The structure and evolution of sex chromosomes in an androdioecious species with two mating types.

Abstract

Though flowering plants are ancestrally hermaphroditic, some species have evolved sexual specialization and are now composed of individuals expressing just one of their two reproductive functions (either male or female) together with co-sexual individuals. Androdioecy, the co-existence of males with hermaphrodites, is rare across the living world, but unusually common in species of the Oleaceae plant family. The mediterranean shrub Phillyrea angustifolia has a simple mendelian XY sex-determination system for androdioecy, but the underlying molecular determinants and the evolutionary history of the X and Y chromosomes remain unknown. The ability of males to by-pass the self-incompatibility phenotype expressed in hermaphrodites is essential to explain their high frequency in natural populations, but how the loci governing sex and self-incompatibility epistatically interact also remains unknown. To address these questions, we obtained full haplotype-resolved de novo chromosomal assemblies of P. angustifolia and its sister species P. latifolia. The sex-determining region in P. angustifolia spanned a fifth of chromosome 12, and was strikingly larger and more rearranged than that in P. latifolia. The male-specific region contains two putative sex-determining genes, ANDY1 and ANDY2, a tandem encoding two flowering-related transcription factors that arose by translocation followed by duplication of an autosomal gene before the two species diverged. Strikingly, this sex-determining region also contains a recent duplicate of the pollen allergen gene Ole-e1, which shows the strongest differential expression between the two self-incompatibility groups of hermaphrodites, hence establishing a direct molecular link between sex and self-incompatibility. Overall, our results provide novel insight on sex determination and the evolution of sex chromosomes in a plant lineage where the separation between sexes is still incomplete, and offer a possible mechanistic basis for the strong epistatic interaction between the sex and self-incompatibility determinants, with direct implication for how sex-ratios are established in nature.