Sex chromosome evolution mediated by a large inversion and a possible switch of the sex determination gene

Sex chromosomes often evolve faster than autosomes and commonly degenerate after recombination arrest. However, the underlying evolutionary processes are under persistent debate. In particular, it is unclear whether or not recombination arrest generally evolves in a stepwise manner and how switches in sex determination genes contribute to sex chromosome evolution. Here, we investigate sex chromosome evolution in the dioecious plant genus Salix.

We identify Z- and W-regions (~ 8 Mb) on chromosome 15 of the dwarf willow Salix herbacea using a new haplotype-resolved assembly. The W-region harbours a large (5 Mb) embedded inversion. Analyses of synteny with other Salix species, sequence divergence between sex chromosomes and sequence degeneration suggest that this inversion recently incorporated pseudoautosomal sequence into the W-region, extending its length nearly three-fold. The W-region exclusively contains seven pairs of inverted partial repeats of the male essential floral identity gene PISTILLATA, suggesting a possible PISTILLATA suppression mechanism by interfering RNA in females. Such PISTILLATA pseudogenes are also found in other Salix species with ZW sex determination but not in those with XY sex determination.

Our study provides rare and compelling support for the long-standing theory of inversions underlying stepwise recombination reduction and raises the hypothesis that the turnover of sex chromosomes in the Salicaceae family might be associated with a switch of the sex determination gene.