Evolution of Young Sex Chromosomes in Two Dioecious Sister Plant Species with Distinct Sex Determination Systems

Abstract

In the last decade, progress has been made in methods to identify the sex determination system in plants. This gives the opportunity to study sex chromosomes that arose independently at different phylogenetic scales, and thus allows the discovery and the understanding of early stages of sex chromosome evolution. In the genus Silene, sex chromosomes have evolved independently in at least two clades from a nondioecious ancestor, the Melandrium and Otites sections. In the latter, sex chromosomes could be younger than in the section Melandrium, based on phylogenetic studies and as no heteromorphic sex chromosomes have been detected. This section might also exhibit lability in sex determination, because male heterogamy and female heterogamy have been suggested to occur.In this study, we investigated the sex determination system of two dioecious species in the section Otites (Silene otites and its close relative Silene pseudotites). Applying the new probabilistic method SEX-DETector on RNA-seq data from cross-controlled progenies, we inferred their most likely sex determination system and a list of putative autosomal and sex-linked contigs. We showed that the two phylogenetically close species differed in their sex determination system (XY versus ZW) with sex chromosomes that derived from two different pairs of autosomes. We built a genetic map of the sex chromosomes and showed that both pairs exhibited a large region with lack of recombination. However, the sex-limited chromosomes exhibited no strong degeneration. Finally, using the "ancestral" autosomal expression of sex-linked orthologs of nondioecious S. nutans, we found a slight signature of dosage compensation in the heterogametic females of S. otites.

Fig. 1.

—Genetic map of (a, b) Silene pseudotites and (c, d) Silene otites. (a, c) Contigs with chromosomal category inferred by SEX-DETector were mapped on the genetic map of Silene latifolia (Papadopulos et al. 2015): contigs inferred as autosomal are in gray, contigs inferred as sex linked and among which some were confirmed using a genetic map are in orange and in S. otites, contigs inferred as XY linked but subsequently found to be associated with a male-specific lethal locus (Msl1) are in blue. (b, d) Comparative genetic mapping of LG6 from S. pseudotites and LG1 and LG3 from S. otites. Chromosomal regions containing loci in complete linkage with sex are indicated by an orange star. Loci mapped on LG1 are represented by a circle and the colors indicate distorted segregation in S. otites males: The gradient color goes from white (40% of males are homozygous, i.e., close to 1:1 segregation as expected), to blue (up to 80% of males are heterozygous, i.e., there is segregation distorsion).

Fig. 2.

—Correlation between the expression of X (or Z) and Y (or W) in the heterogametic sex for (a) S. pseudotites and (b) S. otites. Xm = male X allele expression, Ym = male Y allele expression, Zf = female Z allele expression, Wf = female W allele expression, and AAnut = genotype expression of orthologs in the nondioecious S. nutans that do not have sex chromosomes (therefore, orthologs are on autosomes). Diagonal lines across the plot show no change in expression.