Duplicate gene evolution and expression in the wake of vertebrate allopolyploidization

Abstract

BackgroundThe mechanism by which duplicate genes originate – whether by duplication of a whole genome or of a genomic segment – influences their genetic fates. To study events that trigger duplicate gene persistence after whole genome duplication in vertebrates, we have analyzed molecular evolution and expression of hundreds of persistent duplicate gene pairs in allopolyploid clawed frogs (Xenopus and Silurana). We collected comparative data that allowed us to tease apart the molecular events that occurred soon after duplication from those that occurred later on. We also quantified expression profile divergence of hundreds of paralogs during development and in different tissues.ResultsOur analyses indicate that persistent duplicates generated by allopolyploidization are subjected to strong purifying selection soon after duplication. The level of purifying selection is relaxed compared to a singleton ortholog, but not significantly variable over a period spanning about 40 million years. Despite persistent functional constraints, however, analysis of paralogous expression profiles indicates that quantitative aspects of their expression diverged substantially during this period.ConclusionThese results offer clues into how vertebrate transcriptomes are sculpted in the wake of whole genome duplication (WGD), such as those that occurred in our early ancestors. That functional constraints were relaxed relative to a singleton ortholog but not significantly different in the early compared to the later stage of duplicate gene evolution suggests that the timescale for a return to pre-duplication levels is drawn out over tens of millions of years – beyond the age of these tetraploid species. Quantitative expression divergence can occur soon after WGD and with a magnitude that is not correlated with the rate of protein sequence divergence. On a coarse scale, quantitative expression divergence appears to be more prevalent than spatial and temporal expression divergence, and also faster or more frequent than other processes that operate at the protein level, such as some types of neofunctionalization.

Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis

“…We find that the majority of duplicate pairs do not show much divergence in expression since WGD (median correlation rho ϭ 0.64; Fig. S4), a result similar to that of Chain et al (22).…”

“…Many studies have shown expression divergence between WGD-duplicates (17)(18)(19)(20)(21)(22). However, a major obstacle encountered in all these studies is that they could not differentiate between sub and neofunctionalization because the pattern of expression before duplication was unknown.…”

Sex-Biased Expression of Young Genes in <b><i>Silurana (Xenopus) tropicalis</i></b>

“…Duplicated genes may be especially prone to develop sex-biased expression [Connallon and Clark, 2011;Parsch and Ellegren, 2013] and have been found to be in particularly high proportions among male-biased genes in other species [Cutter and Ward, 2005;Gnad and Parsch, 2006]. After duplication, genes often display rapid evolution and expression divergence as shown in clawed frogs [Hellsten et al, 2007;Chain et al, 2008b;Sémon and Wolfe, 2008] and thus possibly contribute to the characteristic patterns observed with sex-biased genes. In this study, both lineage-specific and duplicated genes, particularly recently duplicated genes, were enriched in sex-biased genes, displaying high expression divergence between the sexes and between gonads.…”

Chromosome Banding in Amphibia. XXXII. The Genus Xenopus (Anura, Pipidae)

“…Two decades later, this species was referred to as S . new tetraploid 1 by Evans et al [2004], and this designation has been used in a number of subsequent publications [Evans et al, 2005[Evans et al, , 2011Evans, 2007;Chain et al, 2008;Bewick et al, 2010]. In the meantime, there are nearly 30 nucleotide sequences deposited in GenBank as Xenopus new tetraploid 1 (GenBank taxon ID: 451443).…”