task. Previous studies have shown that motifs in plants are short compared with those found in vertebrates. Furthermore, plant genomes have undergone several diversification mechanisms such as genome duplication events which impact the evolution of regulatory motifs. In this article, a systematic phylogenomic comparison of upstream regions is conducted to further identify features of the plant regulatory genomes, the component of genomes regulating gene expression, to enable future de novo discoveries. The findings highlight differences in upstream region properties between major plant groups and the effects of divergence times and duplication events. First, clear differences in upstream region evolution can be detected between monocots and dicots, thus suggesting that a separation of these groups should be made when searching for novel regulatory motifs, particularly since universal motifs such as the TATA box are rare. Second, investigating the decay rate of significantly aligned regions suggests that a divergence time of ∼100 mya sets a limit for reliable conserved non-coding sequence (CNS) detection. Insights presented here will set a framework to help identify embedded motifs of functional relevance by understanding the limits of bioinformatics detection for CNSs.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The discovery of regulatory motifs embedded in upstream regions of plants is a particularly challenging bioinformatics task. Previous studies have shown that motifs in plants are short compared with those found in vertebrates. Furthermore, plant genomes have undergone several diversification mechanisms such as genome duplication events which impact the evolution of regulatory motifs. In this article, a systematic phylogenomic comparison of upstream regions is conducted to further identify features of the plant regulatory genomes, the component of genomes regulating gene expression, to enable future de novo discoveries. The findings highlight differences in upstream region properties between major plant groups and the effects of divergence times and duplication events. First, clear differences in upstream region evolution can be detected between monocots and dicots, thus suggesting that a separation of these groups should be made when searching for novel regulatory motifs, particularly since universal motifs such as the TATA box are rare. Second, investigating the decay rate of significantly aligned regions suggests that a divergence time of ∼100 mya sets a limit for reliable conserved non-coding sequence (CNS) detection. Insights presented here will set a framework to help identify embedded motifs of functional relevance by understanding the limits of bioinformatics detection for CNSs.
Franssen, Susanne U.; Shrestha, Roshan P; Bräutigam, Andrea; Bornberg-Bauer, Erich; Weber, Andreas P M
Comprehensive transcriptome analysis of the highly complex Pisum sativum genome using next generation sequencing Journal Article
In: BMC Genomics, vol. 12, no. 227, pp. 1-16, 2011.
@article{Franssen2011b,
title = {Comprehensive transcriptome analysis of the highly complex Pisum sativum genome using next generation sequencing},
author = {Susanne U. Franssen and Roshan P Shrestha and Andrea Bräutigam and Erich Bornberg-Bauer and Andreas P M Weber},
url = {https://bornberglab.org/wp-content/uploads/2021/10/franssen20112.pdf, Download},
doi = {10.1186/1471-2164-12-227},
year = {2011},
date = {2011-05-11},
urldate = {2011-05-11},
journal = {BMC Genomics},
volume = {12},
number = {227},
pages = {1-16},
abstract = {Background: The garden pea, Pisum sativum, is among the best-investigated legume plants and of significant agro-commercial relevance. Pisum sativum has a large and complex genome and accordingly few comprehensive genomic resources exist.
Results: We analyzed the pea transcriptome at the highest possible amount of accuracy by current technology. We used next generation sequencing with the Roche/454 platform and evaluated and compared a variety of approaches, including diverse tissue libraries, normalization, alternative sequencing technologies, saturation estimation and diverse assembly strategies. We generated libraries from flowers, leaves, cotyledons, epi- and hypocotyl, and etiolated and light treated etiolated seedlings, comprising a total of 450 megabases. Libraries were assembled into 324,428 unigenes in a first pass assembly.A second pass assembly reduced the amount to 81,449 unigenes but caused a significant number of chimeras. Analyses of the assemblies identified the assembly step as a major possibility for improvement. By recording frequencies of Arabidopsis orthologs hit by randomly drawn reads and fitting parameters of the saturation curve we concluded that sequencing was exhaustive. For leaf libraries we found normalization allows partial recovery of expression strength aside the desired effect of increased coverage. Based on theoretical and biological considerations we concluded that the sequence reads in the database tagged the vast majority of transcripts in the aerial tissues. A pathway representation analysis showed the merits of sampling multiple aerial tissues to increase the number of tagged genes. All results have been made available as a fully annotated database in fasta format.
Conclusions: We conclude that the approach taken resulted in a high quality - dataset which serves well as a first comprehensive reference set for the model legume pea. We suggest future deep sequencing transcriptome projects of species lacking a genomics backbone will need to concentrate mainly on resolving the issues of redundancy and paralogy during transcriptome assembly.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background: The garden pea, Pisum sativum, is among the best-investigated legume plants and of significant agro-commercial relevance. Pisum sativum has a large and complex genome and accordingly few comprehensive genomic resources exist.
Results: We analyzed the pea transcriptome at the highest possible amount of accuracy by current technology. We used next generation sequencing with the Roche/454 platform and evaluated and compared a variety of approaches, including diverse tissue libraries, normalization, alternative sequencing technologies, saturation estimation and diverse assembly strategies. We generated libraries from flowers, leaves, cotyledons, epi- and hypocotyl, and etiolated and light treated etiolated seedlings, comprising a total of 450 megabases. Libraries were assembled into 324,428 unigenes in a first pass assembly.A second pass assembly reduced the amount to 81,449 unigenes but caused a significant number of chimeras. Analyses of the assemblies identified the assembly step as a major possibility for improvement. By recording frequencies of Arabidopsis orthologs hit by randomly drawn reads and fitting parameters of the saturation curve we concluded that sequencing was exhaustive. For leaf libraries we found normalization allows partial recovery of expression strength aside the desired effect of increased coverage. Based on theoretical and biological considerations we concluded that the sequence reads in the database tagged the vast majority of transcripts in the aerial tissues. A pathway representation analysis showed the merits of sampling multiple aerial tissues to increase the number of tagged genes. All results have been made available as a fully annotated database in fasta format.
Conclusions: We conclude that the approach taken resulted in a high quality - dataset which serves well as a first comprehensive reference set for the model legume pea. We suggest future deep sequencing transcriptome projects of species lacking a genomics backbone will need to concentrate mainly on resolving the issues of redundancy and paralogy during transcriptome assembly.
Results: We analyzed the pea transcriptome at the highest possible amount of accuracy by current technology. We used next generation sequencing with the Roche/454 platform and evaluated and compared a variety of approaches, including diverse tissue libraries, normalization, alternative sequencing technologies, saturation estimation and diverse assembly strategies. We generated libraries from flowers, leaves, cotyledons, epi- and hypocotyl, and etiolated and light treated etiolated seedlings, comprising a total of 450 megabases. Libraries were assembled into 324,428 unigenes in a first pass assembly.A second pass assembly reduced the amount to 81,449 unigenes but caused a significant number of chimeras. Analyses of the assemblies identified the assembly step as a major possibility for improvement. By recording frequencies of Arabidopsis orthologs hit by randomly drawn reads and fitting parameters of the saturation curve we concluded that sequencing was exhaustive. For leaf libraries we found normalization allows partial recovery of expression strength aside the desired effect of increased coverage. Based on theoretical and biological considerations we concluded that the sequence reads in the database tagged the vast majority of transcripts in the aerial tissues. A pathway representation analysis showed the merits of sampling multiple aerial tissues to increase the number of tagged genes. All results have been made available as a fully annotated database in fasta format.
Conclusions: We conclude that the approach taken resulted in a high quality - dataset which serves well as a first comprehensive reference set for the model legume pea. We suggest future deep sequencing transcriptome projects of species lacking a genomics backbone will need to concentrate mainly on resolving the issues of redundancy and paralogy during transcriptome assembly.
Suen, Garret; Teiling, Clotilde; Li, Lewyn; Holt, Carson; Abouheif, Ehab; Bornberg-Bauer, Erich; Bouffard, Pascal; Caldera, Eric J.; Cash, Elizabeth; Cavanaugh, Amy; Denas, Olgert; Elhaik, Eran; Favé, Marie-Julie; Gadau, Jürgen; Gibson, Joshua D.; Graur, Dan; Grubbs, Kirk J.; Hagen, Darren E.; Harkins, Timothy T.; Helmkampf, Martin; Hu, Hao; Johnson, Brian R.; Kim, Jay; Marsh, Sarah E.; Moeller, Joseph A.; Muñoz-Torres, Mónica C.; Murphy, Marguerite C.; Naughton, Meredith C.; Nigam, Surabhi; Overson, Rick; Rajakumar, Rajendhran; Reese, Justin T.; Scott, Jarrod J.; Smith, Chris R.; Tao, Shu; Tsutsui, Neil D.; Viljakainen, Lumi; Wissler, Lothar; Yandell, Mark D.; Zimmer, Fabian; Taylor, James; Slater, Steven C.; Clifton, Sandra W.; Warren, Wesley C.; Elsik, Christine G.; Smith, Christopher D.; Weinstock, George M.; Gerardo, Nicole M.; Currie, Cameron R.
The Genome Sequence of the Leaf-Cutter Ant Atta cephalotes Reveals Insights into Its Obligate Symbiotic Lifestyle Journal Article
In: PLOS Genetics, 2011.
@article{Suen2011,
title = {The Genome Sequence of the Leaf-Cutter Ant Atta cephalotes Reveals Insights into Its Obligate Symbiotic Lifestyle},
author = {Garret Suen and Clotilde Teiling and Lewyn Li and Carson Holt and Ehab Abouheif and Erich Bornberg-Bauer and Pascal Bouffard and Eric J. Caldera and Elizabeth Cash and Amy Cavanaugh and Olgert Denas and Eran Elhaik and Marie-Julie Favé and Jürgen Gadau and Joshua D. Gibson and Dan Graur and Kirk J. Grubbs and Darren E. Hagen and Timothy T. Harkins and Martin Helmkampf and Hao Hu and Brian R. Johnson and Jay Kim and Sarah E. Marsh and Joseph A. Moeller and Mónica C. Muñoz-Torres and Marguerite C. Murphy and Meredith C. Naughton and Surabhi Nigam and Rick Overson and Rajendhran Rajakumar and Justin T. Reese and Jarrod J. Scott and Chris R. Smith and Shu Tao and Neil D. Tsutsui and Lumi Viljakainen and Lothar Wissler and Mark D. Yandell and Fabian Zimmer and James Taylor and Steven C. Slater and Sandra W. Clifton and Wesley C. Warren and Christine G. Elsik and Christopher D. Smith and George M. Weinstock and Nicole M. Gerardo and Cameron R. Currie},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Suen2011.pdf, Download},
doi = {10.1371/journal.pgen.1002007},
year = {2011},
date = {2011-02-10},
journal = {PLOS Genetics},
abstract = {Leaf-cutter ants are one of the most important herbivorous insects in the Neotropics, harvesting vast quantities of fresh leaf material. The ants use leaves to cultivate a fungus that serves as the colony's primary food source. This obligate ant-fungus mutualism is one of the few occurrences of farming by non-humans and likely facilitated the formation of their massive colonies. Mature leaf-cutter ant colonies contain millions of workers ranging in size from small garden tenders to large soldiers, resulting in one of the most complex polymorphic caste systems within ants. To begin uncovering the genomic underpinnings of this system, we sequenced the genome of Atta cephalotes using 454 pyrosequencing. One prediction from this ant's lifestyle is that it has undergone genetic modifications that reflect its obligate dependence on the fungus for nutrients. Analysis of this genome sequence is consistent with this hypothesis, as we find evidence for reductions in genes related to nutrient acquisition. These include extensive reductions in serine proteases (which are likely unnecessary because proteolysis is not a primary mechanism used to process nutrients obtained from the fungus), a loss of genes involved in arginine biosynthesis (suggesting that this amino acid is obtained from the fungus), and the absence of a hexamerin (which sequesters amino acids during larval development in other insects). Following recent reports of genome sequences from other insects that engage in symbioses with beneficial microbes, the A. cephalotes genome provides new insights into the symbiotic lifestyle of this ant and advances our understanding of host–microbe symbioses},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Leaf-cutter ants are one of the most important herbivorous insects in the Neotropics, harvesting vast quantities of fresh leaf material. The ants use leaves to cultivate a fungus that serves as the colony's primary food source. This obligate ant-fungus mutualism is one of the few occurrences of farming by non-humans and likely facilitated the formation of their massive colonies. Mature leaf-cutter ant colonies contain millions of workers ranging in size from small garden tenders to large soldiers, resulting in one of the most complex polymorphic caste systems within ants. To begin uncovering the genomic underpinnings of this system, we sequenced the genome of Atta cephalotes using 454 pyrosequencing. One prediction from this ant's lifestyle is that it has undergone genetic modifications that reflect its obligate dependence on the fungus for nutrients. Analysis of this genome sequence is consistent with this hypothesis, as we find evidence for reductions in genes related to nutrient acquisition. These include extensive reductions in serine proteases (which are likely unnecessary because proteolysis is not a primary mechanism used to process nutrients obtained from the fungus), a loss of genes involved in arginine biosynthesis (suggesting that this amino acid is obtained from the fungus), and the absence of a hexamerin (which sequesters amino acids during larval development in other insects). Following recent reports of genome sequences from other insects that engage in symbioses with beneficial microbes, the A. cephalotes genome provides new insights into the symbiotic lifestyle of this ant and advances our understanding of host–microbe symbioses
Wissler, Lothar; Codoñer, Francisco M; Gu, Jenny; Reusch, Thorsten BH; Olsen, Jeanine L; Procaccini, Gabriele; Bornberg-Bauer, Erich
Back to the sea twice: identifying candidate plant genes for molecular evolution to marine life Journal Article
In: BMC Evolutionary Biology, vol. 11, no. 8, pp. 1-13, 2011.
@article{Wissler2011,
title = {Back to the sea twice: identifying candidate plant genes for molecular evolution to marine life},
author = {Lothar Wissler and Francisco M Codoñer and Jenny Gu and Thorsten BH Reusch and Jeanine L Olsen and Gabriele Procaccini and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/wissler2011.pdf, Download},
doi = {10.1186/1471-2148-11-8},
year = {2011},
date = {2011-01-12},
urldate = {2011-01-12},
journal = {BMC Evolutionary Biology},
volume = {11},
number = {8},
pages = {1-13},
abstract = {Background
Seagrasses are a polyphyletic group of monocotyledonous angiosperms that have adapted to a completely submerged lifestyle in marine waters. Here, we exploit two collections of expressed sequence tags (ESTs) of two wide-spread and ecologically important seagrass species, the Mediterranean seagrass Posidonia oceanica (L.) Delile and the eelgrass Zostera marina L., which have independently evolved from aquatic ancestors. This replicated, yet independent evolutionary history facilitates the identification of traits that may have evolved in parallel and are possible instrumental candidates for adaptation to a marine habitat.
Results
In our study, we provide the first quantitative perspective on molecular adaptations in two seagrass species. By constructing orthologous gene clusters shared between two seagrasses (Z. marina and P. oceanica) and eight distantly related terrestrial angiosperm species, 51 genes could be identified with detection of positive selection along the seagrass branches of the phylogenetic tree. Characterization of these positively selected genes using KEGG pathways and the Gene Ontology uncovered that these genes are mostly involved in translation, metabolism, and photosynthesis.
Conclusions
These results provide first insights into which seagrass genes have diverged from their terrestrial counterparts via an initial aquatic stage characteristic of the order and to the derived fully-marine stage characteristic of seagrasses. We discuss how adaptive changes in these processes may have contributed to the evolution towards an aquatic and marine existence.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
Seagrasses are a polyphyletic group of monocotyledonous angiosperms that have adapted to a completely submerged lifestyle in marine waters. Here, we exploit two collections of expressed sequence tags (ESTs) of two wide-spread and ecologically important seagrass species, the Mediterranean seagrass Posidonia oceanica (L.) Delile and the eelgrass Zostera marina L., which have independently evolved from aquatic ancestors. This replicated, yet independent evolutionary history facilitates the identification of traits that may have evolved in parallel and are possible instrumental candidates for adaptation to a marine habitat.
Results
In our study, we provide the first quantitative perspective on molecular adaptations in two seagrass species. By constructing orthologous gene clusters shared between two seagrasses (Z. marina and P. oceanica) and eight distantly related terrestrial angiosperm species, 51 genes could be identified with detection of positive selection along the seagrass branches of the phylogenetic tree. Characterization of these positively selected genes using KEGG pathways and the Gene Ontology uncovered that these genes are mostly involved in translation, metabolism, and photosynthesis.
Conclusions
These results provide first insights into which seagrass genes have diverged from their terrestrial counterparts via an initial aquatic stage characteristic of the order and to the derived fully-marine stage characteristic of seagrasses. We discuss how adaptive changes in these processes may have contributed to the evolution towards an aquatic and marine existence.
Seagrasses are a polyphyletic group of monocotyledonous angiosperms that have adapted to a completely submerged lifestyle in marine waters. Here, we exploit two collections of expressed sequence tags (ESTs) of two wide-spread and ecologically important seagrass species, the Mediterranean seagrass Posidonia oceanica (L.) Delile and the eelgrass Zostera marina L., which have independently evolved from aquatic ancestors. This replicated, yet independent evolutionary history facilitates the identification of traits that may have evolved in parallel and are possible instrumental candidates for adaptation to a marine habitat.
Results
In our study, we provide the first quantitative perspective on molecular adaptations in two seagrass species. By constructing orthologous gene clusters shared between two seagrasses (Z. marina and P. oceanica) and eight distantly related terrestrial angiosperm species, 51 genes could be identified with detection of positive selection along the seagrass branches of the phylogenetic tree. Characterization of these positively selected genes using KEGG pathways and the Gene Ontology uncovered that these genes are mostly involved in translation, metabolism, and photosynthesis.
Conclusions
These results provide first insights into which seagrass genes have diverged from their terrestrial counterparts via an initial aquatic stage characteristic of the order and to the derived fully-marine stage characteristic of seagrasses. We discuss how adaptive changes in these processes may have contributed to the evolution towards an aquatic and marine existence.
Ernst, Antonia M.; Rüping, Boris; Jekat, Stephan B.; Nordzieke, Steffen; Reineke, Anna R.; Müller, Boje; Bornberg-Bauer, Erich; Prüfer, Dirk; Noll, Gundula A.
The sieve element occlusion gene family in dicotyledonous plants Journal Article
In: Plant Signal Behaviour, vol. 6, no. 19, pp. 151-3, 2011.
@article{Ernst2011,
title = {The sieve element occlusion gene family in dicotyledonous plants},
author = {Antonia M. Ernst and Boris Rüping and Stephan B. Jekat and Steffen Nordzieke and Anna R. Reineke and Boje Müller and Erich Bornberg-Bauer and Dirk Prüfer and Gundula A. Noll},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Ernst2011.pdf, Download},
doi = {10.4161/psb.6.1.14308},
year = {2011},
date = {2011-01-03},
urldate = {2011-01-03},
journal = {Plant Signal Behaviour},
volume = {6},
number = {19},
pages = {151-3},
abstract = {Sieve element occlusion (SEO) genes encoding forisome subunits have been identified in Medicago truncatula and other legumes. Forisomes are structural phloem proteins uniquely found in Fabaceae sieve elements. They undergo a reversible conformational change after wounding, from a condensed to a dispersed state, thereby blocking sieve tube translocation and preventing the loss of photoassimilates. Recently, we identified SEO genes in several non-Fabaceae plants (lacking forisomes) and concluded that they most probably encode conventional non-forisome P-proteins. Molecular and phylogenetic analysis of the SEO gene family has identified domains that are characteristic for SEO proteins. Here, we extended our phylogenetic analysis by including additional SEO genes from several diverse species based on recently published genomic data. Our results strengthen the original assumption that SEO genes seem to be widespread in dicotyledonous angiosperms, and further underline the divergent evolution of SEO genes within the Fabaceae.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Sieve element occlusion (SEO) genes encoding forisome subunits have been identified in Medicago truncatula and other legumes. Forisomes are structural phloem proteins uniquely found in Fabaceae sieve elements. They undergo a reversible conformational change after wounding, from a condensed to a dispersed state, thereby blocking sieve tube translocation and preventing the loss of photoassimilates. Recently, we identified SEO genes in several non-Fabaceae plants (lacking forisomes) and concluded that they most probably encode conventional non-forisome P-proteins. Molecular and phylogenetic analysis of the SEO gene family has identified domains that are characteristic for SEO proteins. Here, we extended our phylogenetic analysis by including additional SEO genes from several diverse species based on recently published genomic data. Our results strengthen the original assumption that SEO genes seem to be widespread in dicotyledonous angiosperms, and further underline the divergent evolution of SEO genes within the Fabaceae.
Sikosek, Tobias; Bornberg-Bauer, Erich
Evolution after and before gene duplication? Book Chapter
In: pp. 105-132, John Wiley & Sons, 2011.
@inbook{Sikosek2010,
title = {Evolution after and before gene duplication?},
author = {Tobias Sikosek and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Sikosek2010.pdf, Download},
year = {2011},
date = {2011-01-01},
urldate = {2010-10-01},
pages = {105-132},
publisher = {John Wiley & Sons},
abstract = {Most hypotheses about the evolution of new proteins via the mechanism of gene duplication and divergence only take into account the processes following the duplication event. The Neofunctionalisation hypothesis assumes that, due to the functional redundancy of the two gene copies, one is free to undergo adaptation towards a new function. The Subfunctionalisation hypothesis, assumes that, for a while, the duplicates retain complementary subfunctions of the original gene. Here, we review evidence for adaptive changes occurring in proteins (or single protein domains) that have not (yet) undergone gene duplication. These changes are neutral with respect to the fitness contribution of the native function of a protein, but potentially adaptive regarding the fitness contributions of latent or promiscuous functions. It is likely that those promiscuous functions are associated with different protein conformations existing in equilibrium. If a gene duplication occurs for a protein that has both a native as well as an advantageous promiscuous function, the resulting duplicates potentially subfunctionalise more easily than proteins adapted to just one function.},
keywords = {},
pubstate = {published},
tppubtype = {inbook}
}
Most hypotheses about the evolution of new proteins via the mechanism of gene duplication and divergence only take into account the processes following the duplication event. The Neofunctionalisation hypothesis assumes that, due to the functional redundancy of the two gene copies, one is free to undergo adaptation towards a new function. The Subfunctionalisation hypothesis, assumes that, for a while, the duplicates retain complementary subfunctions of the original gene. Here, we review evidence for adaptive changes occurring in proteins (or single protein domains) that have not (yet) undergone gene duplication. These changes are neutral with respect to the fitness contribution of the native function of a protein, but potentially adaptive regarding the fitness contributions of latent or promiscuous functions. It is likely that those promiscuous functions are associated with different protein conformations existing in equilibrium. If a gene duplication occurs for a protein that has both a native as well as an advantageous promiscuous function, the resulting duplicates potentially subfunctionalise more easily than proteins adapted to just one function.
2010
Schüler, Andreas; Bornberg-Bauer, Erich
The Evolution of Protein Interaction Networks Journal Article
In: Data Mining in Proteomics, pp. 273-289, 2010.
@article{Schüler2010,
title = {The Evolution of Protein Interaction Networks},
author = {Andreas Schüler and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Schuler2010.pdf, Download},
year = {2010},
date = {2010-10-13},
journal = {Data Mining in Proteomics},
pages = {273-289},
abstract = {The availability of high-throughput methods to detect protein interactions made construction of comprehensive protein interaction networks for several important model organisms possible. Many studies have since focused on uncovering the structural principles of these networks and relating these structures to biological processes. On a global scale, there are striking similarities in the structure of different protein interaction networks, even when distantly related species, such as the yeast Saccharomyces cerevisiae and the fruit fly Drosophila melanogaster, are compared. However, there is also considerable variance in network structures caused by the gain and loss of genes and mutations which alter the interaction behavior of the encoded proteins. Here, we focus on the current state of knowledge on the structure of protein interaction networks and the evolutionary processes that shaped these structures.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The availability of high-throughput methods to detect protein interactions made construction of comprehensive protein interaction networks for several important model organisms possible. Many studies have since focused on uncovering the structural principles of these networks and relating these structures to biological processes. On a global scale, there are striking similarities in the structure of different protein interaction networks, even when distantly related species, such as the yeast Saccharomyces cerevisiae and the fruit fly Drosophila melanogaster, are compared. However, there is also considerable variance in network structures caused by the gain and loss of genes and mutations which alter the interaction behavior of the encoded proteins. Here, we focus on the current state of knowledge on the structure of protein interaction networks and the evolutionary processes that shaped these structures.
Rüping, Boris; Ernst, Antonia M.; Jekat, Stephan B.; Nordzieke, Steffen; Reineke, Anna R.; Müller, Boje; Bornberg-Bauer, Erich; Prüfer, Dirk
Molecular and phylogenetic characterization of the sieve element occlusion gene family in Fabaceae and non-Fabaceae plants Journal Article
In: BMC Plant Biology, vol. 10, no. 219, pp. 1-14, 2010.
@article{Rüping2010,
title = {Molecular and phylogenetic characterization of the sieve element occlusion gene family in Fabaceae and non-Fabaceae plants},
author = {Boris Rüping and Antonia M. Ernst and Stephan B. Jekat and Steffen Nordzieke and Anna R. Reineke and Boje Müller and Erich Bornberg-Bauer and Dirk Prüfer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Ruping2010.pdf, Download},
doi = {10.1186/1471-2229-10-219},
year = {2010},
date = {2010-10-08},
urldate = {2010-10-08},
journal = {BMC Plant Biology},
volume = {10},
number = {219},
pages = {1-14},
abstract = {Background The phloem of dicotyledonous plants contains specialized P-proteins (phloem proteins) that accumulate during sieve element differentiation and remain parietally associated with the cisternae of the endoplasmic reticulum in mature sieve elements. Wounding causes P-protein filaments to accumulate at the sieve plates and block the translocation of photosynthate. Specialized, spindle-shaped P-proteins known as forisomes that undergo reversible calcium-dependent conformational changes have evolved exclusively in the Fabaceae. Recently, the molecular characterization of three genes encoding forisome components in the model legume Medicago truncatula (MtSEO1, MtSEO2 and MtSEO3; SEO = sieve element occlusion) was reported, but little is known about the molecular characteristics of P-proteins in non-Fabaceae.
Results
We performed a comprehensive genome-wide comparative analysis by screening the M. truncatula, Glycine max, Arabidopsis thaliana, Vitis vinifera and Solanum phureja genomes, and a Malus domestica EST library for homologs of MtSEO1, MtSEO2 and MtSEO3 and identified numerous novel SEO genes in Fabaceae and even non-Fabaceae plants, which do not possess forisomes. Even in Fabaceae some SEO genes appear to not encode forisome components. All SEO genes have a similar exon-intron structure and are expressed predominantly in the phloem. Phylogenetic analysis revealed the presence of several subgroups with Fabaceae-specific subgroups containing all of the known as well as newly identified forisome component proteins. We constructed Hidden Markov Models that identified three conserved protein domains, which characterize SEO proteins when present in combination. In addition, one common and three subgroup specific protein motifs were found in the amino acid sequences of SEO proteins. SEO genes are organized in genomic clusters and the conserved synteny allowed us to identify several M. truncatula vs G. max orthologs as well as paralogs within the G. max genome.
Conclusions
The unexpected occurrence of forisome-like genes in non-Fabaceae plants may indicate that these proteins encode species-specific P-proteins, which is backed up by the phloem-specific expression profiles. The conservation of gene structure, the presence of specific motifs and domains and the genomic synteny argue for a common phylogenetic origin of forisomes and other P-proteins.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background The phloem of dicotyledonous plants contains specialized P-proteins (phloem proteins) that accumulate during sieve element differentiation and remain parietally associated with the cisternae of the endoplasmic reticulum in mature sieve elements. Wounding causes P-protein filaments to accumulate at the sieve plates and block the translocation of photosynthate. Specialized, spindle-shaped P-proteins known as forisomes that undergo reversible calcium-dependent conformational changes have evolved exclusively in the Fabaceae. Recently, the molecular characterization of three genes encoding forisome components in the model legume Medicago truncatula (MtSEO1, MtSEO2 and MtSEO3; SEO = sieve element occlusion) was reported, but little is known about the molecular characteristics of P-proteins in non-Fabaceae.
Results
We performed a comprehensive genome-wide comparative analysis by screening the M. truncatula, Glycine max, Arabidopsis thaliana, Vitis vinifera and Solanum phureja genomes, and a Malus domestica EST library for homologs of MtSEO1, MtSEO2 and MtSEO3 and identified numerous novel SEO genes in Fabaceae and even non-Fabaceae plants, which do not possess forisomes. Even in Fabaceae some SEO genes appear to not encode forisome components. All SEO genes have a similar exon-intron structure and are expressed predominantly in the phloem. Phylogenetic analysis revealed the presence of several subgroups with Fabaceae-specific subgroups containing all of the known as well as newly identified forisome component proteins. We constructed Hidden Markov Models that identified three conserved protein domains, which characterize SEO proteins when present in combination. In addition, one common and three subgroup specific protein motifs were found in the amino acid sequences of SEO proteins. SEO genes are organized in genomic clusters and the conserved synteny allowed us to identify several M. truncatula vs G. max orthologs as well as paralogs within the G. max genome.
Conclusions
The unexpected occurrence of forisome-like genes in non-Fabaceae plants may indicate that these proteins encode species-specific P-proteins, which is backed up by the phloem-specific expression profiles. The conservation of gene structure, the presence of specific motifs and domains and the genomic synteny argue for a common phylogenetic origin of forisomes and other P-proteins.
Results
We performed a comprehensive genome-wide comparative analysis by screening the M. truncatula, Glycine max, Arabidopsis thaliana, Vitis vinifera and Solanum phureja genomes, and a Malus domestica EST library for homologs of MtSEO1, MtSEO2 and MtSEO3 and identified numerous novel SEO genes in Fabaceae and even non-Fabaceae plants, which do not possess forisomes. Even in Fabaceae some SEO genes appear to not encode forisome components. All SEO genes have a similar exon-intron structure and are expressed predominantly in the phloem. Phylogenetic analysis revealed the presence of several subgroups with Fabaceae-specific subgroups containing all of the known as well as newly identified forisome component proteins. We constructed Hidden Markov Models that identified three conserved protein domains, which characterize SEO proteins when present in combination. In addition, one common and three subgroup specific protein motifs were found in the amino acid sequences of SEO proteins. SEO genes are organized in genomic clusters and the conserved synteny allowed us to identify several M. truncatula vs G. max orthologs as well as paralogs within the G. max genome.
Conclusions
The unexpected occurrence of forisome-like genes in non-Fabaceae plants may indicate that these proteins encode species-specific P-proteins, which is backed up by the phloem-specific expression profiles. The conservation of gene structure, the presence of specific motifs and domains and the genomic synteny argue for a common phylogenetic origin of forisomes and other P-proteins.
Bornberg-Bauer, Erich
Signals: Tinkering with Domains Journal Article
In: Science Signaling, vol. 14, no. 3, pp. 31-32, 2010.
@article{Bornberg-Bauer2010,
title = {Signals: Tinkering with Domains},
author = {Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/bornberg-bauer2010.pdf, Download},
doi = {10.1126/scisignal.3139pe31},
year = {2010},
date = {2010-09-14},
urldate = {2010-09-14},
journal = {Science Signaling},
volume = {14},
number = {3},
pages = {31-32},
abstract = {Evolution reuses established modules. At the level of cell signaling, protein domains are used in many contexts to transfer different messages. A frequently occurring binding domain uses a structural scaffold to allow for sequence variation at critical sites without compromising structural stability. Even random mutations have a high chance of conferring a novel function, and only a small fraction of available sequence space is actually explored. Accordingly, current lab techniques allow us to infer evolutionary routes, exploring the possible and the attainable in terms of complex structure-function relationships.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Evolution reuses established modules. At the level of cell signaling, protein domains are used in many contexts to transfer different messages. A frequently occurring binding domain uses a structural scaffold to allow for sequence variation at critical sites without compromising structural stability. Even random mutations have a high chance of conferring a novel function, and only a small fraction of available sequence space is actually explored. Accordingly, current lab techniques allow us to infer evolutionary routes, exploring the possible and the attainable in terms of complex structure-function relationships.
Chen, Tao; Vernazobres, David; Yomo, Tetsuya; Bornberg-Bauer, Erich; Chan, Hue Sun
Evolvability and Single-Genotype Fluctuation in Phenotypic Properties: A Simple Heteropolymer Model Journal Article
In: Biophysical Journal, vol. 98, no. 11, pp. 2487-2496, 2010.
@article{Chen2010,
title = {Evolvability and Single-Genotype Fluctuation in Phenotypic Properties: A Simple Heteropolymer Model},
author = {Tao Chen and David Vernazobres and Tetsuya Yomo and Erich Bornberg-Bauer and Hue Sun Chan},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Chen2010.pdf, Download},
doi = {10.1016/j.bpj.2010.02.046},
year = {2010},
date = {2010-06-02},
journal = {Biophysical Journal},
volume = {98},
number = {11},
pages = {2487-2496},
abstract = {Experiment showed that the response of a genotype to mutation, i.e., the magnitude of mutational change in a phenotypic property, can be correlated with the extent of phenotypic fluctuation among genetic clones. To address a possible statistical mechanical basis for such phenomena at the protein level, we consider a simple hydrophobic-polar lattice protein-chain model with an exhaustive mapping between sequence (genotype) and conformational (phenotype) spaces. Using squared end-to-end distance, RN2, as an example conformational property, we study how the thermal fluctuation of a sequence's RN2 may be predictive of the changes in the Boltzmann average 〈RN2〉 caused by single-point mutations on that sequence. We found that sequences with the same ground-state (RN2)0 exhibit a funnel-like organization under conditions favorable to chain collapse or folding: fluctuation (standard deviation σ) of RN2 tends to increase with mutational distance from a prototype sequence whose 〈RN2〉 deviates little from its (RN2)0. In general, large mutational decreases in 〈RN2〉 or in σ are only possible for some, though not all, sequences with large σ values. This finding suggests that single-genotype phenotypic fluctuation is a necessary, though not sufficient, indicator of evolvability toward genotypes with less phenotypic fluctuations.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Experiment showed that the response of a genotype to mutation, i.e., the magnitude of mutational change in a phenotypic property, can be correlated with the extent of phenotypic fluctuation among genetic clones. To address a possible statistical mechanical basis for such phenomena at the protein level, we consider a simple hydrophobic-polar lattice protein-chain model with an exhaustive mapping between sequence (genotype) and conformational (phenotype) spaces. Using squared end-to-end distance, RN2, as an example conformational property, we study how the thermal fluctuation of a sequence's RN2 may be predictive of the changes in the Boltzmann average 〈RN2〉 caused by single-point mutations on that sequence. We found that sequences with the same ground-state (RN2)0 exhibit a funnel-like organization under conditions favorable to chain collapse or folding: fluctuation (standard deviation σ) of RN2 tends to increase with mutational distance from a prototype sequence whose 〈RN2〉 deviates little from its (RN2)0. In general, large mutational decreases in 〈RN2〉 or in σ are only possible for some, though not all, sequences with large σ values. This finding suggests that single-genotype phenotypic fluctuation is a necessary, though not sufficient, indicator of evolvability toward genotypes with less phenotypic fluctuations.
Bornberg-Bauer, Erich; Kramer, Linus
Robustness versus evolvability: a paradigm revisited Journal Article
In: HFSP Journal, vol. 4, no. 3-4, pp. 105-108, 2010.
@article{Bornberg-Bauer2010b,
title = {Robustness versus evolvability: a paradigm revisited},
author = {Erich Bornberg-Bauer and Linus Kramer},
url = {https://bornberglab.org/wp-content/uploads/2021/10/bornberg-bauer20102.pdf, Download},
doi = {10.2976/1.3404403},
year = {2010},
date = {2010-06-01},
journal = {HFSP Journal},
volume = {4},
number = {3-4},
pages = {105-108},
abstract = {Evolvability is the property of a biological system to quickly adapt to new requirements. Robustness seems to be the opposite. Nonetheless many biological systems display both properties—a puzzling observation, which has caused many debates over the last decades. A recently published model by Draghi et al. [Nature 463, 353–355 (2010)] elegantly circumvents complications of earlier in silico studies of molecular systems and provides an analytical solution, which is surprisingly independent from parameter choice. Depending on the mutation rate and the number of accessible phenotypes at any given genotype, evolvability and robustness can be reconciled. Further research will need to investigate if these parameter settings adequately represent the range of degrees of freedom covered by natural systems and if natural systems indeed assume a state in which both properties, robustness and evolvability, are featured.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Evolvability is the property of a biological system to quickly adapt to new requirements. Robustness seems to be the opposite. Nonetheless many biological systems display both properties—a puzzling observation, which has caused many debates over the last decades. A recently published model by Draghi et al. [Nature 463, 353–355 (2010)] elegantly circumvents complications of earlier in silico studies of molecular systems and provides an analytical solution, which is surprisingly independent from parameter choice. Depending on the mutation rate and the number of accessible phenotypes at any given genotype, evolvability and robustness can be reconciled. Further research will need to investigate if these parameter settings adequately represent the range of degrees of freedom covered by natural systems and if natural systems indeed assume a state in which both properties, robustness and evolvability, are featured.
Bornberg-Bauer, Erich; Huylmans, Ann K.; Sikosek, Tobias
How do new proteins arise? Journal Article
In: Current Opinion in Structural Biology, vol. 20, no. 344, pp. 390-396, 2010.
@article{Bornberg-Bauer2010c,
title = {How do new proteins arise?},
author = {Erich Bornberg-Bauer and Ann K. Huylmans and Tobias Sikosek},
url = {https://bornberglab.org/wp-content/uploads/2021/10/bornberg-bauer20103.pdf, Download},
doi = {10.1016/j.sbi.2010.02.005},
year = {2010},
date = {2010-06-01},
urldate = {2010-06-01},
journal = {Current Opinion in Structural Biology},
volume = {20},
number = {344},
pages = {390-396},
abstract = {Proteins are surreptitious cellular agents: while robust against mutations they are very evolvable; most are marginally stable and dynamic but others form a stable cellular matrix. Some genes seem to have emerged de novo from random pieces of genomic DNA, others may have been around for billions of years, virtually unchanged. Genomic and structural data provide new insights on how proteins came such a long way, probably from an initially very small set of domains and domain arrangements: gene duplicates provide the raw material for adaptive transitions (for example from one fold to another) which are very rare, albeit not impossible. ‘New’ proteins predominantly arise via tinkering, that is by their underlying genes recruiting and adapting smaller fragments of neighbouring DNA or by modular rearrangements of established domain combinations. Such rearrangements arise predominantly via fusion and terminal loss.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Proteins are surreptitious cellular agents: while robust against mutations they are very evolvable; most are marginally stable and dynamic but others form a stable cellular matrix. Some genes seem to have emerged de novo from random pieces of genomic DNA, others may have been around for billions of years, virtually unchanged. Genomic and structural data provide new insights on how proteins came such a long way, probably from an initially very small set of domains and domain arrangements: gene duplicates provide the raw material for adaptive transitions (for example from one fold to another) which are very rare, albeit not impossible. ‘New’ proteins predominantly arise via tinkering, that is by their underlying genes recruiting and adapting smaller fragments of neighbouring DNA or by modular rearrangements of established domain combinations. Such rearrangements arise predominantly via fusion and terminal loss.
Moore, Andrew D.; Bornberg-Bauer, Erich
Protein Domains as Evolutionary Units Journal Article
In: Evolutionary Genomics and Systems Biology, 2010.
@article{Moore2010,
title = {Protein Domains as Evolutionary Units},
author = {Andrew D. Moore and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/moore2010.pdf, Download},
year = {2010},
date = {2010-04-01},
journal = {Evolutionary Genomics and Systems Biology},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Werren, John H.; Richards, Stephen; [....],; Bornberg-Bauer, Erich; [....],; Yamada, Takuji; Yi, Soojin V.; Zecher, Courtney N.; Zhang, Lan; Gibbs, Richard A.
Functional and Evolutionary Insights from the Genomes of Three Parasitoid Nasonia Species Journal Article
In: Science, vol. 327, no. 5963, pp. 343-348, 2010.
@article{Werren2010,
title = {Functional and Evolutionary Insights from the Genomes of Three Parasitoid Nasonia Species},
author = {John H. Werren and Stephen Richards and [....] and Erich Bornberg-Bauer and [....] and Takuji Yamada and Soojin V. Yi and Courtney N. Zecher and Lan Zhang and Richard A. Gibbs},
url = {https://bornberglab.org/wp-content/uploads/2021/10/werren2010.pdf, Download},
doi = {10.1126/science.1178028},
year = {2010},
date = {2010-01-15},
urldate = {2010-01-15},
journal = {Science},
volume = {327},
number = {5963},
pages = {343-348},
abstract = {We report here genome sequences and comparative analyses of three closely related parasitoid wasps: Nasonia vitripennis, N. giraulti, and N. longicornis. Parasitoids are important regulators of arthropod populations, including major agricultural pests and disease vectors, and Nasonia is an emerging genetic model, particularly for evolutionary and developmental genetics. Key findings include the identification of a functional DNA methylation tool kit; hymenopteran-specific genes including diverse venoms; lateral gene transfers among Pox viruses, Wolbachia, and Nasonia; and the rapid evolution of genes involved in nuclear-mitochondrial interactions that are implicated in speciation. Newly developed genome resources advance Nasonia for genetic research, accelerate mapping and cloning of quantitative trait loci, and will ultimately provide tools and knowledge for further increasing the utility of parasitoids as pest insect-control agents.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
We report here genome sequences and comparative analyses of three closely related parasitoid wasps: Nasonia vitripennis, N. giraulti, and N. longicornis. Parasitoids are important regulators of arthropod populations, including major agricultural pests and disease vectors, and Nasonia is an emerging genetic model, particularly for evolutionary and developmental genetics. Key findings include the identification of a functional DNA methylation tool kit; hymenopteran-specific genes including diverse venoms; lateral gene transfers among Pox viruses, Wolbachia, and Nasonia; and the rapid evolution of genes involved in nuclear-mitochondrial interactions that are implicated in speciation. Newly developed genome resources advance Nasonia for genetic research, accelerate mapping and cloning of quantitative trait loci, and will ultimately provide tools and knowledge for further increasing the utility of parasitoids as pest insect-control agents.
2009
Wissler, Lothar; Dattolo, E.; Moore, Andrew D.; Reusch, T. B. H.; Olsen, J. L.; Migliaccio, M.; Bornberg-Bauer, Erich; Procaccini, G.
Dr. Zompo: an online data repository for Zostera marina and Posidonia oceanica ESTs Journal Article
In: Database, 2009.
@article{Wissler2009,
title = {Dr. Zompo: an online data repository for Zostera marina and Posidonia oceanica ESTs},
author = {Lothar Wissler and E. Dattolo and Andrew D. Moore and T. B. H. Reusch and J. L. Olsen and M. Migliaccio and Erich Bornberg-Bauer and G. Procaccini},
url = {https://bornberglab.org/wp-content/uploads/2021/04/wissler2009.pdf, Download},
doi = {10.1093/database/bap009},
year = {2009},
date = {2009-08-04},
urldate = {2009-08-04},
journal = {Database},
abstract = {As ecosystem engineers, seagrasses are angiosperms of paramount ecological importance in shallow shoreline habitats around the globe. Furthermore, the ancestors of independent seagrass lineages have secondarily returned into the sea in separate, independent evolutionary events. Thus, understanding the molecular adaptation of this clade not only makes significant contributions to the field of ecology, but also to principles of parallel evolution as well. With the use of Dr. Zompo, the first interactive seagrass sequence database presented here, new insights into the molecular adaptation of marine environments can be inferred. The database is based on a total of 14 597 ESTs obtained from two seagrass species, Zostera marina and Posidonia oceanica, which have been processed, assembled and comprehensively annotated. Dr. Zompo provides experimentalists with a broad foundation to build experiments and consider challenges associated with the investigation of this class of non-domesticated monocotyledon systems. Our database, based on the Ruby on Rails framework, is rich in features including the retrieval of experimentally determined heat-responsive transcripts, mining for molecular markers (SSRs and SNPs), and weighted key word searches that allow access to annotation gathered on several levels including Pfam domains, GeneOntology and KEGG pathways. Well established plant genome sites such as The Arabidopsis Information Resource (TAIR) and the Rice Genome Annotation Project are interfaced by Dr. Zompo. With this project, we have initialized a valuable resource for plant biologists in general and the seagrass community in particular. The database is expected to grow together with more data to come in the near future, particularly with the recent initiation of the Zostera genome sequencing project.
The Dr. Zompo database is available at http://drzompo.uni-muenster.de/},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
As ecosystem engineers, seagrasses are angiosperms of paramount ecological importance in shallow shoreline habitats around the globe. Furthermore, the ancestors of independent seagrass lineages have secondarily returned into the sea in separate, independent evolutionary events. Thus, understanding the molecular adaptation of this clade not only makes significant contributions to the field of ecology, but also to principles of parallel evolution as well. With the use of Dr. Zompo, the first interactive seagrass sequence database presented here, new insights into the molecular adaptation of marine environments can be inferred. The database is based on a total of 14 597 ESTs obtained from two seagrass species, Zostera marina and Posidonia oceanica, which have been processed, assembled and comprehensively annotated. Dr. Zompo provides experimentalists with a broad foundation to build experiments and consider challenges associated with the investigation of this class of non-domesticated monocotyledon systems. Our database, based on the Ruby on Rails framework, is rich in features including the retrieval of experimentally determined heat-responsive transcripts, mining for molecular markers (SSRs and SNPs), and weighted key word searches that allow access to annotation gathered on several levels including Pfam domains, GeneOntology and KEGG pathways. Well established plant genome sites such as The Arabidopsis Information Resource (TAIR) and the Rice Genome Annotation Project are interfaced by Dr. Zompo. With this project, we have initialized a valuable resource for plant biologists in general and the seagrass community in particular. The database is expected to grow together with more data to come in the near future, particularly with the recent initiation of the Zostera genome sequencing project.
The Dr. Zompo database is available at http://drzompo.uni-muenster.de/
The Dr. Zompo database is available at http://drzompo.uni-muenster.de/
2008
Weiner, January; Moore, Andrew D.; Bornberg-Bauer, Erich
Just how versatile are domains? Journal Article
In: BMC Evolutionary Biology, vol. 8, no. 285, pp. 1-14, 2008.
@article{Weiner2008,
title = {Just how versatile are domains?},
author = {January Weiner and Andrew D. Moore and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/weiner2008.pdf, Download},
doi = {10.1186/1471-2148-8-285},
year = {2008},
date = {2008-10-14},
urldate = {2008-10-14},
journal = {BMC Evolutionary Biology},
volume = {8},
number = {285},
pages = {1-14},
abstract = {Background
Creating new protein domain arrangements is a frequent mechanism of evolutionary innovation. While some domains always form the same combinations, others form many different arrangements. This ability, which is often referred to as versatility or promiscuity of domains, its a random evolutionary model in which a domain's promiscuity is based on its relative frequency of domains.
Results
We show that there is a clear relationship across genomes between the promiscuity of a given domain and its frequency. However, the strength of this relationship differs for different domains. We thus redefine domain promiscuity by defining a new index, DV I ("domain versatility index"), which eliminates the effect of domain frequency. We explore links between a domain's versatility, when unlinked from abundance, and its biological properties.
Conclusion
Our results indicate that domains occurring as single domain proteins and domains appearing frequently at protein termini have a higher DV I. This is consistent with previous observations that the evolution of domain re-arrangements is primarily driven by fusion of pre-existing arrangements and single domains as well as loss of domains at protein termini. Furthermore, we studied the link between domain age, defined as the first appearance of a domain in the species tree, and the DV I. Contrary to previous studies based on domain promiscuity, it seems as if the DV I is age independent. Finally, we find that contrary to previously reported findings, versatility is lower in Eukaryotes. In summary, our measure of domain versatility indicates that a random attachment process is sufficient to explain the observed distribution of domain arrangements and that several views on domain promiscuity need to be revised.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
Creating new protein domain arrangements is a frequent mechanism of evolutionary innovation. While some domains always form the same combinations, others form many different arrangements. This ability, which is often referred to as versatility or promiscuity of domains, its a random evolutionary model in which a domain's promiscuity is based on its relative frequency of domains.
Results
We show that there is a clear relationship across genomes between the promiscuity of a given domain and its frequency. However, the strength of this relationship differs for different domains. We thus redefine domain promiscuity by defining a new index, DV I ("domain versatility index"), which eliminates the effect of domain frequency. We explore links between a domain's versatility, when unlinked from abundance, and its biological properties.
Conclusion
Our results indicate that domains occurring as single domain proteins and domains appearing frequently at protein termini have a higher DV I. This is consistent with previous observations that the evolution of domain re-arrangements is primarily driven by fusion of pre-existing arrangements and single domains as well as loss of domains at protein termini. Furthermore, we studied the link between domain age, defined as the first appearance of a domain in the species tree, and the DV I. Contrary to previous studies based on domain promiscuity, it seems as if the DV I is age independent. Finally, we find that contrary to previously reported findings, versatility is lower in Eukaryotes. In summary, our measure of domain versatility indicates that a random attachment process is sufficient to explain the observed distribution of domain arrangements and that several views on domain promiscuity need to be revised.
Creating new protein domain arrangements is a frequent mechanism of evolutionary innovation. While some domains always form the same combinations, others form many different arrangements. This ability, which is often referred to as versatility or promiscuity of domains, its a random evolutionary model in which a domain's promiscuity is based on its relative frequency of domains.
Results
We show that there is a clear relationship across genomes between the promiscuity of a given domain and its frequency. However, the strength of this relationship differs for different domains. We thus redefine domain promiscuity by defining a new index, DV I ("domain versatility index"), which eliminates the effect of domain frequency. We explore links between a domain's versatility, when unlinked from abundance, and its biological properties.
Conclusion
Our results indicate that domains occurring as single domain proteins and domains appearing frequently at protein termini have a higher DV I. This is consistent with previous observations that the evolution of domain re-arrangements is primarily driven by fusion of pre-existing arrangements and single domains as well as loss of domains at protein termini. Furthermore, we studied the link between domain age, defined as the first appearance of a domain in the species tree, and the DV I. Contrary to previous studies based on domain promiscuity, it seems as if the DV I is age independent. Finally, we find that contrary to previously reported findings, versatility is lower in Eukaryotes. In summary, our measure of domain versatility indicates that a random attachment process is sufficient to explain the observed distribution of domain arrangements and that several views on domain promiscuity need to be revised.
Moore, Andrew D.; Björklund, Åsa K.; Ekman, Diana; Bornberg-Bauer, Erich; Elofsson, Arne
Arrangements in the modular evolution of proteins Journal Article
In: Trends in Biomedical Science, vol. 33, no. 9, pp. 444-451, 2008.
@article{Moore2008,
title = {Arrangements in the modular evolution of proteins},
author = {Andrew D. Moore and Åsa K. Björklund and Diana Ekman and Erich Bornberg-Bauer and Arne Elofsson},
url = {https://bornberglab.org/wp-content/uploads/2021/04/moore2008.pdf, Download},
doi = {10.1016/j.tibs.2008.05.008},
year = {2008},
date = {2008-09-01},
journal = {Trends in Biomedical Science},
volume = {33},
number = {9},
pages = {444-451},
abstract = {It has been known for the last couple of decades that proteins evolve partly through rearrangements of larger fragments, typically domains. These units are considered the basic modules of protein structure, evolution and function. In the last few years, the analysis of protein-domain rearrangements has provided us with functional and evolutionary insights and has aided improved functional predictions and domain assignments to previously uncharacterised genes and proteins. Although some mechanisms that govern modular rearrangements of protein domains have been uncovered, such as the addition or deletion of a single N- or C-terminal domain, much is still unknown about the genetics behind these arrangements.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
It has been known for the last couple of decades that proteins evolve partly through rearrangements of larger fragments, typically domains. These units are considered the basic modules of protein structure, evolution and function. In the last few years, the analysis of protein-domain rearrangements has provided us with functional and evolutionary insights and has aided improved functional predictions and domain assignments to previously uncharacterised genes and proteins. Although some mechanisms that govern modular rearrangements of protein domains have been uncovered, such as the addition or deletion of a single N- or C-terminal domain, much is still unknown about the genetics behind these arrangements.
Whitehead, Dion; Wilke, Claus O; Vernazobres, David; Bornberg-Bauer, Erich
The look-ahead effect of phenotypic mutations Journal Article
In: Biology Direct, vol. 3, no. 18, pp. 1-15, 2008.
@article{Whitehead2008,
title = {The look-ahead effect of phenotypic mutations},
author = {Dion Whitehead and Claus O Wilke and David Vernazobres and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/whitehead2008.pdf, Download},
doi = {10.1186/1745-6150-3-18},
year = {2008},
date = {2008-05-14},
urldate = {2008-05-14},
journal = {Biology Direct},
volume = {3},
number = {18},
pages = {1-15},
abstract = {Background
The evolution of complex molecular traits such as disulphide bridges often requires multiple mutations. The intermediate steps in such evolutionary trajectories are likely to be selectively neutral or deleterious. Therefore, large populations and long times may be required to evolve such traits.
Results
We propose that errors in transcription and translation may allow selection for the intermediate mutations, if the final trait provides a large enough selective advantage. We test this hypothesis using a population based model of protein evolution.
Conclusion
If an individual acquires one of two mutations needed for a novel trait, the second mutation can be introduced into the phenotype due to transcription and translation errors. If the novel trait is advantageous enough, the allele with only one mutation will spread through the population, even though the gene sequence does not yet code for the complettrait. Thus, errors allow protein sequences to "look-ahead" for a more direct path to a complex trait.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
The evolution of complex molecular traits such as disulphide bridges often requires multiple mutations. The intermediate steps in such evolutionary trajectories are likely to be selectively neutral or deleterious. Therefore, large populations and long times may be required to evolve such traits.
Results
We propose that errors in transcription and translation may allow selection for the intermediate mutations, if the final trait provides a large enough selective advantage. We test this hypothesis using a population based model of protein evolution.
Conclusion
If an individual acquires one of two mutations needed for a novel trait, the second mutation can be introduced into the phenotype due to transcription and translation errors. If the novel trait is advantageous enough, the allele with only one mutation will spread through the population, even though the gene sequence does not yet code for the complettrait. Thus, errors allow protein sequences to "look-ahead" for a more direct path to a complex trait.
The evolution of complex molecular traits such as disulphide bridges often requires multiple mutations. The intermediate steps in such evolutionary trajectories are likely to be selectively neutral or deleterious. Therefore, large populations and long times may be required to evolve such traits.
Results
We propose that errors in transcription and translation may allow selection for the intermediate mutations, if the final trait provides a large enough selective advantage. We test this hypothesis using a population based model of protein evolution.
Conclusion
If an individual acquires one of two mutations needed for a novel trait, the second mutation can be introduced into the phenotype due to transcription and translation errors. If the novel trait is advantageous enough, the allele with only one mutation will spread through the population, even though the gene sequence does not yet code for the complettrait. Thus, errors allow protein sequences to "look-ahead" for a more direct path to a complex trait.
Schulenburg, Hinrich; Hoeppner, Marc P.; Weiner, January; Bornberg-Bauer, Erich
Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans Journal Article
In: Immunobiology, vol. 213, no. 3-4, pp. 237-250, 2008.
@article{Schulenburg2008,
title = {Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans},
author = {Hinrich Schulenburg and Marc P. Hoeppner and January Weiner and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Schulenburg2008.pdf, Download},
doi = {10.1016/j.imbio.2007.12.004},
year = {2008},
date = {2008-05-14},
journal = {Immunobiology},
volume = {213},
number = {3-4},
pages = {237-250},
abstract = {The nematode Caenorhabditis elegans has become an important model for the study of innate immunity. Its immune system is based on several signaling cascades, including a Toll-like receptor, three mitogen-activated protein kinases (MAPK), one transforming growth factor-β (TGF-β), the insulin-like receptor (ILR), and the programmed cell death (PCD) pathway. Furthermore, it also involves C-type lectin domain- (CTLD) containing proteins as well as several classes of antimicrobial effectors such as lysozymes. Almost all components of the nematode immune system have homologs in other organisms, including humans, and are therefore likely of ancient evolutionary origin. At the same time, most of them are part of a general stress response, suggesting that they only provide unspecific defense. In the current article, we re-evaluate this suggestion and explore the level of specificity in C. elegans innate immunity, i.e. the nematode's ability to mount a distinct defense response towards different pathogens. We draw particular attention to the CTLD proteins, which are abundant in the nematode genome (278 genes) and many of which show a pathogen-specific response during infection. Specificity may also be achieved through the differential activation of antimicrobial genes, distinct functions of the immunity signaling cascades as well as signal integration across pathways. Taken together, our evaluation reveals high potential for immune specificity in C. elegans that may enhance the nematode's ability to fight off pathogens.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The nematode Caenorhabditis elegans has become an important model for the study of innate immunity. Its immune system is based on several signaling cascades, including a Toll-like receptor, three mitogen-activated protein kinases (MAPK), one transforming growth factor-β (TGF-β), the insulin-like receptor (ILR), and the programmed cell death (PCD) pathway. Furthermore, it also involves C-type lectin domain- (CTLD) containing proteins as well as several classes of antimicrobial effectors such as lysozymes. Almost all components of the nematode immune system have homologs in other organisms, including humans, and are therefore likely of ancient evolutionary origin. At the same time, most of them are part of a general stress response, suggesting that they only provide unspecific defense. In the current article, we re-evaluate this suggestion and explore the level of specificity in C. elegans innate immunity, i.e. the nematode's ability to mount a distinct defense response towards different pathogens. We draw particular attention to the CTLD proteins, which are abundant in the nematode genome (278 genes) and many of which show a pathogen-specific response during infection. Specificity may also be achieved through the differential activation of antimicrobial genes, distinct functions of the immunity signaling cascades as well as signal integration across pathways. Taken together, our evaluation reveals high potential for immune specificity in C. elegans that may enhance the nematode's ability to fight off pathogens.
Friedrichs, Frauke; Henckaerts, Liesbet; Vermeire, Severine; Kucharzik, Torsten; Seehafer, Tanja; Möller-Krull, Maren; Bornberg-Bauer, Erich; Stoll, Monika; Weiner, January
The Crohn’s disease susceptibility gene DLG5 as a member of the CARD interaction network Journal Article
In: Journal of Molecular Medicine, vol. 86, pp. 423-432, 2008.
@article{Friedrichs2008,
title = {The Crohn’s disease susceptibility gene DLG5 as a member of the CARD interaction network},
author = {Frauke Friedrichs and Liesbet Henckaerts and Severine Vermeire and Torsten Kucharzik and Tanja Seehafer and Maren Möller-Krull and Erich Bornberg-Bauer and Monika Stoll and January Weiner},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Friedrichs2008.pdf, Download},
doi = {10.1007/s00109-008-0307-5},
year = {2008},
date = {2008-03-12},
journal = {Journal of Molecular Medicine},
volume = {86},
pages = {423-432},
abstract = {Discs large homolog 5 (DLG5), a member of the membrane-associated guanylate kinase (MAGUK) family of scaffolding proteins, has been associated with Crohn’s disease (CD), but its role in the pathogenesis of this inflammatory bowel disease is disputed. Here, we used sequence comparisons and phylogenies to analyse the DLG5 gene and its protein product. We identified a 5′ exon, which codes for an N-terminal caspase recruitment domain (CARD) and experimentally confirmed its expression in colonic tissue. DLG5 shares this new domain with nucleotide-binding oligomerisation domain containing 2 (NOD2); the first CD susceptibility factor identified in genetic studies. An extensive phylogenetic analysis redefines the family organisation of the MAGUK proteins: DLG5 is closely related to CARD10, CARD11 and CARD14, CARD-containing proteins which initiate pro-inflammatory NFκB signalling, but not to DLG1–4, previously considered the closest related proteins. Therefore, we suggest renaming DLG5 to correctly annotate the gene in its phylogenetic and functional context. Our study provides evidence that the scaffolding protein DLG5 belongs to the CARD protein family. Thus, DLG5 likely acts in the regulation of NFkB activation or caspase activation as part of host defence mechanisms. As there is substantial crosstalk between CARD-mediated pathways, both CD susceptibility genes, NOD2 and DLG5, may interact functionally to contribute to CD risk.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Discs large homolog 5 (DLG5), a member of the membrane-associated guanylate kinase (MAGUK) family of scaffolding proteins, has been associated with Crohn’s disease (CD), but its role in the pathogenesis of this inflammatory bowel disease is disputed. Here, we used sequence comparisons and phylogenies to analyse the DLG5 gene and its protein product. We identified a 5′ exon, which codes for an N-terminal caspase recruitment domain (CARD) and experimentally confirmed its expression in colonic tissue. DLG5 shares this new domain with nucleotide-binding oligomerisation domain containing 2 (NOD2); the first CD susceptibility factor identified in genetic studies. An extensive phylogenetic analysis redefines the family organisation of the MAGUK proteins: DLG5 is closely related to CARD10, CARD11 and CARD14, CARD-containing proteins which initiate pro-inflammatory NFκB signalling, but not to DLG1–4, previously considered the closest related proteins. Therefore, we suggest renaming DLG5 to correctly annotate the gene in its phylogenetic and functional context. Our study provides evidence that the scaffolding protein DLG5 belongs to the CARD protein family. Thus, DLG5 likely acts in the regulation of NFkB activation or caspase activation as part of host defence mechanisms. As there is substantial crosstalk between CARD-mediated pathways, both CD susceptibility genes, NOD2 and DLG5, may interact functionally to contribute to CD risk.
Falb, Michaela; Müller, Kerstin; Königsmaier, Lisa; Oberwinkler, Tanja; Horn, Patrick; Gronau, Susanne; Gonzalez, Orland; Pfeiffer, Friedhelm; Bornberg-Bauer, Erich; Oesterhelt, Dieter
Metabolism of halophilic archaea Journal Article
In: Extremophiles, vol. 12, pp. 177–196, 2008.
@article{Falb2008,
title = {Metabolism of halophilic archaea},
author = {Michaela Falb and Kerstin Müller and Lisa Königsmaier and Tanja Oberwinkler and Patrick Horn and Susanne Gronau and Orland Gonzalez and Friedhelm Pfeiffer and Erich Bornberg-Bauer and Dieter Oesterhelt},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Falb2008.pdf, Download},
doi = {10.1007/s00792-008-0138-x},
year = {2008},
date = {2008-02-16},
journal = {Extremophiles},
volume = {12},
pages = {177–196},
abstract = {In spite of their common hypersaline environment, halophilic archaea are surprisingly different in their nutritional demands and metabolic pathways. The metabolic diversity of halophilic archaea was investigated at the genomic level through systematic metabolic reconstruction and comparative analysis of four completely sequenced species: Halobacterium salinarum, Haloarcula marismortui, Haloquadratum walsbyi, and the haloalkaliphile Natronomonas pharaonis. The comparative study reveals different sets of enzyme genes amongst halophilic archaea, e.g. in glycerol degradation, pentose metabolism, and folate synthesis. The carefully assessed metabolic data represent a reliable resource for future system biology approaches as it also links to current experimental data on (halo)archaea from the literature.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
In spite of their common hypersaline environment, halophilic archaea are surprisingly different in their nutritional demands and metabolic pathways. The metabolic diversity of halophilic archaea was investigated at the genomic level through systematic metabolic reconstruction and comparative analysis of four completely sequenced species: Halobacterium salinarum, Haloarcula marismortui, Haloquadratum walsbyi, and the haloalkaliphile Natronomonas pharaonis. The comparative study reveals different sets of enzyme genes amongst halophilic archaea, e.g. in glycerol degradation, pentose metabolism, and folate synthesis. The carefully assessed metabolic data represent a reliable resource for future system biology approaches as it also links to current experimental data on (halo)archaea from the literature.
Reusch, Thorsten B. H.; Veron, Amelie S.; Preuss, Christoph; Weiner, January; Wissler, Lothar; Beck, Alfred; Klages, Sven; Kube, Michael; Reinhardt, Richard; Bornberg-Bauer, Erich
Comparative Analysis of Expressed Sequence Tag (EST) Libraries in the Seagrass Zostera marina Subjected to Temperature Stress Journal Article
In: Marine Biotechnology, vol. 10, pp. 297–309, 2008.
@article{Reusch2008,
title = {Comparative Analysis of Expressed Sequence Tag (EST) Libraries in the Seagrass Zostera marina Subjected to Temperature Stress},
author = {Thorsten B. H. Reusch and Amelie S. Veron and Christoph Preuss and January Weiner and Lothar Wissler and Alfred Beck and Sven Klages and Michael Kube and Richard Reinhardt and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Reusch2008.pdf, Download},
doi = {10.1007/s10126-007-9065-6},
year = {2008},
date = {2008-01-18},
journal = {Marine Biotechnology},
volume = {10},
pages = {297–309},
abstract = {Global warming is associated with increasing stress and mortality on temperate seagrass beds, in particular during periods of high sea surface temperatures during summer months, adding to existing anthropogenic impacts, such as eutrophication and habitat destruction. We compare several expressed sequence tag (EST) in the ecologically important seagrass Zostera marina (eelgrass) to elucidate the molecular genetic basis of adaptation to environmental extremes. We compared the tentative unigene (TUG) frequencies of libraries derived from leaf and meristematic tissue from a control situation with two experimentally imposed temperature stress conditions and found that TUG composition is markedly different among these conditions (all P < 0.0001). Under heat stress, we find that 63 TUGs are differentially expressed (d.e.) at 25°C compared with lower, no-stress condition temperatures (4°C and 17°C). Approximately one-third of d.e. eelgrass genes were characteristic for the stress response of the terrestrial plant model Arabidopsis thaliana. The changes in gene expression suggest complex photosynthetic adjustments among light-harvesting complexes, reaction center subunits of photosystem I and II, and components of the dark reaction. Heat shock encoding proteins and reactive oxygen scavengers also were identified, but their overall frequency was too low to perform statistical tests. In all conditions, the most abundant transcript (3–15%) was a putative metallothionein gene with unknown function. We also find evidence that heat stress may translate to enhanced infection by protists. A total of 210 TUGs contain one or more microsatellites as potential candidates for gene-linked genetic markers. Data are publicly available in a user-friendly database at http://www.uni-muenster.de/Evolution/ebb/Services/zostera.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Global warming is associated with increasing stress and mortality on temperate seagrass beds, in particular during periods of high sea surface temperatures during summer months, adding to existing anthropogenic impacts, such as eutrophication and habitat destruction. We compare several expressed sequence tag (EST) in the ecologically important seagrass Zostera marina (eelgrass) to elucidate the molecular genetic basis of adaptation to environmental extremes. We compared the tentative unigene (TUG) frequencies of libraries derived from leaf and meristematic tissue from a control situation with two experimentally imposed temperature stress conditions and found that TUG composition is markedly different among these conditions (all P < 0.0001). Under heat stress, we find that 63 TUGs are differentially expressed (d.e.) at 25°C compared with lower, no-stress condition temperatures (4°C and 17°C). Approximately one-third of d.e. eelgrass genes were characteristic for the stress response of the terrestrial plant model Arabidopsis thaliana. The changes in gene expression suggest complex photosynthetic adjustments among light-harvesting complexes, reaction center subunits of photosystem I and II, and components of the dark reaction. Heat shock encoding proteins and reactive oxygen scavengers also were identified, but their overall frequency was too low to perform statistical tests. In all conditions, the most abundant transcript (3–15%) was a putative metallothionein gene with unknown function. We also find evidence that heat stress may translate to enhanced infection by protists. A total of 210 TUGs contain one or more microsatellites as potential candidates for gene-linked genetic markers. Data are publicly available in a user-friendly database at http://www.uni-muenster.de/Evolution/ebb/Services/zostera.
2007
Amoutzias, Gregory D.; Pichler, Elgar E; Mian, Nina; Graaf, David De; Imsiridou, Anastasia; Robinson-Rechavi, Marc; Bornberg-Bauer, Erich; Robertson, David L; Oliver, Stephen G
A protein interaction atlas for the nuclear receptors: properties and quality of a hub-based dimerisation network Journal Article
In: BMC Systems Biology, vol. 1, no. 34, pp. 1-12, 2007.
@article{Amoutzias2007,
title = {A protein interaction atlas for the nuclear receptors: properties and quality of a hub-based dimerisation network},
author = {Gregory D. Amoutzias and Elgar E Pichler and Nina Mian and David De Graaf and Anastasia Imsiridou and Marc Robinson-Rechavi and Erich Bornberg-Bauer and David L Robertson and Stephen G Oliver},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Amoutzias2007.pdf, Download},
doi = {10.1186/1752-0509-1-34},
year = {2007},
date = {2007-07-31},
urldate = {2007-07-31},
journal = {BMC Systems Biology},
volume = {1},
number = {34},
pages = {1-12},
abstract = {Background
The nuclear receptors are a large family of eukaryotic transcription factors that constitute major pharmacological targets. They exert their combinatorial control through homotypic heterodimerisation. Elucidation of this dimerisation network is vital in order to understand the complex dynamics and potential cross-talk involved.
Results
Phylogeny, protein-protein interactions, protein-DNA interactions and gene expression data have been integrated to provide a comprehensive and up-to-date description of the topology and properties of the nuclear receptor interaction network in humans. We discriminate between DNA-binding and non-DNA-binding dimers, and provide a comprehensive interaction map, that identifies potential cross-talk between the various pathways of nuclear receptors.
Conclusion
We infer that the topology of this network is hub-based, and much more connected than previously thought. The hub-based topology of the network and the wide tissue expression pattern of NRs create a highly competitive environment for the common heterodimerising partners. Furthermore, a significant number of negative feedback loops is present, with the hub protein SHP [NR0B2] playing a major role. We also compare the evolution, topology and properties of the nuclear receptor network with the hub-based dimerisation network of the bHLH transcription factors in order to identify both unique themes and ubiquitous properties in gene regulation. In terms of methodology, we conclude that such a comprehensive picture can only be assembled by semi-automated text-mining, manual curation and integration of data from various sources.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
The nuclear receptors are a large family of eukaryotic transcription factors that constitute major pharmacological targets. They exert their combinatorial control through homotypic heterodimerisation. Elucidation of this dimerisation network is vital in order to understand the complex dynamics and potential cross-talk involved.
Results
Phylogeny, protein-protein interactions, protein-DNA interactions and gene expression data have been integrated to provide a comprehensive and up-to-date description of the topology and properties of the nuclear receptor interaction network in humans. We discriminate between DNA-binding and non-DNA-binding dimers, and provide a comprehensive interaction map, that identifies potential cross-talk between the various pathways of nuclear receptors.
Conclusion
We infer that the topology of this network is hub-based, and much more connected than previously thought. The hub-based topology of the network and the wide tissue expression pattern of NRs create a highly competitive environment for the common heterodimerising partners. Furthermore, a significant number of negative feedback loops is present, with the hub protein SHP [NR0B2] playing a major role. We also compare the evolution, topology and properties of the nuclear receptor network with the hub-based dimerisation network of the bHLH transcription factors in order to identify both unique themes and ubiquitous properties in gene regulation. In terms of methodology, we conclude that such a comprehensive picture can only be assembled by semi-automated text-mining, manual curation and integration of data from various sources.
The nuclear receptors are a large family of eukaryotic transcription factors that constitute major pharmacological targets. They exert their combinatorial control through homotypic heterodimerisation. Elucidation of this dimerisation network is vital in order to understand the complex dynamics and potential cross-talk involved.
Results
Phylogeny, protein-protein interactions, protein-DNA interactions and gene expression data have been integrated to provide a comprehensive and up-to-date description of the topology and properties of the nuclear receptor interaction network in humans. We discriminate between DNA-binding and non-DNA-binding dimers, and provide a comprehensive interaction map, that identifies potential cross-talk between the various pathways of nuclear receptors.
Conclusion
We infer that the topology of this network is hub-based, and much more connected than previously thought. The hub-based topology of the network and the wide tissue expression pattern of NRs create a highly competitive environment for the common heterodimerising partners. Furthermore, a significant number of negative feedback loops is present, with the hub protein SHP [NR0B2] playing a major role. We also compare the evolution, topology and properties of the nuclear receptor network with the hub-based dimerisation network of the bHLH transcription factors in order to identify both unique themes and ubiquitous properties in gene regulation. In terms of methodology, we conclude that such a comprehensive picture can only be assembled by semi-automated text-mining, manual curation and integration of data from various sources.
Beaussart, Francois; Weiner, January; Bornberg-Bauer, Erich
Automated Improvement of Domain ANnotations using context analysis of domain arrangements (AIDAN) Journal Article
In: Bioinformatics, vol. 23, no. 14, pp. 1834–1836, 2007.
@article{Beaussart2007,
title = {Automated Improvement of Domain ANnotations using context analysis of domain arrangements (AIDAN)},
author = {Francois Beaussart and January Weiner and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Beaussart2007.pdf, Download},
doi = {10.1093/bioinformatics/btm240},
year = {2007},
date = {2007-07-15},
journal = {Bioinformatics},
volume = {23},
number = {14},
pages = {1834–1836},
abstract = {Motivation: Since protein domains are the units of evolution, databases of domain signatures such as ProDom or Pfam enable both a sensitive and selective sequence analysis. However, manually curated databases have a low coverage and automatically generated ones often miss relationships which have not yet been discovered between domains or cannot display similarities between domains which have drifted apart.
Methods: We present a tool which makes use of the fact that overall domain arrangements are often conserved. AIDAN (Automated Improvement of Domain ANnotations) identifies potential annotation artifacts and domains which have drifted apart. The underlying database supplements ProDom and is interfaced by a graphical tool allowing the localization of single domain deletions or annotations which have been falsely made by the automated procedure.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Motivation: Since protein domains are the units of evolution, databases of domain signatures such as ProDom or Pfam enable both a sensitive and selective sequence analysis. However, manually curated databases have a low coverage and automatically generated ones often miss relationships which have not yet been discovered between domains or cannot display similarities between domains which have drifted apart.
Methods: We present a tool which makes use of the fact that overall domain arrangements are often conserved. AIDAN (Automated Improvement of Domain ANnotations) identifies potential annotation artifacts and domains which have drifted apart. The underlying database supplements ProDom and is interfaced by a graphical tool allowing the localization of single domain deletions or annotations which have been falsely made by the automated procedure.
Methods: We present a tool which makes use of the fact that overall domain arrangements are often conserved. AIDAN (Automated Improvement of Domain ANnotations) identifies potential annotation artifacts and domains which have drifted apart. The underlying database supplements ProDom and is interfaced by a graphical tool allowing the localization of single domain deletions or annotations which have been falsely made by the automated procedure.
Wroe, Richard; Chan, Hue Sun; Bornberg-Bauer, Erich
A structural model of latent evolutionary potentials underlying neutral networks in proteins Journal Article
In: HFSP Journal, vol. 1, no. 1, pp. 79–87, 2007.
@article{Wroe2007,
title = {A structural model of latent evolutionary potentials underlying neutral networks in proteins},
author = {Richard Wroe and Hue Sun Chan and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Wroe2007.pdf, Download},
doi = {10.2976/1.2739116},
year = {2007},
date = {2007-05-21},
journal = {HFSP Journal},
volume = {1},
number = {1},
pages = {79–87},
abstract = {A central question in molecular evolution concerns the nature of phenotypic transitions, in particular, if neutral mutations hamper or somehow facilitate adaptability of proteins to new requirements. Proteins have been found to fluctuate between different structures, with frequencies of structures being proportional to their stability. Therefore, functional promiscuity may correspond to different structures with energies close to the ground state which then represent multiple selectable traits. We here postulate that these near-ground-state structures facilitate smooth transitions between phenotypes. Using a biophysical heteropolymer model with exhaustive mappings of sequences onto structures, we demonstrate that this is indeed possible because of a smooth gradient of stability along which any structural phenotype can be optimized and also because of mutational proximity of similar phenotypes in genotype space. Our model provides a biophysical rationalization of the intriguing, and otherwise puzzling experimental observation that adaptation to new requirements, e.g., latent function of a promiscuous enzyme, can proceed while the “old,” phenotypically dominant function is maintained along a series of seemingly neutral mutations (see accompanying article). Thus pleiotropy may facilitate adaptation of latent traits before gene duplications and increase the effective adaptability of proteins.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
A central question in molecular evolution concerns the nature of phenotypic transitions, in particular, if neutral mutations hamper or somehow facilitate adaptability of proteins to new requirements. Proteins have been found to fluctuate between different structures, with frequencies of structures being proportional to their stability. Therefore, functional promiscuity may correspond to different structures with energies close to the ground state which then represent multiple selectable traits. We here postulate that these near-ground-state structures facilitate smooth transitions between phenotypes. Using a biophysical heteropolymer model with exhaustive mappings of sequences onto structures, we demonstrate that this is indeed possible because of a smooth gradient of stability along which any structural phenotype can be optimized and also because of mutational proximity of similar phenotypes in genotype space. Our model provides a biophysical rationalization of the intriguing, and otherwise puzzling experimental observation that adaptation to new requirements, e.g., latent function of a promiscuous enzyme, can proceed while the “old,” phenotypically dominant function is maintained along a series of seemingly neutral mutations (see accompanying article). Thus pleiotropy may facilitate adaptation of latent traits before gene duplications and increase the effective adaptability of proteins.
Kilian, Joachim; Whitehead, Dion; Horak, Jakub; Wanke, Dierk; Weinl, Stefan; Batistic, Oliver; D’Angelo, Cecilia; Bornberg-Bauer, Erich; Kudla, Jörg; Harter, Klaus
In: The Plant Journal, vol. 50, no. 2, pp. 347-363, 2007.
@article{Kilian2007,
title = {The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV‐B light, drought and cold stress responses},
author = {Joachim Kilian and Dion Whitehead and Jakub Horak and Dierk Wanke and Stefan Weinl and Oliver Batistic and Cecilia D’Angelo and Erich Bornberg-Bauer and Jörg Kudla and Klaus Harter},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Kilian2007.pdf, Download},
doi = {10.1111/j.1365-313X.2007.03052.x},
year = {2007},
date = {2007-03-21},
journal = {The Plant Journal},
volume = {50},
number = {2},
pages = {347-363},
abstract = {The tolerance responses of plants to many abiotic stresses are conjectured to be controlled by complex gene networks. In the frame of the AtGenExpress project a comprehensive Arabidopsis thaliana genome transcript expression study was performed using the Affymetrix ATH1 microarray in order to understand these regulatory networks in detail. In contrast to earlier studies, we subjected, side‐by‐side and in a high‐resolution kinetic series, Arabidopsis plants, of identical genotype grown under identical conditions, to different environmental stresses comprising heat, cold, drought, salt, high osmolarity, UV‐B light and wounding. Furthermore, the harvesting of tissue and RNA isolation were performed in parallel at the same location using identical experimental protocols. Here we describe the technical performance of the experiments. We also present a general overview of environmental abiotic stress‐induced gene expression patterns and the results of a model bioinformatics analysis of gene expression in response to UV‐B light, drought and cold stress. Our results suggest that the initial transcriptional stress reaction of Arabidopsis might comprise a set of core environmental stress response genes which, by adjustment of the energy balance, could have a crucial function in various stress responses. In addition, there are indications that systemic signals generated by the tissue exposed to stress play a major role in the coordination and execution of stress responses. In summary, the information reported provides a prime reference point and source for the subsequent exploitation of this important resource for research into plant abiotic stress.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The tolerance responses of plants to many abiotic stresses are conjectured to be controlled by complex gene networks. In the frame of the AtGenExpress project a comprehensive Arabidopsis thaliana genome transcript expression study was performed using the Affymetrix ATH1 microarray in order to understand these regulatory networks in detail. In contrast to earlier studies, we subjected, side‐by‐side and in a high‐resolution kinetic series, Arabidopsis plants, of identical genotype grown under identical conditions, to different environmental stresses comprising heat, cold, drought, salt, high osmolarity, UV‐B light and wounding. Furthermore, the harvesting of tissue and RNA isolation were performed in parallel at the same location using identical experimental protocols. Here we describe the technical performance of the experiments. We also present a general overview of environmental abiotic stress‐induced gene expression patterns and the results of a model bioinformatics analysis of gene expression in response to UV‐B light, drought and cold stress. Our results suggest that the initial transcriptional stress reaction of Arabidopsis might comprise a set of core environmental stress response genes which, by adjustment of the energy balance, could have a crucial function in various stress responses. In addition, there are indications that systemic signals generated by the tissue exposed to stress play a major role in the coordination and execution of stress responses. In summary, the information reported provides a prime reference point and source for the subsequent exploitation of this important resource for research into plant abiotic stress.
2006
Amoutzias, Gregory D.; Veron, Amelie S.; Weiner, January; Robinson-Rechavi, M; Bornberg-Bauer, Erich; Oliver, SG; Robertson, DL
One Billion Years of bZIP Transcription Factor Evolution: Conservation and Change in Dimerization and DNA-Binding Site Specificity Journal Article
In: Molecular Biology and Evolution, vol. 24, no. 3, pp. 827–835, 2006.
@article{Amoutzias2006b,
title = {One Billion Years of bZIP Transcription Factor Evolution: Conservation and Change in Dimerization and DNA-Binding Site Specificity},
author = {Gregory D. Amoutzias and Amelie S. Veron and January Weiner and M Robinson-Rechavi and Erich Bornberg-Bauer and SG Oliver and DL Robertson},
url = {https://bornberglab.org/wp-content/uploads/2021/10/Amoutzias20062.pdf, Download},
doi = {10.1093/molbev/msl211},
year = {2006},
date = {2006-12-28},
journal = {Molecular Biology and Evolution},
volume = {24},
number = {3},
pages = {827–835},
abstract = {The genomic era has revealed that the large repertoire of observed animal phenotypes is dependent on changes in the expression patterns of a finite number of genes, which are mediated by a plethora of transcription factors (TFs) with distinct specificities. The dimerization of TFs can also increase the complexity of a genetic regulatory network manifold, by combining a small number of monomers into dimers with distinct functions. Therefore, studying the evolution of these dimerizing TFs is vital for understanding how complexity increased during animal evolution. We focus on the second largest family of dimerizing TFs, the basic-region leucine zipper (bZIP), and infer when it expanded and how bZIP DNA-binding and dimerization functions evolved during the major phases of animal evolution. Specifically, we classify the metazoan bZIPs into 19 families and confirm the ancient nature of at least 13 of these families, predating the split of the cnidaria. We observe fixation of a core dimerization network in the last common ancestor of protostomes–deuterostomes. This was followed by an expansion of the number of proteins in the network, but no major dimerization changes in interaction partners, during the emergence of vertebrates. In conclusion, the bZIPs are an excellent model with which to understand how DNA binding and protein interactions of TFs evolved during animal evolution.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The genomic era has revealed that the large repertoire of observed animal phenotypes is dependent on changes in the expression patterns of a finite number of genes, which are mediated by a plethora of transcription factors (TFs) with distinct specificities. The dimerization of TFs can also increase the complexity of a genetic regulatory network manifold, by combining a small number of monomers into dimers with distinct functions. Therefore, studying the evolution of these dimerizing TFs is vital for understanding how complexity increased during animal evolution. We focus on the second largest family of dimerizing TFs, the basic-region leucine zipper (bZIP), and infer when it expanded and how bZIP DNA-binding and dimerization functions evolved during the major phases of animal evolution. Specifically, we classify the metazoan bZIPs into 19 families and confirm the ancient nature of at least 13 of these families, predating the split of the cnidaria. We observe fixation of a core dimerization network in the last common ancestor of protostomes–deuterostomes. This was followed by an expansion of the number of proteins in the network, but no major dimerization changes in interaction partners, during the emergence of vertebrates. In conclusion, the bZIPs are an excellent model with which to understand how DNA binding and protein interactions of TFs evolved during animal evolution.
Veron, Amelie S.; Kaufmann, Kerstin; Bornberg-Bauer, Erich
Evidence of Interaction Network Evolution by Whole-Genome Duplications: A Case Study in MADS-Box Proteins Journal Article
In: Molecular Biology and Evolution, vol. 24, no. 3, pp. 670-678, 2006.
@article{Veron2006,
title = {Evidence of Interaction Network Evolution by Whole-Genome Duplications: A Case Study in MADS-Box Proteins},
author = {Amelie S. Veron and Kerstin Kaufmann and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Veron2006.pdf, Download},
doi = {10.1093/molbev/msl197},
year = {2006},
date = {2006-12-14},
journal = {Molecular Biology and Evolution},
volume = {24},
number = {3},
pages = {670-678},
abstract = {Recent investigations on metazoan transcription factors (TFs) indicate that single-gene duplication events and the gain and loss of protein domains are 2 crucial factors in shaping their protein–protein interaction networks. Plant genomes, on the other hand, have a history of polyploidy and whole-genome duplications (WGDs), and thus, their study helps to understand whether WGDs have also had a significant influence on protein network evolution. Here we investigate the evolution of the interaction network in the well-studied MADS domain MIKC-type proteins, a TF family which plays an important role in both the vegetative and the reproductive phases of plant life. We combine phylogenetic reconstruction, protein domain analysis, and interaction data from different species. We show that, unlike previously analyzed interaction networks, the MIKC-type protein network displays a characteristic topology, with overall high inter-subfamily connectivity, shared interactors between paralogs, and conservation of interaction patterns across species. The evaluation of the number of MIKC-type proteins at key time points throughout the evolution of land plants in the lineage leading to Arabidopsis suggested that most duplicates were retained after each round of WGD. We provide evidence that an initial network, formed by 9–11 homodimerizing proteins interacting with each other, existed in the common ancestor of all seed plants. This basic structure has been conserved after each round of WGD, adding layers of paralogs with similar interaction patterns. We thus present the first model where we can show that a network of eukaryotic TFs has evolved via rounds of WGD. Furthermore, we found that in subfamilies in which the K domain is most diverged, the interactions with other subfamilies have been largely lost. We discuss the possibility that such a high proportion of genes were retained after each WGD because of their capacity to form higher order complexes involving proteins from different subfamilies. The simultaneous duplications allowed for the conservation of the quantitative balance between the constituents and facilitated sub- and neofunctionalization through differential expression of whole units.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Recent investigations on metazoan transcription factors (TFs) indicate that single-gene duplication events and the gain and loss of protein domains are 2 crucial factors in shaping their protein–protein interaction networks. Plant genomes, on the other hand, have a history of polyploidy and whole-genome duplications (WGDs), and thus, their study helps to understand whether WGDs have also had a significant influence on protein network evolution. Here we investigate the evolution of the interaction network in the well-studied MADS domain MIKC-type proteins, a TF family which plays an important role in both the vegetative and the reproductive phases of plant life. We combine phylogenetic reconstruction, protein domain analysis, and interaction data from different species. We show that, unlike previously analyzed interaction networks, the MIKC-type protein network displays a characteristic topology, with overall high inter-subfamily connectivity, shared interactors between paralogs, and conservation of interaction patterns across species. The evaluation of the number of MIKC-type proteins at key time points throughout the evolution of land plants in the lineage leading to Arabidopsis suggested that most duplicates were retained after each round of WGD. We provide evidence that an initial network, formed by 9–11 homodimerizing proteins interacting with each other, existed in the common ancestor of all seed plants. This basic structure has been conserved after each round of WGD, adding layers of paralogs with similar interaction patterns. We thus present the first model where we can show that a network of eukaryotic TFs has evolved via rounds of WGD. Furthermore, we found that in subfamilies in which the K domain is most diverged, the interactions with other subfamilies have been largely lost. We discuss the possibility that such a high proportion of genes were retained after each WGD because of their capacity to form higher order complexes involving proteins from different subfamilies. The simultaneous duplications allowed for the conservation of the quantitative balance between the constituents and facilitated sub- and neofunctionalization through differential expression of whole units.
Amoutzias, Gregory D.; Bornberg-Bauer, Erich; Oliver, Stephen G; Robertson, David L
Reduction/oxidation-phosphorylation control of DNA binding in the bZIP dimerization network Journal Article
In: BMC Genomics, vol. 7, no. 107, pp. 1-10, 2006.
@article{Amoutzias2006,
title = {Reduction/oxidation-phosphorylation control of DNA binding in the bZIP dimerization network},
author = {Gregory D. Amoutzias and Erich Bornberg-Bauer and Stephen G Oliver and David L Robertson},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Amoutzias2006.pdf, Download},
doi = {10.1186/1471-2164-7-107},
year = {2006},
date = {2006-05-04},
urldate = {2006-05-04},
journal = {BMC Genomics},
volume = {7},
number = {107},
pages = {1-10},
abstract = {Background
bZIPs are transcription factors that are found throughout the eukarya from fungi to flowering plants and mammals. They contain highly conserved basic region (BR) and leucine zipper (LZ) domains and often function as environmental sensors. Specifically, bZIPs frequently have a role in mediating the response to oxidative stress, a crucial environmental signal that needs to be transduced to the gene regulatory network.
Results
Based on sequence comparisons and experimental data on a number of important bZIP transcription factors, we predict which bZIPs are under redox control and which are regulated via protein phosphorylation. By integrating genomic, phylogenetic and functional data from the literature, we then propose a link between oxidative stress and the choice of interaction partners for the bZIP proteins.
Conclusion
This integration permits the bZIP dimerization network to be interpreted in functional terms, especially in the context of the role of bZIP proteins in the response to environmental stress. This analysis demonstrates the importance of abiotic factors in shaping regulatory networks.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background
bZIPs are transcription factors that are found throughout the eukarya from fungi to flowering plants and mammals. They contain highly conserved basic region (BR) and leucine zipper (LZ) domains and often function as environmental sensors. Specifically, bZIPs frequently have a role in mediating the response to oxidative stress, a crucial environmental signal that needs to be transduced to the gene regulatory network.
Results
Based on sequence comparisons and experimental data on a number of important bZIP transcription factors, we predict which bZIPs are under redox control and which are regulated via protein phosphorylation. By integrating genomic, phylogenetic and functional data from the literature, we then propose a link between oxidative stress and the choice of interaction partners for the bZIP proteins.
Conclusion
This integration permits the bZIP dimerization network to be interpreted in functional terms, especially in the context of the role of bZIP proteins in the response to environmental stress. This analysis demonstrates the importance of abiotic factors in shaping regulatory networks.
bZIPs are transcription factors that are found throughout the eukarya from fungi to flowering plants and mammals. They contain highly conserved basic region (BR) and leucine zipper (LZ) domains and often function as environmental sensors. Specifically, bZIPs frequently have a role in mediating the response to oxidative stress, a crucial environmental signal that needs to be transduced to the gene regulatory network.
Results
Based on sequence comparisons and experimental data on a number of important bZIP transcription factors, we predict which bZIPs are under redox control and which are regulated via protein phosphorylation. By integrating genomic, phylogenetic and functional data from the literature, we then propose a link between oxidative stress and the choice of interaction partners for the bZIP proteins.
Conclusion
This integration permits the bZIP dimerization network to be interpreted in functional terms, especially in the context of the role of bZIP proteins in the response to environmental stress. This analysis demonstrates the importance of abiotic factors in shaping regulatory networks.
Weiner, January; Beaussart, Francois; Bornberg-Bauer, Erich
Domain deletions and substitutions in the modular protein evolution Journal Article
In: The FEBS journal, vol. 273, pp. 2037-2047, 2006.
@article{Weiner2006b,
title = {Domain deletions and substitutions in the modular protein evolution},
author = {January Weiner and Francois Beaussart and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/10/weiner20062.pdf, Download},
doi = {10.1111/j.1742-4658.2006.05220.x},
year = {2006},
date = {2006-04-26},
journal = {The FEBS journal},
volume = {273},
pages = {2037-2047},
abstract = {The main mechanisms shaping the modular evolution of proteins are gene duplication, fusion and fission, recombination and loss of fragments. While a large body of research has focused on duplications and fusions, we concentrated, in this study, on how domains are lost. We investigated motif databases and introduced a measure of protein similarity that is based on domain arrangements. Proteins are represented as strings of domains and comparison was based on the classic dynamic alignment scheme. We found that domain losses and duplications were more frequent at the ends of proteins. We showed that losses can be explained by the introduction of start and stop codons which render the terminal domains nonfunctional, such that further shortening, until the whole domain is lost, is not evolutionarily selected against. We demonstrated that domains which also occur as single‐domain proteins are less likely to be lost at the N terminus and in the middle, than at the C terminus. We conclude that fission/fusion events with single‐domain proteins occur mostly at the C terminus. We found that domain substitutions are rare, in particular in the middle of proteins.We also showed that many cases of substitutions or losses result from erroneous annotations, but we were also able to find courses of evolutionary events where domains vanish over time. This is explained by a case study on the bacterial formate dehydrogenases.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The main mechanisms shaping the modular evolution of proteins are gene duplication, fusion and fission, recombination and loss of fragments. While a large body of research has focused on duplications and fusions, we concentrated, in this study, on how domains are lost. We investigated motif databases and introduced a measure of protein similarity that is based on domain arrangements. Proteins are represented as strings of domains and comparison was based on the classic dynamic alignment scheme. We found that domain losses and duplications were more frequent at the ends of proteins. We showed that losses can be explained by the introduction of start and stop codons which render the terminal domains nonfunctional, such that further shortening, until the whole domain is lost, is not evolutionarily selected against. We demonstrated that domains which also occur as single‐domain proteins are less likely to be lost at the N terminus and in the middle, than at the C terminus. We conclude that fission/fusion events with single‐domain proteins occur mostly at the C terminus. We found that domain substitutions are rare, in particular in the middle of proteins.We also showed that many cases of substitutions or losses result from erroneous annotations, but we were also able to find courses of evolutionary events where domains vanish over time. This is explained by a case study on the bacterial formate dehydrogenases.
Weiner, January; Bornberg-Bauer, Erich
Evolution of Circular Permutations in Multidomain Proteins Journal Article
In: Molecular Biology and Evolution, vol. 23, no. 4, pp. 734–743, 2006.
@article{Weiner2006,
title = {Evolution of Circular Permutations in Multidomain Proteins},
author = {January Weiner and Erich Bornberg-Bauer},
url = {https://bornberglab.org/wp-content/uploads/2021/04/weiner2006.pdf, Download},
doi = {10.1093/molbev/msj091},
year = {2006},
date = {2006-01-23},
journal = {Molecular Biology and Evolution},
volume = {23},
number = {4},
pages = {734–743},
abstract = {Modular rearrangements play an important role in protein evolution. Functional modules, often tantamount to structural domains or smaller fragments, are in many cases well conserved but reoccur in a different order and across many protein families. The underlying genetic mechanisms are gene duplication, fusion, and loss of sequence fragments. As a consequence, the sequential order of domains can be inverted, leading to what is known as circularly permutated proteins. Using a recently developed algorithm, we have identified a large number of such rearrangements and analyzed their evolutionary history. We searched for examples which have arisen by one of the three postulated mechanisms: independent fusion/fission, “duplication/deletion,” and plasmid-mediated “cut and paste.” We conclude that all three mechanisms can be observed, with the independent fusion/fission being the most frequent. This can be partly attributed to highly mobile domains. Duplication/deletion has been found in modular proteins such as peptide synthases.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Modular rearrangements play an important role in protein evolution. Functional modules, often tantamount to structural domains or smaller fragments, are in many cases well conserved but reoccur in a different order and across many protein families. The underlying genetic mechanisms are gene duplication, fusion, and loss of sequence fragments. As a consequence, the sequential order of domains can be inverted, leading to what is known as circularly permutated proteins. Using a recently developed algorithm, we have identified a large number of such rearrangements and analyzed their evolutionary history. We searched for examples which have arisen by one of the three postulated mechanisms: independent fusion/fission, “duplication/deletion,” and plasmid-mediated “cut and paste.” We conclude that all three mechanisms can be observed, with the independent fusion/fission being the most frequent. This can be partly attributed to highly mobile domains. Duplication/deletion has been found in modular proteins such as peptide synthases.
Gerke, Mirco; Bornberg-Bauer, Erich; Jiang, Xiaoyi; Fuellen, Georg
Finding Common Protein Interaction Patterns Across Organisms Journal Article
In: Evolutionary Bioinformatics, 2006.
@article{Gerke2006,
title = {Finding Common Protein Interaction Patterns Across Organisms},
author = {Mirco Gerke and Erich Bornberg-Bauer and Xiaoyi Jiang and Georg Fuellen},
url = {https://bornberglab.org/wp-content/uploads/2021/04/Gerke2006.pdf, Download},
year = {2006},
date = {2006-01-01},
journal = {Evolutionary Bioinformatics},
abstract = {Protein interactions are an important resource to obtain an understanding of cell function. Recently, researchers have compared networks of interactions in order to understand network evolution. While current methods first infer homologs and then compare topologies, we here present a method which first searches for interesting topologies and then looks for homologs. PINA (protein interaction network analysis) takes the protein interaction networks of two organisms, scans both networks for subnetworks deemed interesting, and then tries to find orthologs among the interesting subnetworks. The application is very fast because orthology investigations are restricted to subnetworks like hubs and clusters that fulfill certain criteria regarding neighborhood and connectivity. Finally, the hubs or clusters found to be related can be visualized and analyzed according to protein annotation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Protein interactions are an important resource to obtain an understanding of cell function. Recently, researchers have compared networks of interactions in order to understand network evolution. While current methods first infer homologs and then compare topologies, we here present a method which first searches for interesting topologies and then looks for homologs. PINA (protein interaction network analysis) takes the protein interaction networks of two organisms, scans both networks for subnetworks deemed interesting, and then tries to find orthologs among the interesting subnetworks. The application is very fast because orthology investigations are restricted to subnetworks like hubs and clusters that fulfill certain criteria regarding neighborhood and connectivity. Finally, the hubs or clusters found to be related can be visualized and analyzed according to protein annotation.
2005
Teichmann, Sarah A; Bornberg-Bauer, Erich; Luscombe, Nicholas M
Transcriptional networking Journal Article
In: Genome Biology, vol. 6, no. 344, 2005.