The evolutionary conundrum of whole‐genome duplication

Carretero‐Paulet, Lorenzo; Peer, Yves Van de

doi:10.1002/ajb2.1520

Cited by 32 publications

(34 citation statements)

References 25 publications

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“…LORe can readily be mistaken for lineage-specific (e.g., tandem) gene duplication during phylogenetic analyses, if global expectations of WGD (i.e., collinearity among ohnolog pairs on distinct chromosomes) are overlooked ( Robertson et al 2017 ). When considering the potential evolutionary impacts of WGD events, LORe was hypothesized to promote lineage-specific adaptation ( Robertson et al 2017 ) and offers a plausible framework to explain frequent observations of time-lags between WGD event and subsequent species or phenotypic diversification regimes ( Schranz et al 2012 ; Clark and Donoghue 2017 ; Carretero‐Paulet and Van de Peer 2020 ). Following the discovery of delayed rediploidization and LORe in salmonids, many authors have realized the possible importance of these processes for WGD events in divergent taxa ( Macqueen and Johnston 2014 ; Martin and Holland 2014 ; Clark and Donoghue 2017 ; Van de Peer et al 2017 ; Rozenfeld et al 2019 ; Carretero‐Paulet and Van de Peer 2020 ).…”

Section: Introductionmentioning

confidence: 99%

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

Gundappa

Grønvold

et al. 2021

Molecular Biology and Evolution

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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 genomewide 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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Section: Introductionmentioning

confidence: 99%

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

Gundappa

Grønvold

et al. 2021

Molecular Biology and Evolution

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“…Genome sequencing explosion has highlighted a profound impact of polyploidy and subsequent post-polyploid diploidization (PPD) on evolutionary innovations and adaptation. As the impact might lead to genomic diversity, variability, and complexity, polyploidy is generally considered to have far-reaching consequences in shaping species speciation, diversification, and ecological adaption (1)(2)(3)(4)(5)(6)(7)(8)(9)(10). The evolutionary fates of duplicated genes are dynamic and complex and include pseudogenization or gene deletion, subfunctionalization, or neofunctionalization under relaxed purifying selection (3).…”

Section: Introductionmentioning

confidence: 99%

Divergent Antiviral Mechanisms of Two Viperin Homeologs in a Recurrent Polyploid Fish

Mou

et al. 2021

Front. Immunol.

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Polyploidy and subsequent diploidization provide genomic opportunities for evolutionary innovations and adaptation. The researches on duplicated gene evolutionary fates in recurrent polyploids have seriously lagged behind that in paleopolyploids with diploidized genomes. Moreover, the antiviral mechanisms of Viperin remain largely unclear in fish. Here, we elaborate the distinct antiviral mechanisms of two viperin homeologs (Cgviperin-A and Cgviperin-B) in auto-allo-hexaploid gibel carp (Carassius gibelio). First, Cgviperin-A and Cgviperin-B showed differential and biased expression patterns in gibel carp adult tissues. Subsequently, using co-immunoprecipitation (Co-IP) screening analysis, both CgViperin-A and CgViperin-B were found to interact with crucian carp (C. auratus) herpesvirus (CaHV) open reading frame 46 right (ORF46R) protein, a negative herpesvirus regulator of host interferon (IFN) production, and to promote the proteasomal degradation of ORF46R via decreasing K63-linked ubiquitination. Additionally, CgViperin-B also mediated ORF46R degradation through autophagosome pathway, which was absent in CgViperin-A. Moreover, we found that the N-terminal α-helix domain was necessary for the localization of CgViperin-A and CgViperin-B at the endoplasmic reticulum (ER), and the C-terminal domain of CgViperin-A and CgViperin-B was indispensable for the interaction with degradation of ORF46R. Therefore, the current findings clarify the divergent antiviral mechanisms of the duplicated viperin homeologs in a recurrent polyploid fish, which will shed light on the evolution of teleost duplicated genes.

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“…Studies in yeasts indicate that plasticity and adaptive nature of regulatory networks allow polyploidy to accelerate evolutionary adaptation to problematic environments [42,90]. Studies with model (digital) organisms showed that adaptation to unstable and stressful conditions is facilitated by WGDs, while fitness in favorable conditions is impaired when WGDs are maintained [89,91]. It is still unclear why WGDs are advantageous in stressful conditions and deleterious in normal conditions.…”

Section: Whole-genome Duplications Improvementioning

confidence: 99%

“…It is still unclear why WGDs are advantageous in stressful conditions and deleterious in normal conditions. One of the hypotheses suggests that random mutations in regulatory network genes are often harmful in a stable environment and that similar changes arising in a stressful environment increase plasticity and pave the way for the radical adaptations that are essential for survival [91].…”

Section: Whole-genome Duplications Improvementioning

confidence: 99%

Whole-Genome Duplications in Evolution, Ontogeny, and Pathology: Complexity and Emergency Reserves

Anatskaya

Vinogradov

2021

Mol Biol

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Whole-genome duplication (WGD), or polyploidy, increases the amount of genetic information in the cell. WGDs of whole organisms are found in all branches of eukaryotes and act as a driving force of speciation, complication, and adaptations. Somatic-cell WGDs are observed in all types of tissues and can result from normal or altered ontogenetic programs, regeneration, pathological conditions, aging, malignancy, and metastasis. Despite the versatility of WGDs, their functional significance, general properties, and causes of their higher adaptive potential are unclear. Comparisons of whole-transcriptome data and information from various fields of molecular biology, genomics, and molecular medicine showed several common features for polyploidy of organisms and somatic and cancer cells, making it possible to understand what WGD properties lead to the emergence of an adaptive phenotype. The adaptation potential of WGDs may be associated with an increase in the complexity of the regulation of networks and signaling systems; a higher resistance to stress; and activation of ancient evolutionary programs of unicellularity and pathways of morphogenesis, survival, and life extension. A balance between the cell and organismal levels in controlling gene regulation may shift in stress towards the priority of cell survival, and the shift can lead to cardiovascular diseases and carcinogenesis. The presented information helps to understand how polyploidy creates new phenotypes and why it acts as a driving force of evolution and an important regulator of biological processes in somatic cells during ontogeny, pathogenesis, regeneration, and transformation.

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The evolutionary conundrum of whole‐genome duplication

Cited by 32 publications

References 25 publications

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

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

Divergent Antiviral Mechanisms of Two Viperin Homeologs in a Recurrent Polyploid Fish

Whole-Genome Duplications in Evolution, Ontogeny, and Pathology: Complexity and Emergency Reserves

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