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Genome-wide reconstruction of rediploidization following autopolyploidization across one hundred million years of salmonid evolution

View ORCID ProfileManu Kumar Gundappa, Thu-Hien To, View ORCID ProfileLars Grønvold, Samuel A.M. Martin, Sigbjørn Lien, Juergen Geist, David Hazlerigg, View ORCID ProfileSimen R. Sandve, View ORCID ProfileDaniel J. Macqueen
doi: https://doi.org/10.1101/2021.06.05.447185
Manu Kumar Gundappa
1The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Midlothian, EH25 9RG, UK
2School of Biological Sciences, University of Aberdeen, AB24 2TZ, United Kingdom
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Thu-Hien To
3Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, PO Box 5003, Ås, Norway
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Lars Grønvold
3Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, PO Box 5003, Ås, Norway
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Samuel A.M. Martin
2School of Biological Sciences, University of Aberdeen, AB24 2TZ, United Kingdom
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Sigbjørn Lien
3Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, PO Box 5003, Ås, Norway
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Juergen Geist
4Aquatic Systems Biology Unit, TUM School of Life Sciences, Technical University of Munich, Mühlenweg 22, D-85354 Freising, Germany
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David Hazlerigg
5Department of Arctic and Marine Biology, Faculty of BioSciences Fisheries & Economy, University of Tromsø, Norway
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Simen R. Sandve
3Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, PO Box 5003, Ås, Norway
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Daniel J. Macqueen
1The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Midlothian, EH25 9RG, UK
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  • For correspondence: daniel.macqueen@roslin.ed.ac.uk
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Abstract

The long-term evolutionary impacts of whole genome duplication (WGD) are strongly influenced by the ensuing rediploidization process. Following autopolyploidization, rediploidization involves a transition from tetraploid to diploid meiotic pairing, allowing duplicated genes (ohnologues) to diverge genetically and functionally. Our understanding of autopolyploid rediploidization has been informed by a WGD event ancestral to salmonid fishes, where large genomic regions are characterized by temporally delayed rediploidization, allowing lineage-specific ohnologue sequence divergence in the major salmonid clades. Here, we investigate the long-term outcomes of autopolyploid rediploidization at genome-wide resolution, exploiting a recent ‘explosion’ of salmonid genome assemblies, including a new genome sequence for the huchen (Hucho hucho). We developed a genome alignment approach to capture duplicated regions across multiple species, allowing us to create 121,864 phylogenetic trees describing ohnologue divergence across salmonid evolution. Using molecular clock analysis, we show that 61% of the ancestral salmonid genome experienced an initial ‘wave’ of rediploidization in the late Cretaceous (85-106 Mya). This was followed by a period of relative genomic stasis lasting 17-39 My, where much of the genome remained in a tetraploid state. A second rediploidization wave began in the early Eocene and proceeded alongside species diversification, generating predictable patterns of lineage-specific ohnologue divergence, scaling in complexity with the number of speciation events. Finally, using gene set enrichment, gene expression, and codon-based selection analyses, we provide insights into potential functional outcomes of delayed rediploidization. Overall, this study enhances our understanding of delayed autopolyploid rediploidization and has broad implications for future studies of WGD events.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://figshare.com/s/b30a7c7a579392320085

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-NC-ND 4.0 International license.
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Genome-wide reconstruction of rediploidization following autopolyploidization across one hundred million years of salmonid evolution
Manu Kumar Gundappa, Thu-Hien To, Lars Grønvold, Samuel A.M. Martin, Sigbjørn Lien, Juergen Geist, David Hazlerigg, Simen R. Sandve, Daniel J. Macqueen
bioRxiv 2021.06.05.447185; doi: https://doi.org/10.1101/2021.06.05.447185
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Genome-wide reconstruction of rediploidization following autopolyploidization across one hundred million years of salmonid evolution
Manu Kumar Gundappa, Thu-Hien To, Lars Grønvold, Samuel A.M. Martin, Sigbjørn Lien, Juergen Geist, David Hazlerigg, Simen R. Sandve, Daniel J. Macqueen
bioRxiv 2021.06.05.447185; doi: https://doi.org/10.1101/2021.06.05.447185

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