Recurrent allopolyploidization, Y-chromosome introgression and the evolution of sexual systems in the plant genus Mercurialis

Abstract

The plant genus Mercurialis includes dioecious, monoecious and androdioecious species (where males coexist with hermaphrodites). Its diversification involved reticulate evolution via hybridization and polyploidization. The Y chromosome of the diploid species Mercurialis annua shows only mild signs of degeneration. We used sequence variation at a Y-linked locus in several species and at multiple autosomal and pseudoautosomal loci to investigate the origin and evolution of the Y chromosome across the genus. Our study provides evidence for further cases of allopolyploid speciation. It also reveals that all lineages with separate sexes (with one possible exception) share the same ancestral Y chromosome. Surprisingly, males in androdioecious populations of hexaploid M. annua carry a Y chromosome that is not derived from either of its two putative progenitor lineages but from a more distantly related perennial dioecious lineage via introgression. These results throw new light on the evolution of sexual systems and polyploidy in Mercurialis and secure it as a promising model for further study of plant sex chromosomes. This article is part of the theme issue ‘Sex determination and sex chromosome evolution in land plants’.

Evolutionary origin and establishment of a dioecious diploid‐tetraploid complex

“…This implies that the autotetraploids have a stable dioecious sexual system. The other similar plant systems (Akagi et al, 2016;Gerchen et al, 2022;Krasovec et al, 2018;Toups et al, 2022;Warmke & Blakeslee, 1939;Westergaard, 1958). Hence, we speculated that the W2 inherited female-heterogametic system from its diploid progenitor, this system was maintained during polyploidization and helped W2 to keep the dioecious sexual system rather than reversion to another sexual system.…”

“…This barrier, however, does not always work (Stöck et al, 2021; Warmke & Blakeslee, 1939), especially for less differentiated and nondegenerated sex chromosomes which are common in plants (Charlesworth, 2015). Polyploidization in plants may trigger transitions of diploid dioecy to other sexual systems, especially in species with less differentiated sex chromosomes (Akagi et al, 2016; Gerchen et al, 2022). A dominant sex determinator on a single Y or W chromosome can compensate the dosage effect of polyploidization, thus maintaining a stable dioecy system (Henry et al, 2018; Warmke & Blakeslee, 1939).…”

Does polyploidy inhibit sex chromosome evolution in angiosperms?

“…Polyploids have been observed to be associated with loss of dioecy of diploid progenitors, with changes occurring to monoecy, e.g., in hexaploid Diospyros kaki (Akagi et al, 2016), to hermaphroditism, e.g., in tetraploid Empetrum (Anderberg, 1994), or to monoecy and androdioecy in tetra-to dodecaploid Mercurialis (Pannell et al, 2004;Gerchen et al, 2022). In willows (Salix), shifts to diverse sexual systems occur in polyploids (Mirski, 2014;Mirski et al, 2017).…”

“…However, also gene dosage effects and differential homeolog expression could cause lability if only one active Y interacts with multiple copies of x (unless all but one have turned into autosomes). Interestingly, introgression of a new Y chromosome from distantly related species happened at the origin of hexaploid, androdioecious Mercurialis annua (Gerchen et al, 2022). Such reversals to non-dioecious sexual systems may be indicators that polyploidization can prevent the maintenance of sexdetermining systems for long evolutionary times, and this may be a further factor contributing to the rarity of degenerated sex chromosomes in plants.…”

“…Almost all angiosperms in which sex chromosome evolution is currently studied, including kiwi, papaya, persimmon, asparagus, strawberry, are cultivated plants (Henry et al, 2018), and little is known about sex chromosome evolution in natural polyploid systems. However, some examples (Table 1) include the tetraploids Rumex acetosella (Cunado et al, 2007) and hexaploid Mercurialis annua (Gerchen et al, 2022) all with male heterogamety. We briefly summarize sex chromosome evolution in diploids, and focus here on models of polyploidization from progenitors with established diploid non-degenerated systems (XY), and discuss how the presence of SLR-bearing chromosomes may affect new polyploids, and the cytological consequences, and whether polyploidy favors breakdown of dioecy, or causes reversals of X (or Z) chromosomes back to autosomes.…”