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De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data

New genes can arise through duplication of a pre-existing gene or de novo from non-coding DNA, providing raw material for evolution of new functions in response to a changing environment. A prime example is the independent evolution of antifreeze glycoprotein genes (afgps) in the Arctic codfishes an...

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Autores principales: Baalsrud, Helle Tessand, Tørresen, Ole Kristian, Solbakken, Monica Hongrø, Salzburger, Walter, Hanel, Reinhold, Jakobsen, Kjetill S, Jentoft, Sissel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5850335/
https://www.ncbi.nlm.nih.gov/pubmed/29216381
http://dx.doi.org/10.1093/molbev/msx311
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author Baalsrud, Helle Tessand
Tørresen, Ole Kristian
Solbakken, Monica Hongrø
Salzburger, Walter
Hanel, Reinhold
Jakobsen, Kjetill S
Jentoft, Sissel
author_facet Baalsrud, Helle Tessand
Tørresen, Ole Kristian
Solbakken, Monica Hongrø
Salzburger, Walter
Hanel, Reinhold
Jakobsen, Kjetill S
Jentoft, Sissel
author_sort Baalsrud, Helle Tessand
collection PubMed
description New genes can arise through duplication of a pre-existing gene or de novo from non-coding DNA, providing raw material for evolution of new functions in response to a changing environment. A prime example is the independent evolution of antifreeze glycoprotein genes (afgps) in the Arctic codfishes and Antarctic notothenioids to prevent freezing. However, the highly repetitive nature of these genes complicates studies of their organization. In notothenioids, afgps evolved from an extant gene, yet the evolutionary origin of afgps in codfishes is unknown. Here, we demonstrate that afgps in codfishes have evolved de novo from non-coding DNA 13–18 Ma, coinciding with the cooling of the Northern Hemisphere. Using whole-genome sequence data from several codfishes and notothenioids, we find higher copy number of afgp in species exposed to more severe freezing suggesting a gene dosage effect. Notably, antifreeze function is lost in one lineage of codfishes analogous to the afgp losses in non-Antarctic notothenioids. This indicates that selection can eliminate the antifreeze function when freezing is no longer imminent. In addition, we show that evolution of afgp-assisting antifreeze potentiating protein genes (afpps) in notothenioids coincides with origin and lineage-specific losses of afgp. The origin of afgps in codfishes is one of the first examples of an essential gene born from non-coding DNA in a non-model species. Our study underlines the power of comparative genomics to uncover past molecular signatures of genome evolution, and further highlights the impact of de novo gene origin in response to a changing selection regime.
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spelling pubmed-58503352018-03-23 De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data Baalsrud, Helle Tessand Tørresen, Ole Kristian Solbakken, Monica Hongrø Salzburger, Walter Hanel, Reinhold Jakobsen, Kjetill S Jentoft, Sissel Mol Biol Evol Discoveries New genes can arise through duplication of a pre-existing gene or de novo from non-coding DNA, providing raw material for evolution of new functions in response to a changing environment. A prime example is the independent evolution of antifreeze glycoprotein genes (afgps) in the Arctic codfishes and Antarctic notothenioids to prevent freezing. However, the highly repetitive nature of these genes complicates studies of their organization. In notothenioids, afgps evolved from an extant gene, yet the evolutionary origin of afgps in codfishes is unknown. Here, we demonstrate that afgps in codfishes have evolved de novo from non-coding DNA 13–18 Ma, coinciding with the cooling of the Northern Hemisphere. Using whole-genome sequence data from several codfishes and notothenioids, we find higher copy number of afgp in species exposed to more severe freezing suggesting a gene dosage effect. Notably, antifreeze function is lost in one lineage of codfishes analogous to the afgp losses in non-Antarctic notothenioids. This indicates that selection can eliminate the antifreeze function when freezing is no longer imminent. In addition, we show that evolution of afgp-assisting antifreeze potentiating protein genes (afpps) in notothenioids coincides with origin and lineage-specific losses of afgp. The origin of afgps in codfishes is one of the first examples of an essential gene born from non-coding DNA in a non-model species. Our study underlines the power of comparative genomics to uncover past molecular signatures of genome evolution, and further highlights the impact of de novo gene origin in response to a changing selection regime. Oxford University Press 2018-03 2017-12-05 /pmc/articles/PMC5850335/ /pubmed/29216381 http://dx.doi.org/10.1093/molbev/msx311 Text en © The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Baalsrud, Helle Tessand
Tørresen, Ole Kristian
Solbakken, Monica Hongrø
Salzburger, Walter
Hanel, Reinhold
Jakobsen, Kjetill S
Jentoft, Sissel
De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data
title De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data
title_full De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data
title_fullStr De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data
title_full_unstemmed De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data
title_short De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data
title_sort de novo gene evolution of antifreeze glycoproteins in codfishes revealed by whole genome sequence data
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5850335/
https://www.ncbi.nlm.nih.gov/pubmed/29216381
http://dx.doi.org/10.1093/molbev/msx311
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