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Genome-Wide Reconstruction of Rediploidization Following Autopolyploidization across One Hundred Million Years of Salmonid Evolution

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 (ohnologs) to diverge gen...

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Autores principales: Gundappa, Manu Kumar, To, Thu-Hien, Grønvold, Lars, Martin, Samuel A M, Lien, Sigbjørn, Geist, Juergen, Hazlerigg, David, Sandve, Simen R, Macqueen, Daniel J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8760942/
https://www.ncbi.nlm.nih.gov/pubmed/34718723
http://dx.doi.org/10.1093/molbev/msab310
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author Gundappa, Manu Kumar
To, Thu-Hien
Grønvold, Lars
Martin, Samuel A M
Lien, Sigbjørn
Geist, Juergen
Hazlerigg, David
Sandve, Simen R
Macqueen, Daniel J
author_facet Gundappa, Manu Kumar
To, Thu-Hien
Grønvold, Lars
Martin, Samuel A M
Lien, Sigbjørn
Geist, Juergen
Hazlerigg, David
Sandve, Simen R
Macqueen, Daniel J
author_sort Gundappa, Manu Kumar
collection PubMed
description 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 (ohnologs) 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 ohnolog 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 genome-wide ohnolog 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 Ma). This was followed by a period of relative genomic stasis lasting 17–39 My, where much of the genome remained tetraploid. A second rediploidization wave began in the early Eocene and proceeded alongside species diversification, generating predictable patterns of lineage-specific ohnolog divergence, scaling in complexity with the number of speciation events. Using gene set enrichment, gene expression, and codon-based selection analyses, we provide insights into potential functional outcomes of delayed rediploidization. This study enhances our understanding of delayed autopolyploid rediploidization and has broad implications for future studies of WGD events.
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spelling pubmed-87609422022-01-18 Genome-Wide Reconstruction of Rediploidization Following Autopolyploidization across One Hundred Million Years of Salmonid Evolution Gundappa, Manu Kumar To, Thu-Hien Grønvold, Lars Martin, Samuel A M Lien, Sigbjørn Geist, Juergen Hazlerigg, David Sandve, Simen R Macqueen, Daniel J Mol Biol Evol Discoveries 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 (ohnologs) 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 ohnolog 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 genome-wide ohnolog 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 Ma). This was followed by a period of relative genomic stasis lasting 17–39 My, where much of the genome remained tetraploid. A second rediploidization wave began in the early Eocene and proceeded alongside species diversification, generating predictable patterns of lineage-specific ohnolog divergence, scaling in complexity with the number of speciation events. Using gene set enrichment, gene expression, and codon-based selection analyses, we provide insights into potential functional outcomes of delayed rediploidization. This study enhances our understanding of delayed autopolyploid rediploidization and has broad implications for future studies of WGD events. Oxford University Press 2021-10-28 /pmc/articles/PMC8760942/ /pubmed/34718723 http://dx.doi.org/10.1093/molbev/msab310 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://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 (https://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
Gundappa, Manu Kumar
To, Thu-Hien
Grønvold, Lars
Martin, Samuel A M
Lien, Sigbjørn
Geist, Juergen
Hazlerigg, David
Sandve, Simen R
Macqueen, Daniel J
Genome-Wide Reconstruction of Rediploidization Following Autopolyploidization across One Hundred Million Years of Salmonid Evolution
title Genome-Wide Reconstruction of Rediploidization Following Autopolyploidization across One Hundred Million Years of Salmonid Evolution
title_full Genome-Wide Reconstruction of Rediploidization Following Autopolyploidization across One Hundred Million Years of Salmonid Evolution
title_fullStr Genome-Wide Reconstruction of Rediploidization Following Autopolyploidization across One Hundred Million Years of Salmonid Evolution
title_full_unstemmed Genome-Wide Reconstruction of Rediploidization Following Autopolyploidization across One Hundred Million Years of Salmonid Evolution
title_short Genome-Wide Reconstruction of Rediploidization Following Autopolyploidization across One Hundred Million Years of Salmonid Evolution
title_sort genome-wide reconstruction of rediploidization following autopolyploidization across one hundred million years of salmonid evolution
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8760942/
https://www.ncbi.nlm.nih.gov/pubmed/34718723
http://dx.doi.org/10.1093/molbev/msab310
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