Codon-usage bias versus gene conversion in the evolution of yeast duplicate genes

Abstract

Many Saccharomyces cerevisiae duplicate genes that were derived from an ancient whole-genome duplication (WGD) unexpectedly show a small synonymous divergence (K(S)), a higher sequence similarity to each other than to orthologues in Saccharomyces bayanus, or slow evolution compared with the orthologue in Kluyveromyces waltii, a non-WGD species. This decelerated evolution was attributed to gene conversion between duplicates. Using approximately 300 WGD gene pairs in four species and their orthologues in non-WGD species, we show that codon-usage bias and protein-sequence conservation are two important causes for decelerated evolution of duplicate genes, whereas gene conversion is effective only in the presence of strong codon-usage bias or protein-sequence conservation. Furthermore, we find that change in mutation pattern or in tDNA copy number changed codon-usage bias and increased the K(S) distance between K. waltii and S. cerevisiae. Intriguingly, some proteins showed fast evolution before the radiation of WGD species but little or no sequence divergence between orthologues and paralogues thereafter, indicating that functional conservation after the radiation may also be responsible for decelerated evolution in duplicates.

Fig. 1.

Effects of gene conversion on tree topology and observed patterns of synonymous distances between orthologous or between paralogous genes. (a) Genes a and α (b and β) are paralogues derived from a gene duplication, and a and b (α and β) are orthologues derived from a speciation event. Blue and red lines indicate the distances between paralogues (a and α) and orthologues, respectively. (b) α was converted by a. (c) α was converted by a, and β was converted by b. (d) α was converted by a, and b was converted by β. Note that gene conversion can reduce the distance between paralogues but tends to increase the distance between syntenic orthologues. (e) K_S between paralogues in S. cerevisiae (distance between a and α) vs. K_S between orthologues (distances between a and b or α and β). Dark blue, S. cerevisiae vs. S. paradoxus; pink, S. cerevisiae vs. S. mikatae; yellow, S. cerevisiae vs. S. bayanus; open arrows indicate the average distances for these species pairs under weak codon-usage bias (K_S = 0.4, 0.8, and 1.3). Circle sizes indicate the CAI values of the genes in S. cerevisiae. The slope line indicates that the distance between paralogues is equal to that between orthologues. The red and green solid arrows indicate gene pairs YGR138C/YPR156C between S. cerevisiae and S. mikatae and YML063W/YLR441C between S. cerevisiae and S. paradoxus, respectively. Genes with incomplete sequences, paralogous pairs with K_S > 3, and orthologous pairs with K_S > 2 are not included in this figure. (f) Neighbor-joining tree (K_S distances) of the WGD gene pair YGR138C/YPR156C in S. cerevisiae (Sc), their orthologues in S. paradoxus (Sp), S. mikatae (Sm), and S. bayanus (Sb), and the outgroups in K. waltii (3) and A. gossypii (11) (the red arrow in 1e, CAI = 0.310/0.261). The orthologue of YGR138C in S. bayanus was not completely sequenced and not included in this figure. (g) YML063W/YLR441C (the green arrow, CAI = 0.769/0.696). The numbers at branch nodes are bootstrap values.

Fig. 2.

Neighbor-joining tree of the whole-genome duplicated ORFs of S. cerevisiae (Sc) and their orthologues in S. paradoxus (Sp), S. mikatae (Sm), and S. bayanus (Sb) and outgroups K. waltii, A. gossypii, and Candida albicans for YER131W (gene 1)/YGL189C (gene 2) (cytoplasmic small ribosomal subunits, CAI = 0.711/0.781). The tree was constructed by using protein Poisson distances. The numbers at branch nodes are bootstrap values.

Fig. 3.

The neighbor-joining tree of tDNA-Glu genes among three yeast species [S. cerevisiae (Sc), K. waltii (Kw), and A. gossypii (Ag)]. The triplet and number in the parentheses indicate, respectively, the tDNA anticodon and the gene copy number in the corresponding genome. The numbers at branch nodes are bootstrap values. This phylogeny suggests that the switch between anticodons occurred at least twice in the evolution of the tDNA-Glu gene in these yeast species.