Abstract

BackgroundWhole-genome duplication (WGD) events have shaped the genomes of eukaryotic organisms. Relaxed selection after duplication along with inherent functional constraints are thought to determine the fate of the paralogs and, ultimately, the evolution of gene function. Here, we investigated the rate of protein evolution (as measured by dN/dS ratios) before and after the WGD in the hemiascomycete yeasts, and the way in which changes in such rates relate to molecular and biological function.ResultsFor most groups of orthologous genes (81%) we observed a change in the rates of evolution after genome duplication. Genes with atypically-low dN/dS ratio before the WGD were prone to increase their rates of evolution after duplication. Importantly, the paralogs were often different in their rates of evolution after the WGD (50% cases), however, this was more consistent with an asymmetric deceleration in the protein-evolution rates, rather than an asymmetric increase of the initial rates. Functional-category analysis showed that regulatory proteins such as protein kinases and transcription factors were enriched in genes that increase their rates of evolution after the WGD. While changes in the rate of protein-sequence evolution were associated to protein abundance, content of disordered regions, and contribution to fitness, these features were an attribute of specific functional classes.ConclusionsOur results indicate that strong purifying selection in ancestral pre-duplication sequences is a strong predictor of increased rates after the duplication in yeasts and that asymmetry in evolution rate is established during the deceleration phase. In addition, changes in the rates at which paralogous sequences evolve before and after WGD are different for specific protein functions; increased rates of protein evolution after duplication occur preferentially in specific protein functions.

Highlights

  • Whole-genome duplication (WGD) events have shaped the genomes of eukaryotic organisms

  • Ancestral proteins evolving at very slow rates undergo relaxation of purifying selection after the WGD The classic model of evolution by gene duplication suggests that the co-occurrence of two paralogs that can compensate for each other's mutations leads to increased rates in sequence divergence after duplication [33, 34]

  • We asked to what extent this scenario is consistent with the dN/dS ratios estimated for phylogenetic lineages that diverged before or after the WGD in the hemiascomycetes

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Summary

Introduction

Whole-genome duplication (WGD) events have shaped the genomes of eukaryotic organisms. Analyses of genomic sequences indicate that wholegenome duplication (WGD) events have had strong influence in the genomes and evolution of several eukaryotic lineages of vertebrates [1], flowering plants [2], and fungi [3, 4]. The budding yeast Saccharomyces cerevisiae evolved from an ancestor which underwent a WGD event, dated ~100 mya [3, 4]. This genome duplication in the Ascencio et al BMC Evolutionary Biology (2017) 17:40 hemiascomycete yeasts is perhaps the best documented event of its kind. It has been suggested that gene duplication improved the glycolytic flux in S. cerevisiae, which may have led to the colonization of high-sugar content ecological niches [15, 16]

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