Substitution Rates in the X- and Y-Linked Genes of the Plants, Silene latifolia and S. dioica

Abstract

Theory predicts that selection should be less effective in the nonrecombining genes of Y-chromosomes, relative to the situation for genes on the other chromosomes, and this should lead to the accumulation of deleterious nonsynonymous substitutions. In addition, synonymous substitution rates may differ between X- and Y-linked genes because of the male-driven evolution effect and also because of actual differences in per-replication mutation rates between the sex chromosomes. Here, we report the first study of synonymous and nonsynonymous substitution rates on plant sex chromosomes. We sequenced two pairs of sex-linked genes, SlX1-SlY1 and SlX4-SlY4, from dioecious Silene latifolia and S. dioica, and their non-sex-linked homologues from nondioecious S. vulgaris and Lychnis flos-jovis, respectively. The rate of nonsynonymous substitutions in the SlY4 gene is significantly higher than that in the SlX4 gene. Silent substitution rates are also significantly higher in both Y-linked genes, compared with their X-linked homologues. The higher nonsynonymous substitution rate in the SlY4 gene is therefore likely to be caused by a mutation rate difference between the sex chromosomes. The difference in silent substitution rates between the SlX4 and SlY4 genes is too great to be explained solely by a higher per-generation mutation rate in males than females. It is thus probably caused by a difference in per-replication mutation rates between the sex chromosomes. This suggests that the local mutation rate can change in a relatively short evolutionary time.

Steps in the evolution of heteromorphic sex chromosomes

“…Their ages can be estimated, subject to the uncertainty of molecular clock dating, if reliably alignable sequence data (from coding sequences) are available to estimate X-Y divergence. To compare patterns of X and Y sequence divergence, including testing whether the X and Y mutation rates differ (Li and Makova, 2002), and to understand the history of chromosome rearrangements, data from outgroup species with orthologous sequences are also needed (Filatov and Charlesworth, 2002).…”

Nucleotide diversity inSilene latifoliaautosomal and sex-linked genes

“…The data so far collected cannot distinguish whether the difference is due to the predicted reduction in Y N e , or to some process increasing high species-wide diversity for X-linked genes. Possibilities include a higher X than Y mutation rate (although this is the opposite of the expectation for any difference between the mutation rates of the two chromosomes, and the data so far available support that expectation, see Filatov & Charlesworth 2002;Filatov 2005), sexual selection causing a high variance in male reproductive success (Laporte & Charlesworth 2002) or introgression of sequences from another species; hybridization is well known to occur between S. latifolia and S. dioica (Baker 1948;Minder & Widmer 2007) and seems to have led to sequences within each species having recombined into X-linked genes of the other (Atanassov et al 2001;Laporte et al 2005). Population size changes also affect the relative diversity levels of genome regions with different N e (Fay & Wu 1999;Pool & Nielsen 2007).…”

Recent Spread of a Retrotransposon in theSilene latifoliaGenome, Apart From the Y Chromosome

“…One of the most interesting features of this species is the presence of sex chromosomes that determine whether the plant develops as a male with XY chromosomes or a female with XX sex chromosomes (Westergaard 1958). The sex chromosomes in Silene evolved relatively recently, probably $10 7 years ago (Filatov and Charlesworth 2002) within a small cluster of dioecious Silene species, (section Elisanthe), while the rest of the genus is mostly nondioecious. S. latifolia sex chromosomes apparently evolved from a single pair of autosomes that ceased recombining with each other along most of their length and began to diverge (Filatov 2005a).…”

“…On the other hand, there is no signal on S. vulgaris chromosomes (Figure 1e), suggesting that SlOgre1 is not present in multiple copies in S. vulgaris. Alternatively, the lack of FISH signal in S. vulgaris could be due to divergence between the S. latifolia and S. vulgaris sequences ($15% for silent sites, see Filatov and Charlesworth 2002), precluding effective in situ hybridization. However, the low divergence between the copies of the element present within S. latifolia (see below) suggests that SlOgre1 started to actively transpose quite recently in S. latifolia and its relatives (or their ancestor), providing additional support to the view that this TE has not been widespread in the S. vulgaris genome.…”