Heterochiasmy and Sex Chromosome Evolution in Silene

Abstract

The evolution of a non-recombining sex-specific region is a key step in sex chromosome evolution. Suppression of recombination between the (proto-) X- and Y-chromosomes in male meiosis creates a non-recombining Y-linked region (NRY), while the X-chromosome continues to recombine in females. Lack of recombination in the NRY defines its main properties-genetic degeneration and accumulation of repetitive DNA, making X and Y chromosomes very different from each other. How and why recombination suppression on sex chromosomes evolves remains controversial. A strong difference in recombination rates between the sexes (heterochiasmy) can facilitate or even cause recombination suppression. In the extreme case-complete lack of recombination in the heterogametic sex (achiasmy)-the entire sex-specific chromosome is automatically non-recombining. In this study, I analyse sex-specific recombination rates in a dioecious plant Silene latifolia (Caryophyllaceae), which evolved separate sexes and sex chromosomes ~11 million years ago. I reconstruct high-density RNAseq-based genetic maps including over five thousand genic markers for the two sexes separately. The comparison of the male and female maps reveals only modest heterochiasmy across the genome, with the exception of the sex chromosomes, where recombination is suppressed in males. This indicates that heterochiasmy likely played only a minor, if any, role in NRY evolution in S. latifolia, as recombination suppression is specific to NRY rather than to the entire genome in males. Other mechanisms such as structural rearrangements and/or epigenetic modifications were likely involved, and comparative genome analysis and genetic mapping in multiple Silene species will help to shed light on the mechanism(s) of recombination suppression that led to the evolution of sex chromosomes.

Keywords: Silene latifolia; genetic mapping; heterochiasmy; sex chromosome evolution.

Figure 1

Comparison of genetic maps for the X-chromosome of S. latifolia. (A) Sex-average map showing only the markers shared with the female map constructed in this study (B). (C) Male genetic map. The genetic distances are shown for each position (in cM), rounded to integer values in (A). The numbers of genes sharing the same or very similar position are shown in brackets. The genetic positions sharing genic markers in different maps are connected by dotted lines. The locations of the pseudoautosomal region (PAR), the non-recombining Y-linked region (NRY) and two evolutionary strata are shown.

Figure 2

Cumulative genetic distance for 12 linkage groups (LG) in the female (blue) and male (orange) genetic maps.

Figure 3

A comparison of different genetic maps for the S. latifolia X-chromosome. Names of the genes are shown along the horizontal axis. The vertical axis shows a rescaled fraction of the total map length for each gene. The genetic positions for S. latifolia genes listed in Table 2 were rescaled and re-oriented for maps to have the same orientation and length. The male map is not shown because it lacks recombination [62,69,70].