A Gradual Process of Recombination Restriction in the Evolutionary History of the Sex Chromosomes in Dioecious Plants

Abstract

To help understand the evolution of suppressed recombination between sex chromosomes, and its consequences for evolution of the sequences of Y-linked genes, we have studied four X-Y gene pairs, including one gene not previously characterized, in plants in a group of closely related dioecious species of Silene which have an X-Y sex-determining system (S. latifolia, S. dioica, and S. diclinis). We used the X-linked copies to build a genetic map of the X chromosomes, with a marker in the pseudoautosomal region (PAR) to orient the map. The map covers a large part of the X chromosomes—at least 50 centimorgans. Except for a recent rearrangement in S. dioica, the gene order is the same in the X chromosomes of all three species. Silent site divergence between the DNA sequences of the X and Y copies of the different genes increases with the genes' distances from the PAR, suggesting progressive restriction of recombination between the X and Y chromosomes. This was confirmed by phylogenetic analyses of the four genes, which also revealed that the least-diverged X-Y pair could have ceased recombining independently in the dioecious species after their split. Analysis of amino acid replacements vs. synonymous changes showed that, with one possible exception, the Y-linked copies appear to be functional in all three species, but there are nevertheless some signs of degenerative processes affecting the genes that have been Y-linked for the longest times. Although the X-Y system evolved quite recently in Silene (less than 10 million years ago) compared to mammals (about 320 million years ago), our results suggest that similar processes have been at work in the evolution of sex chromosomes in plants and mammals, and shed some light on the molecular mechanisms suppressing recombination between X and Y chromosomes.

Silene as a model system in ecology and evolution

“…The oldest stratum includes highly diverged genes that ceased recombining long ago, whereas genes in the youngest stratum are much less diverged (Lahn and Page, 1999). Over the last decade, several S. latifolia sex-linked genes have been identified (for example, Matsunaga et al, 2003;Filatov, 2005b), and they reveal that Silene sex chromosomes also have evolutionary strata with different divergence levels, indicating that recombination between these chromosomes also stopped in a step-wise manner over time (Nicolas et al, 2005;Bergero et al, 2007).…”

Sex determination in dioecious Mercurialis annua and its close diploid and polyploid relatives

“…Most plants with separate sexes, however, appear to possess genetic s.d., with either heteromorphic or homomorphic sex chromosomes (Ming et al, 2011). Species with heteromorphic sex chromosomes include both those with an XY (for example, Cycas revoluta- (Segawa et al, 1971;Hizume et al, 1998); Cannabis sativa- (Sakamoto et al, 1998;Rode et al, 2005;Sakamoto et al, 2005); Silene latifolia- (Correns, 1928;Westergaard, 1958;Filatov, 2005;Nicolas et al, 2005;Marais et al, 2008;Qiu et al, 2013) and S. diclinis- Howell et al, 2009) or ZW s.d. (for example, Gingko biloba- (Lan et al, 2008); S. otitis- (Slancarova et al, 2013)).…”

Chromatin structural changes around satellite repeats on the female sex chromosome in Schistosoma mansoni and their possible role in sex chromosome emergence

“…To prevent the production of infertile individuals, recombination of these loci becomes restricted [3,4]. This crucial step is intensively debated and two mechanisms of action have been proposed: (i) structural changes by translocation or inversion (reviewed in [5]); or (ii) chromatin status changes involving heterochromatization of the heterosexual chromosome [4,6-9]. Heterochromatization of the sex-determining region has been shown in species with primitive or nascent sex chromosomes, such as in papaya or tilapia (reviewed in [10]).…”