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Comparative regulomics reveals pervasive selection on gene dosage following whole genome duplication

View ORCID ProfileGareth B. Gillard, View ORCID ProfileLars Grønvold, Line L. Røsæg, Matilde Mengkrog Holen, Øystein Monsen, View ORCID ProfileBen F. Koop, View ORCID ProfileEric B. Rondeau, View ORCID ProfileManu Kumar Gundappa, John Mendoza, View ORCID ProfileDaniel J. Macqueen, View ORCID ProfileRori V. Rohlfs, View ORCID ProfileSimen R. Sandve, View ORCID ProfileTorgeir R. Hvidsten
doi: https://doi.org/10.1101/2020.07.20.212316
Gareth B. Gillard
1Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Norway
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Lars Grønvold
2Center for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Norway
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  • ORCID record for Lars Grønvold
Line L. Røsæg
2Center for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Norway
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Matilde Mengkrog Holen
2Center for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Norway
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Øystein Monsen
2Center for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Norway
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Ben F. Koop
3Department of Biology, University of Victoria, Canada
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Eric B. Rondeau
3Department of Biology, University of Victoria, Canada
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Manu Kumar Gundappa
4The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Midlothian, UK
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  • ORCID record for Manu Kumar Gundappa
John Mendoza
5Department of Computer Science, San Francisco State University, USA
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Daniel J. Macqueen
4The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Midlothian, UK
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  • ORCID record for Daniel J. Macqueen
Rori V. Rohlfs
6Department of Biology, San Francisco State University, USA
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Simen R. Sandve
2Center for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Norway
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  • ORCID record for Simen R. Sandve
  • For correspondence: simen.sandve@nmbu.no torgeir.r.hvidsten@nmbu.no
Torgeir R. Hvidsten
1Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Norway
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  • For correspondence: simen.sandve@nmbu.no torgeir.r.hvidsten@nmbu.no
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Abstract

Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80-100 million years ago. We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Although ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards pseudogenization, strong evolutionary constraints have frequently also favoured symmetric shifts in gene dosage of both copies, likely to achieve gene dose reduction while avoiding accumulation of ‘toxic mutations’. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one source of novel binding sites driving tissue-specific gains in expression. Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • GG: gareth.gillard{at}nmbu.no

  • LG: lars.gronvold{at}nmbu.no

  • LR: line.raseg{at}nmbu.no

  • MMH: matilde.holen{at}nmbu.no

  • ØM: oystein.monsen{at}nmbu.no

  • BK: bkoop{at}uvic.ca

  • EBR: erondeau{at}uvic.ca

  • MKG: manu.gundappa{at}roslin.ed.ac.uk

  • JM: jmendo.1024{at}gmail.com

  • DJM: daniel.macqueen{at}roslin.ed.ac.uk

  • RR: rrohlfs{at}sfsu.edu

  • SRS: simen.sandve{at}nmbu.no

  • TRH: torgeir.r.hvidsten{at}nmbu.no

  • https://gitlab.com/sandve-lab/gillard-groenvold

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted August 27, 2020.
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Comparative regulomics reveals pervasive selection on gene dosage following whole genome duplication
Gareth B. Gillard, Lars Grønvold, Line L. Røsæg, Matilde Mengkrog Holen, Øystein Monsen, Ben F. Koop, Eric B. Rondeau, Manu Kumar Gundappa, John Mendoza, Daniel J. Macqueen, Rori V. Rohlfs, Simen R. Sandve, Torgeir R. Hvidsten
bioRxiv 2020.07.20.212316; doi: https://doi.org/10.1101/2020.07.20.212316
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Comparative regulomics reveals pervasive selection on gene dosage following whole genome duplication
Gareth B. Gillard, Lars Grønvold, Line L. Røsæg, Matilde Mengkrog Holen, Øystein Monsen, Ben F. Koop, Eric B. Rondeau, Manu Kumar Gundappa, John Mendoza, Daniel J. Macqueen, Rori V. Rohlfs, Simen R. Sandve, Torgeir R. Hvidsten
bioRxiv 2020.07.20.212316; doi: https://doi.org/10.1101/2020.07.20.212316

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