Widespread recombination suppression facilitates plant sex chromosome evolution

Classical models suggest that recombination rates on sex chromosomes
evolve in a stepwise manner to localize sexually antagonistic variants in
the sex in which they are beneficial, thereby lowering rates of
recombination between X and Y chromosomes. However, it is also possible
that sex chromosome formation occurs in regions with pre-existing
recombination suppression. To evaluate these possibilities, we constructed
linkage maps and a chromosome-scale genome assembly for the dioecious
plant Rumex hastatulus. This species has a polymorphic karyotype with a
young neo-sex chromosome, resulting from a Robertsonian fusion between the
X chromosome and an autosome, in part of its geographical range. We
identified the shared and neo-sex chromosome using comparative genetic
maps of the two cytotypes. We found that sex-linked regions of both the
ancestral and the neo-sex chromosome are embedded in large regions of low
recombination. Furthermore, our comparison of the recombination landscape
of the neo-sex chromosome to its autosomal homologue indicates that low
recombination rates preceded sex linkage. These patterns are not unique to
the sex chromosomes; all chromosomes were characterized by massive regions
of suppressed recombination spanning most of each chromosome. This
represents an extreme case of the periphery-biased recombination seen in
other systems with large chromosomes. Across all chromosomes, gene and
repetitive sequence density correlated with recombination rate, with
patterns of variation differing between repetitive element type. Our
findings suggest that ancestrally low rates of recombination may
facilitate the formation and subsequent evolution of heteromorphic sex
chromosomes.