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Impact of whole-genome duplications on structural variant evolution in Cochlearia.

ABSTRACT: Polyploidy, the result of whole-genome duplication (WGD), is a major driver of eukaryote evolution. Yet WGDs are hugely disruptive mutations, and we still lack a clear understanding of their fitness consequences. Here, we study whether WGDs result in greater diversity of genomic structural variants (SVs) and how they influence evolutionary dynamics in a plant genus, Cochlearia (Brassicaceae). By using long-read sequencing and a graph-based pangenome, we find both negative and positive interactions between WGDs and SVs. Masking of recessive mutations due to WGDs leads to a progressive accumulation of deleterious SVs across four ploidal levels (from diploids to octoploids), likely reducing the adaptive potential of polyploid populations. However, we also discover putative benefits arising from SV accumulation, as more ploidy-specific SVs harbor signals of local adaptation in polyploids than in diploids. Together, our results suggest that SVs play diverse and contrasting roles in the evolutionary trajectories of young polyploids.

SUBMITTER: Hamala T

PROVIDER: S-EPMC11199601 | biostudies-literature | 2024 Jun

REPOSITORIES: biostudies-literature

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Impact of whole-genome duplications on structural variant evolution in Cochlearia.

Hämälä Tuomas T Moore Christopher C Cowan Laura L Carlile Matthew M Gopaulchan David D Brandrud Marie K MK Birkeland Siri S Loose Matthew M Kolář Filip F Koch Marcus A MA Yant Levi L

Nature communications 20240625 1

Polyploidy, the result of whole-genome duplication (WGD), is a major driver of eukaryote evolution. Yet WGDs are hugely disruptive mutations, and we still lack a clear understanding of their fitness consequences. Here, we study whether WGDs result in greater diversity of genomic structural variants (SVs) and how they influence evolutionary dynamics in a plant genus, Cochlearia (Brassicaceae). By using long-read sequencing and a graph-based pangenome, we find both negative and positive interactio ...[more]

PMID: 38918389

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Project description:The neuronal and neuroendocrine peptides oxytocin (OT) and vasotocin (VT), including vasopressins, have six cognate receptors encoded by six receptor subtype genes in jawed vertebrates. The peptides elicit a broad range of responses that are specifically mediated by the receptor subtypes including neuronal functions regulating behavior and hormonal actions on reproduction and water/electrolyte balance. Previously, we have demonstrated that these six receptor subtype genes, which we designated VTR1A, VTR1B, OTR, VTR2A, VTR2B and VTR2C, arose from a syntenic ancestral gene pair, one VTR1/OTR ancestor and one VTR2 ancestor, through the early vertebrate whole-genome duplications (WGD) called 1R and 2R. This was supported by both phylogenetic and chromosomal conserved synteny data. More recently, other studies have focused on confounding factors, such as the OTR/VTR orthologs in cyclostomes, to question this scenario for the origin of the OTR/VTR gene family; proposing instead less parsimonious interpretations involving only one WGD followed by complex series of chromosomal or segmental duplications. Here, we have updated the phylogeny of the OTR/VTR gene family, including a larger number of vertebrate species, and revisited seven representative neighboring gene families from our previous conserved synteny analyses, adding chromosomal information from newer high-coverage genome assemblies from species that occupy key phylogenetic positions: the polypteriform fish reedfish (Erpetoichthys calabaricus), the cartilaginous fish thorny skate (Amblyraja radiata) and a more recent high-quality assembly of the Western clawed frog (Xenopus tropicalis) genome. Our analyses once again add strong support for four-fold symmetry, i.e., chromosome quadruplication in the same time window as the WGD events early in vertebrate evolution, prior to the jawed vertebrate radiation. Thus, the evolution of the OTR/VTR gene family can be most parsimoniously explained by two WGD events giving rise to the six ancestral genes, followed by differential gene losses of VTR2 genes in different lineages. We also argue for more coherence and clarity in the nomenclature of OT/VT receptors, based on the most parsimonious scenario.

Project description:BackgroundThe vertebrate tetraspanin family has many features which make it suitable for preserving the imprint of ancient sequence evolution and amenable for phylogenomic analysis. So we believe that an in-depth analysis of the tetraspanin evolution not only provides more complete understanding of tetraspanin biology, but offers new insights into the influence of the two rounds of whole genome duplication (2R-WGD) at the origin of vertebrates.ResultsA detailed phylogeny of vertebrate tetraspanins was constructed by using multiple lines of information, including sequence-based phylogenetics, key structural features, intron configuration and genomic synteny. In particular, a total of 38 modern tetraspanin ortholog lineages in bony vertebrates have been identified and subsequently classified into 17 ancestral lineages existing before 2R-WGD. Based on this phylogeny, we found that the ohnolog retention rate of tetraspanins after 2R-WGD was three times as the average (a rate similar to those of transcription factors and protein kinases). This high rate didn't increase the tetrapanin family size, but changed the family composition, possibly by displacing vertebrate-specific gene lineages with the lineages conserved across deuterostomes. We also found that the period from 2R-WGD to recent time is controlled by gene losses. Meanwhile, positive selection has been detected on 80% of the branches right after 2R-WGDs, which declines significantly on both magnitude and extensity on the following speciation branches. Notably, the loss of mammalian RDS2 is accompanied by strong positive selection on mammalian ROM1, possibly due to gene loss-induced compensatory evolution.ConclusionsFirst, different from transcription factors and kinases, high duplicate retention rate after 2R-WGD didn't increase the tetraspanin family size but just reshaped the family composition. Second, the evolution of tetraspanins right after 2R-WGD had been impacted by a massive wave of gene loss and positive selection on coding sequences. Third, the lingering effect of 2R-WGD on tetraspanin gene loss and positive selection might last for 300-400 million years.

Dataset Information

Impact of whole-genome duplications on structural variant evolution in Cochlearia.

Publications

Impact of whole-genome duplications on structural variant evolution in Cochlearia.

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