Abstract
BackgroundGenome duplication has played a pivotal role in the evolution of many eukaryotic lineages, including the vertebrates. A relatively recent vertebrate genome duplication is that in Xenopus laevis, which resulted from the hybridization of two closely related species about 17 million years ago. However, little is known about the consequences of this duplication at the level of the genome, the epigenome, and gene expression.ResultsThe X. laevis genome consists of two subgenomes, referred to as L (long chromosomes) and S (short chromosomes), that originated from distinct diploid progenitors. Of the parental subgenomes, S chromosomes have degraded faster than L chromosomes from the point of genome duplication until the present day. Deletions appear to have the largest effect on pseudogene formation and loss of regulatory regions. Deleted regions are enriched for long DNA repeats and the flanking regions have high alignment scores, suggesting that non-allelic homologous recombination has played a significant role in the loss of DNA. To assess innovations in the X. laevis subgenomes we examined p300-bound enhancer peaks that are unique to one subgenome and absent from X. tropicalis. A large majority of new enhancers comprise transposable elements. Finally, to dissect early and late events following interspecific hybridization, we examined the epigenome and the enhancer landscape in X. tropicalis × X. laevis hybrid embryos. Strikingly, young X. tropicalis DNA transposons are derepressed and recruit p300 in hybrid embryos.ConclusionsThe results show that erosion of X. laevis genes and functional regulatory elements is associated with repeats and non-allelic homologous recombination and furthermore that young repeats have also contributed to the p300-bound regulatory landscape following hybridization and whole-genome duplication.
Highlights
Genome duplication has played a pivotal role in the evolution of many eukaryotic lineages, including the vertebrates
The X. laevis L and S subgenomes show a bias in chromatin state and gene expression To study the evolution of gene regulation in the context of wholegenome duplications (WGD), we generated transcriptomic and epigenomic profiles in X. laevis early gastrula embryos (Nieuwkoop-Faber stage 10.5; Additional file 1)
The anp32e gene is an example of a conserved gene that is expressed from all three genomes, as evidenced by H3K4me3 at the promoter and H3K36me3 and elongating RNA Polymerase II (RNAPII) in the gene body
Summary
Genome duplication has played a pivotal role in the evolution of many eukaryotic lineages, including the vertebrates. A relatively recent vertebrate genome duplication is that in Xenopus laevis, which resulted from the hybridization of two closely related species about 17 million years ago. In Xenopus (African clawed frogs), duplications have occurred on multiple occasions, giving rise to tetraploid, octoploid, and dodecaploid species [7]. One such duplication occurred in the ancestor of the amphibian Xenopus laevis 17 Mya [8]. The allo-tetraploid genome of X. laevis consists of two subgenomes, referred to as L (long chromosomes) and S (short chromosomes), that originated from distinct diploid progenitors [8]. Most of the additional genes that result from WGD events tend to be lost in evolution. One explanation for biased fractionation is the variation in the level of gene expression between the homeologous chromosomes [10], with the lowest expressed gene having the highest probability of being lost because it would contribute less to fitness
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