Plant sex chromosomes defy evolutionary models of expanding recombination suppression and genetic degeneration.

Abstract

Hundreds of land plant lineages have independently evolved separate sexes in either gametophytes (dioicy) or sporophytes (dioecy), but 43% of all dioecious angiosperms are found in just 34 entirely dioecious clades, suggesting that their mode of sex determination evolved a long time ago. Here, we review recent insights on the molecular mechanisms that underlie the evolutionary change from individuals that each produce male and female gametes to individuals specializing in the production of just one type of gamete. The canonical model of sex chromosome evolution in plants predicts that two sex-determining genes will become linked in a sex-determining region (SDR), followed by expanding recombination suppression, chromosome differentiation and, ultimately, degeneration. Experimental work, however, is showing that single genes function as master regulators in model systems, such as the liverwort Marchantia and the angiosperms Diospyros and Populus. In Populus, this type of regulatory function has been demonstrated by genome editing. In other systems, including Actinidia, Asparagus and Vitis, two coinherited factors appear to independently regulate female and male function, yet sex chromosome differentiation has remained low. We discuss the best-understood systems and evolutionary pathways to dioecy, and present a meta-analysis of the sizes and ages of SDRs. We propose that limited sexual conflict explains why most SDRs are small and sex chromosomes remain homomorphic. It appears that models of increasing recombination suppression with age do not apply because selection favours mechanisms in which sex determination depends on minimal differences, keeping it surgically precise.