Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification
Abstract Background The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification are often temporally separated from WGD. Salmonid fish, whose ances...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2017-06-01
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| Series: | Genome Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13059-017-1241-z |
| _version_ | 1818154111433965568 |
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| author | Fiona M. Robertson Manu Kumar Gundappa Fabian Grammes Torgeir R. Hvidsten Anthony K. Redmond Sigbjørn Lien Samuel A. M. Martin Peter W. H. Holland Simen R. Sandve Daniel J. Macqueen |
| author_facet | Fiona M. Robertson Manu Kumar Gundappa Fabian Grammes Torgeir R. Hvidsten Anthony K. Redmond Sigbjørn Lien Samuel A. M. Martin Peter W. H. Holland Simen R. Sandve Daniel J. Macqueen |
| author_sort | Fiona M. Robertson |
| collection | DOAJ |
| description | Abstract Background The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification are often temporally separated from WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 million years ago, fit such a ‘time-lag’ model of post-WGD radiation, which occurred alongside a major delay in the rediploidization process. Here we propose a model, ‘lineage-specific ohnologue resolution’ (LORe), to address the consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event. Results Using cross-species sequence capture, phylogenomics and genome-wide analyses of ohnologue expression divergence, we demonstrate the major impact of LORe on salmonid evolution. One-quarter of each salmonid genome, harbouring at least 4550 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions >50 million years post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that potentially facilitated salmonid species radiation. We show that LORe ohnologues are enriched for different functions than ‘older’ ohnologues that began diverging in the salmonid ancestor. Conclusions LORe has unappreciated significance as a nested component of post-WGD divergence that impacts the functional properties of genes, whilst providing ohnologues available solely for lineage-specific adaptation. Under LORe, which is predicted following many WGD events, the functional outcomes of WGD need not appear ‘explosively’, but can arise gradually over tens of millions of years, promoting lineage-specific diversification regimes under prevailing ecological pressures. |
| first_indexed | 2024-12-11T14:21:19Z |
| format | Article |
| id | doaj.art-6585d8f30a2d4646bfa8da6866726cd1 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-12-11T14:21:19Z |
| publishDate | 2017-06-01 |
| publisher | BMC |
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| series | Genome Biology |
| spelling | doaj.art-6585d8f30a2d4646bfa8da6866726cd12022-12-22T01:02:53ZengBMCGenome Biology1474-760X2017-06-0118111410.1186/s13059-017-1241-zLineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversificationFiona M. Robertson0Manu Kumar Gundappa1Fabian Grammes2Torgeir R. Hvidsten3Anthony K. Redmond4Sigbjørn Lien5Samuel A. M. Martin6Peter W. H. Holland7Simen R. Sandve8Daniel J. Macqueen9Institute of Biological and Environmental Sciences, University of AberdeenInstitute of Biological and Environmental Sciences, University of AberdeenCentre for Integrative Genetics (CIGENE), Faculty of Biosciences, Norwegian University of Life SciencesDepartment of Chemistry, Biotechnology and Food Science, Norwegian University of Life SciencesInstitute of Biological and Environmental Sciences, University of AberdeenCentre for Integrative Genetics (CIGENE), Faculty of Biosciences, Norwegian University of Life SciencesInstitute of Biological and Environmental Sciences, University of AberdeenDepartment of Zoology, University of OxfordCentre for Integrative Genetics (CIGENE), Faculty of Biosciences, Norwegian University of Life SciencesInstitute of Biological and Environmental Sciences, University of AberdeenAbstract Background The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification are often temporally separated from WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 million years ago, fit such a ‘time-lag’ model of post-WGD radiation, which occurred alongside a major delay in the rediploidization process. Here we propose a model, ‘lineage-specific ohnologue resolution’ (LORe), to address the consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event. Results Using cross-species sequence capture, phylogenomics and genome-wide analyses of ohnologue expression divergence, we demonstrate the major impact of LORe on salmonid evolution. One-quarter of each salmonid genome, harbouring at least 4550 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions >50 million years post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that potentially facilitated salmonid species radiation. We show that LORe ohnologues are enriched for different functions than ‘older’ ohnologues that began diverging in the salmonid ancestor. Conclusions LORe has unappreciated significance as a nested component of post-WGD divergence that impacts the functional properties of genes, whilst providing ohnologues available solely for lineage-specific adaptation. Under LORe, which is predicted following many WGD events, the functional outcomes of WGD need not appear ‘explosively’, but can arise gradually over tens of millions of years, promoting lineage-specific diversification regimes under prevailing ecological pressures.http://link.springer.com/article/10.1186/s13059-017-1241-zWhole genome duplicationRediploidizationSpecies radiationLineage-specific Ohnologue Resolution (LORe)Duplicate genesFunctional divergence |
| spellingShingle | Fiona M. Robertson Manu Kumar Gundappa Fabian Grammes Torgeir R. Hvidsten Anthony K. Redmond Sigbjørn Lien Samuel A. M. Martin Peter W. H. Holland Simen R. Sandve Daniel J. Macqueen Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification Genome Biology Whole genome duplication Rediploidization Species radiation Lineage-specific Ohnologue Resolution (LORe) Duplicate genes Functional divergence |
| title | Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification |
| title_full | Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification |
| title_fullStr | Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification |
| title_full_unstemmed | Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification |
| title_short | Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification |
| title_sort | lineage specific rediploidization is a mechanism to explain time lags between genome duplication and evolutionary diversification |
| topic | Whole genome duplication Rediploidization Species radiation Lineage-specific Ohnologue Resolution (LORe) Duplicate genes Functional divergence |
| url | http://link.springer.com/article/10.1186/s13059-017-1241-z |
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