The evolution of sexually dimorphic expression in Salicaceae with repeated sex chromosome turnovers

Abstract Sexual dimorphism in dioecious plants is common in reproductive tissues. Genes expressed in these tissues often show sex bias and differ between sexes in their protein evolutionary rates. At the same time, sex‐linked genes often balance their expression levels between sexes through dosage compensation. We compared gene expression between males and females in floral and leaf tissues of eight dioecious Salicaceae species whose sex chromosomes are young to understand the level of conservation and diversity of genes with sex‐biased expression. Our results revealed that sexually dimorphic gene expression showed large numbers of differences among these species, with only 6% of the genes remaining conserved, showing a consistent sex‐biased direction in at least seven species. Protein evolutionary rates depended on their degree of conservation and the direction of sex bias in expression. Non‐core sex‐biased genes showed elevated evolutionary rates and core male‐biased genes showed higher nonsynonymous and synonymous substitutions than unbiased genes. Detailed studies in three willow species revealed that the expression dosage of most sex‐linked genes was partially (0.5 < X male /XX female < 1) or excessively (Z female /ZZ male > 1) compensated through reducing gene expression in the homogametic sex. Our results provide novel insights into how sexually dimorphic gene expression evolves during repeated turnovers of sex chromosomes in plants and confirm that dosage compensation mechanisms evolve relatively early in the development of sex chromosomes.