Evolutionary forces affecting synonymous variations in plant genomes

Abstract

Base composition is highly variable among and within plant genomes, especially at third codon positions, ranging from GC-poor and homogeneous species to GC-rich and highly heterogeneous ones (particularly Monocots). Consequently, synonymous codon usage is biased in most species, even when base composition is relatively homogeneous. The causes of these variations are still under debate, with three main forces being possibly involved: mutational bias, selection and GC-biased gene conversion (gBGC). So far, both selection and gBGC have been detected in some species but how their relative strength varies among and within species remains unclear. Population genetics approaches allow to jointly estimating the intensity of selection, gBGC and mutational bias. We extended a recently developed method and applied it to a large population genomic dataset based on transcriptome sequencing of 11 angiosperm species spread across the phylogeny. We found that at synonymous positions, base composition is far from mutation-drift equilibrium in most genomes and that gBGC is a widespread and stronger process than selection. gBGC could strongly contribute to base composition variation among plant species, implying that it should be taken into account in plant genome analyses, especially for GC-rich ones.PLOS Genetics | https://doi.org/10.1371/journal.pgen

A pseudomolecule‐scale genome assembly of the liverwort Marchantia polymorpha

“…Another common feature of plant genomes is a correlation of recombination rate with GC content. In most plant genomes, recombination rates are positively correlated with GC content but exceptions with negative or no correlation are known, especially in frequent selfers (Marais et al, 2004;Paape et al, 2012;Pessia et al, 2012;Cl ement et al, 2017). The significant relationship between recombination rate and GC content is thought to be maintained by GC-biased gene conversion after cross-overs (Cl ement et al, 2017).…”

“…In most plant genomes, recombination rates are positively correlated with GC content but exceptions with negative or no correlation are known, especially in frequent selfers (Marais et al, 2004;Paape et al, 2012;Pessia et al, 2012;Cl ement et al, 2017). The significant relationship between recombination rate and GC content is thought to be maintained by GC-biased gene conversion after cross-overs (Cl ement et al, 2017). Alternatively, the correlation could also be maintained by selection for higher GC content or by a recombination-inducing effect of GC-rich genomic regions (Liu et al, 2018).…”

Codon usage and codon pair patterns in non-grass monocot genomes

“…Hence, gBGC is considered a neutral process as it does not rely on the fitness effect of alleles of the individuals. For the last 10 years a plethora of evidence has been accumulated for gBGC as a major evolutionary force affecting codon usage and base composition in humans (reviewed by Galtier, 2009, Glémin et al, 2015), yeast (Lesecque et al, 2013) and plants (Muyle et al, 2011;Pessia et al, 2012;Wu et al, 2015;Rodgers-Melnick et al, 2016;Clément et al, 2017).…”

The effects of GC-biased gene conversion on patterns of genetic diversity among and across butterfly genomes

“…The GC content is determined by the relative fixation of S→W and W→S mutations (Sueoka 1962), which is governed by the balance of a mutation bias from S→W over W→S, and a fixation bias from W→S over S→W. The latter may be caused by gBGC only, but may also be observed at synonymous sites due to selection for preferred codons (Duret and Mouchiroud 1999; Clément, et al 2017; Galtier, et al 2018). Protein coding genes make up only 3.7 % of the L. sinapis genome (Talla, Soler, et al 2019) and potential selection on codon usage will hence only affect genome-wide base composition marginally in this species.…”