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The grayling genome reveals selection on gene expression regulation after whole genome duplication

View ORCID ProfileSrinidhi Varadharajan, View ORCID ProfileSimen R. Sandve, Gareth B. Gillard, Ole K. Tørresen, Teshome D. Mulugeta, Torgeir R. Hvidsten, Sigbjørn Lien, Leif Asbjørn Vøllestad, Sissel Jentoft, View ORCID ProfileAlexander J. Nederbragt, View ORCID ProfileKjetill S. Jakobsen
doi: https://doi.org/10.1101/153270
Srinidhi Varadharajan
1Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo NO-0316, Norway
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  • ORCID record for Srinidhi Varadharajan
Simen R. Sandve
2Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås NO-1432, Norway
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  • For correspondence: k.s.jakobsen@ibv.uio.no simen.sandve@nmbu.no
Gareth B. Gillard
3Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås NO-1432, Norway
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Ole K. Tørresen
1Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo NO-0316, Norway
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Teshome D. Mulugeta
2Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås NO-1432, Norway
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Torgeir R. Hvidsten
3Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås NO-1432, Norway
4Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, Sweden
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Sigbjørn Lien
2Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås NO-1432, Norway
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Leif Asbjørn Vøllestad
1Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo NO-0316, Norway
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Sissel Jentoft
1Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo NO-0316, Norway
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Alexander J. Nederbragt
1Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo NO-0316, Norway
5Biomedical Informatics Research Group, Department of Informatics, University of Oslo, Oslo NO-0316, Norway
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Kjetill S. Jakobsen
1Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo NO-0316, Norway
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  • For correspondence: k.s.jakobsen@ibv.uio.no simen.sandve@nmbu.no
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Abstract

Whole genome duplication (WGD) has been a major evolutionary driver of increased genomic complexity in vertebrates. One such event occurred in the salmonid family ~80 million years ago (Ss4R) giving rise to a plethora of structural and regulatory duplicate-driven divergence, making salmonids an exemplary system to investigate the evolutionary consequences of WGD. Here, we present a draft genome assembly of European grayling (Thymallus thymallus) and use this in a comparative framework to study evolution of gene regulation following WGD. Among the Ss4R duplicates identified in European grayling and Atlantic salmon (Salmo salar), one third reflect non-neutral tissue expression evolution, with strong purifying selection, maintained over ~50 million years. Of these, the majority reflect conserved tissue regulation under strong selective constraints related to brain and neural-related functions, as well as higher-order protein-protein interactions. A small subset of the duplicates has evolved tissue regulatory expression divergence in a common ancestor, which have been subsequently conserved in both lineages, suggestive of adaptive divergence following WGD. These candidates for adaptive tissue expression divergence have elevated rates of protein coding- and promoter-sequence evolution and are enriched for immune- and lipid metabolism ontology terms. Lastly, lineage-specific duplicate divergence points towards underlying differences in adaptive pressures on expression regulation in the non-anadromous grayling versus the anadromous Atlantic salmon.

Our findings enhance our understanding of the role of WGD in genome evolution and highlights cases of regulatory divergence of Ss4R duplicates, possibly related to a niche shift in early salmonid evolution.

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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 4.0 International license.
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Posted May 18, 2018.
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The grayling genome reveals selection on gene expression regulation after whole genome duplication
Srinidhi Varadharajan, Simen R. Sandve, Gareth B. Gillard, Ole K. Tørresen, Teshome D. Mulugeta, Torgeir R. Hvidsten, Sigbjørn Lien, Leif Asbjørn Vøllestad, Sissel Jentoft, Alexander J. Nederbragt, Kjetill S. Jakobsen
bioRxiv 153270; doi: https://doi.org/10.1101/153270
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The grayling genome reveals selection on gene expression regulation after whole genome duplication
Srinidhi Varadharajan, Simen R. Sandve, Gareth B. Gillard, Ole K. Tørresen, Teshome D. Mulugeta, Torgeir R. Hvidsten, Sigbjørn Lien, Leif Asbjørn Vøllestad, Sissel Jentoft, Alexander J. Nederbragt, Kjetill S. Jakobsen
bioRxiv 153270; doi: https://doi.org/10.1101/153270

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