Recurrent sex chromosome turnover mediated by distinct ARR17 and PISTILLATA duplications in willows

Sex chromosome turnovers evolve via translocation or duplication of established sex-determining genes, or their replacement by newly evolved ones. Few cases of replacements by new factors have been documented in dioecious plants, but are suspected in Salix, in which both XY and ZW systems occur, with sex-linked regions (SLRs) of different species on various chromosomes. The male-determining genes in XY species' SLRs are partial duplicates of autosomal ARR17-like genes and regulate the expression of downstream genes involved in stamen development by producing small RNAs that suppress the expression of intact copies.

Here we describe phased chromosomal assemblies of three Salix species with a ZW system derived from an XY system, including four lineages of the Salix polyclona complex (six assemblies in total). Their SLRs are within the same repeat-rich pericentromeric region of chromosome 15 as in the willows with XY system. Although these Z- and W- SLRs carry intact and/or partial ARR17 duplicates, few RNA products are detectable in our sampled tissues. However, the W-SLRs include partial duplicates of PISTILLATA (PI), a stamen development gene. These are arranged in inverted repeats and express small interfering RNAs targeting the autosomal intact Salix PI gene, suggesting that they reduce its expression, and therefore act as maleness-suppressing factors.

The turnover events involving intact ARR17 and partial PI duplications in the 15ZW clade I species involve pericentromeric regions that recombine rarely, making changes possible in these Salix species that would be unlikely in other genome regions.