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Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification
Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Department of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway.
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2017 (English)In: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 18, 111Article in journal (Refereed) Published
Abstract [en]

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 similar to 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.

Place, publisher, year, edition, pages
BioMed Central, 2017. Vol. 18, 111
Keyword [en]
Whole genome duplication, Rediploidization, Species radiation, Lineage-specific Ohnologue Resolution (LORe), Duplicate genes, Functional divergence, Autotetraploidization, Salmonid fish
National Category
Biochemistry and Molecular Biology Genetics
Identifiers
URN: urn:nbn:se:umu:diva-137380DOI: 10.1186/s13059-017-1241-zISI: 000403239100006OAI: oai:DiVA.org:umu-137380DiVA: diva2:1120650
Available from: 2017-07-06 Created: 2017-07-06 Last updated: 2017-07-06Bibliographically approved

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Hvidsten, Torgeir R.
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Umeå Plant Science Centre (UPSC)Department of Plant Physiology
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