Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

Abstract

There are two very interesting aspects to the evolution of sex chromosomes: what happens after recombination between these chromosome pairs stops and why suppressed recombination evolves. The former question has been intensively studied in a diversity of organisms, but the latter has been studied largely theoretically. To obtain empirical data, we used codominant genic markers in genetic mapping of the dioecious plant Silene latifolia, together with comparative mapping of S. latifolia sex-linked genes in S. vulgaris (a related hermaphrodite species without sex chromosomes). We mapped 29 S. latifolia fully sex-linked genes (including 21 newly discovered from transcriptome sequencing), plus 6 genes in a recombining pseudo-autosomal region (PAR) whose genetic map length is 25 cM in both male and female meiosis, suggesting that the PAR may contain many genes. Our comparative mapping shows that most fully sex-linked genes in S. latifolia are located on a single S. vulgaris linkage group and were probably inherited from a single autosome of an ancestor. However, unexpectedly, our maps suggest that the S. latifolia PAR region expanded through translocation events. Some genes in these regions still recombine in S. latifolia, but some genes from both addition events are now fully sex-linked. Recombination suppression is therefore still ongoing in S. latifolia, and multiple recombination suppression events have occurred in a timescale of few million years, much shorter than the timescale of formation of the most recent evolutionary strata of mammal and bird sex chromosomes. It is now understood that the large nonrecombining regions of sex chromosomes in mammals have expanded over evolutionary time, forming "evolutionary strata" with differing levels of sequence divergence between X-and Y-gene pairs, from ancient highly diverged regions, to regions in which the genes started diverging much more recently, which are located closest to the pseudo-autosomal region (PAR) on the X chromosome genetic and physical maps (Lahn and Page 1999;Skaletsky et al. 2003;Marais et al. 2008). The more recent evolutionary strata were formed by recombination suppression in regions formed by an addition of autosomal genetic material to the sex chromosomes (Waters et al. 2001), demonstrating that suppressed recombination spread from the ancestral sex chromosomal region into initially recombining regions. The PAR is shared across Eutherian mammals (despite differences in its boundary and the recent addition of a second PAR, PAR2, in humans), which is a physically small remnant of the added region, which is still autosomal in marsupials (Waters et al. 2001).The major current explanation for the evolution of expanded nonrecombining regions of sex chromosomes is

Testing for the Footprint of Sexually Antagonistic Polymorphisms in the Pseudoautosomal Region of a Plant Sex Chromosome Pair

“…In the small fully sex-linked region (3.5 and 8.1 Mb in the X and Y, respectively), MSY genes are diverged from their X homologs, but sequence divergence decays within 80 kb of the border with the PAR (Wang et al 2012); assuming a plausible recombination rate of 5 cM/Mb, this represents 0.4 cM. In S. latifolia, however, we find indications of associations with the MSY, including high diversity, for several PAR genes, all of which recombine with the fully sexlinked region, at least in some families, indicating that the recombination rate for these genes in the population is at least several centimorgans (see Bergero et al 2013). Below, we discuss possible explanations for our findings.…”

“…Alleles of these loci were sequenced from our natural population sample, together with three candidate PAR genes, E559, E523, and E521, which are apparently fully sex linked, based on the diversity survey (see Bergero et al 2013). The PCR conditions in a Finnzymes' Piko cycler with Phire Hot-Start DNA Polymerase (Finnzymes) were as follows: 1 cycle of initial denaturation at 98°for 30 sec, 10 cycles of DNA denaturation at 98°for 5 sec, primer annealing varying from 60 to 70°for 5 sec, and DNA amplification at 72°for 30 sec, 25 cycles at 98°for 5 sec, 60°for 5 sec, 72°f or 60 sec, and finally 1 cycle at 72°for 5 min.…”

“…The genetic results in Bergero et al (2013) show that most of the PAR genes studied are clearly single copy in the S. latifolia genome (section entitled "The S. latifolia X map and the PAR"). For two genes, E241 and E284, however, some results suggested potential paralogues.…”

“…We tested for the presence of loci with SA polymorphism in the plant Silene latifolia, which is dioecious (with separate male and female individuals) and has a pair of highly heteromorphic sex chromosomes, with XY males. Suppressed recombination between much of the Y and X sex chromosomes evolved in several steps, and the results in Bergero et al (2013) show that it is still ongoing in the recombining or pseudoautosomal, regions (PARs) of these chromosomes. We used molecular evolutionary approaches to test for the footprints of SA polymorphisms, based on sequence diversity levels in S. latifolia PAR genes identified by genetic mapping.…”

“…In the accompanying article in this issue (Bergero et al 2013), we mapped several genes to the S. latifolia PAR. The 25-cM genetic map length of the S. latifolia PAR suggests that it probably carries many genes that could potentially undergo SA mutations, and so this species is well suited for testing the SA hypothesis, unlike species whose PARs include very few genes.…”