Genomic determinants of protein evolution and polymorphism in Arabidopsis

Abstract

Recent results from Drosophila suggest that positive selection has a substantial impact on genomic patterns of polymorphism and divergence. However, species with smaller population sizes and/or stronger population structure may not be expected to exhibit Drosophila-like patterns of sequence variation. We test this prediction and identify determinants of levels of polymorphism and rates of protein evolution using genomic data from Arabidopsis thaliana and the recently sequenced Arabidopsis lyrata genome. We find that, in contrast to Drosophila, there is no negative relationship between nonsynonymous divergence and silent polymorphism at any spatial scale examined. Instead, synonymous divergence is a major predictor of silent polymorphism, which suggests variation in mutation rate as the main determinant of silent variation. Variation in rates of protein divergence is mainly correlated with gene expression level and breadth, consistent with results for a broad range of taxa, and map-based estimates of recombination rate are only weakly correlated with nonsynonymous divergence. Variation in mutation rates and the strength of purifying selection seem to be major drivers of patterns of polymorphism and divergence in Arabidopsis. Nevertheless, a model allowing for varying negative and positive selection by functional gene category explains the data better than a homogeneous model, implying the action of positive selection on a subset of genes. Genes involved in disease resistance and abiotic stress display high proportions of adaptive substitution. Our results are important for a general understanding of the determinants of rates of protein evolution and the impact of selection on patterns of polymorphism and divergence.

FIG. 1.—

The relationship between nonsynonymous divergence and synonymous polymorphism in Arabidopsis thaliana does not show a signature of recurrent hitchhiking. Levels of synonymous polymorphism—as measured through nucleotide diversity Pi—were corrected for the joint effect of d_S and exon density per window (n = 515 windows of 200 kb are used here) using a linear model. The dotted line denotes the standard least square regression line through the data points, and the continuous line—almost superimposed—denotes a local robust “lowess” regression.

FIG. 2.—

(A) Levels of synonymous divergence, d_N/d_S, recombination rate, and synonymous heterozygosity plotted in 200-kb windows across Arabidopsis thaliana chromosome 1. There is no reduction in synonymous divergence at a previously identified swept region in A. thaliana (indicated by arrow at ∼20 Mb). (B) A close-up of the putatively swept region shows that there is no evidence for a reduction in synonymous divergence (20-kb windows).

FIG. 3.—

The upper panel shows partial correlation coefficients for an analysis aimed at understanding the genomic factors correlated with variation in d_N/d_S, and the lower panel shows results from an analysis of genomic factors correlated with codon bias. Partial correlation coefficients (below diagonal) are color coded according to sign and degree of correlation, and P values (above diagonal) are color coded by significance level. In the lower panel, the upper value in each cell comes from analysis of codon bias in Arabidopsis thaliana, whereas the lower value corresponds to results for Arabidopsis lyrata. FOP is the frequency of optimal codons.