Rapid evolution of yeast centromeres in the absence of drive

Abstract

To find the most rapidly evolving regions in the yeast genome we compared most of chromosome III from three closely related lineages of the wild yeast Saccharomyces paradoxus. Unexpectedly, the centromere appears to be the fastest-evolving part of the chromosome, evolving even faster than DNA sequences unlikely to be under selective constraint (i.e., synonymous sites after correcting for codon usage bias and remnant transposable elements). Centromeres on other chromosomes also show an elevated rate of nucleotide substitution. Rapid centromere evolution has also been reported for some plants and animals and has been attributed to selection for inclusion in the egg or the ovule at female meiosis. But Saccharomyces yeasts have symmetrical meioses with all four products surviving, thus providing no opportunity for meiotic drive. In addition, yeast centromeres show the high levels of polymorphism expected under a neutral model of molecular evolution. We suggest that yeast centromeres suffer an elevated rate of mutation relative to other chromosomal regions and they change through a process of "centromere drift," not drive.

Figure 1.—

Sliding-window analysis of nucleotide divergence along chromosome III. Each bar represents the pairwise divergence estimated from a 50-bp window, with 10 bp offset, chosen to capture divergence of short elements such as the centromere (red) and transposable element fragments (blue). Other intergenic regions are shown in gold, and genic regions (gray) include protein-coding exons, introns, tRNA, and snoRNA genes. All gaps shown are due to gaps in the alignment rather than zero divergence. For Europe vs. Far East there are 255,186 aligned sites, ∼81% of the complete S. cerevisiae chromosome; for S. paradoxus (Europe) vs. S. cariocanus there are 218,286 aligned sites (69%).

Figure 2.—

Polymorphism among European (circles) and Far East (triangles) strains as a function of divergence for different types of DNA sequence. Note the square-root scale on both axes, used to spread the points.

Figure 3.—

Unrooted phylogram showing that centromeres from the same chromosome cluster together [maximum-parsimony analysis using PAUP v.4b10 (Swofford 1999); note that branch lengths between centromeres from different chromosomes are approximate due to uncertainties in the alignment].

Figure 4.—

Alignment of sequences at CEN3. N indicates missing data. SCA, S. cariocanus; SCE, S. cerevisiae. Also shown is the sequence for centromere 11 from S. cerevisiae, which has been shown to be functionally interchangeable with CEN3 (Clarke and Carbon 1983). For visual clarity three sequences with missing data are not shown.

Figure 5.—

Divergence at synonymous sites as a function of the degree of “unbias” in codon usage, 1 − CAI, where CAI is the codon adaptation index from Hirsh et al. (2005). Lines are regressions forced through the origin, and divergence in the absence of codon usage bias (Table 1) is estimated from the regression line using 1 − CAI = 1. For two genes there were <10 synonymous sites in the alignment of S. paradoxus (Europe) vs. S. cariocanus (due to missing sequence), and these have been omitted from the graph.