YY males of the dioecious plant Mercurialis annua are fully viable but produce largely infertile pollen

Abstract

The suppression of recombination during sex-chromosome evolution is thought to be favoured by linkage between the sex-determining locus and sexually antagonistic loci, and leads to the degeneration of the chromosome restricted to the heterogametic sex. Despite substantial evidence for genetic degeneration at the sequence level, the phenotypic effects of the earliest stages of sex-chromosome evolution are poorly known.Here, we compare the morphology, viability and fertility between XY and YY individuals produced by crossing seed-producing males in the dioecious plant Mercurialis annua, which has young sex chromosomes with limited XÀY sequence divergence.We found no significant difference in viability or vegetative morphology between XY and YY males. However, electron microscopy revealed clear differences in pollen anatomy, and YY males were significantly poorer sires in competition with their XY counterparts. Our study suggests either that the X chromosome is required for full male fertility in M. annua, or that male fertility is sensitive to the dosage of relevant Y-linked genes.We discuss the possibility that the maintenance of male-fertility genes on the X chromosome might have been favoured in recent population expansions that selected for the ability of females to produce pollen in the absence of males.

Herbivory enhances leaky sex expression in the dioecious herbMercurialis annua

“…Our experiment on male plants involved a comparison between two treatments of simulated herbivory of contrasting intensity, but did not include undamaged plants. This is because it was initially part of a study that specifically aimed at generating males with leaky sex expression for the production of YY male plants (Li et al 2019). The absence of undamaged males means that our low vs. high herbivory comparison is a more conservative estimate of sensitivity to the intensity of herbivory, as confirmed by previously documented levels of leaky sex expression for undamaged males of the same population (Cossard and Pannell 2019, see Discussion for details).…”

“…Plant hormones are known to regulate both sex determination and defensive responses in a number of plants (Robert-Seilaniantz et al 2011, Yuan andZhang 2015), and it thus seems plausible that damage-induced hormonal changes might have altered the balance of sex-determining hormones in our experiment with M. annua. Although M. annua has chromosomal sex determination (Russell andPannell 2015, Veltsos et al 2018), its sex expression appears to be mediated by the endogenous levels of cytokinin and auxin (Hamdi et al 1987, Louis et al 1990, Durand and Durand 1991, Li et al 2019, and the exogenous application of cytokinins and auxins feminises males and masculinises females, respectively (Hamdi et al 1987, Durand andDurand 1991). It seems possible that plant responses to herbivory may collaterally affect the cytokinin/auxin ratio resulting in enhanced leakiness, perhaps in an interaction with the phytohormone jasmonate, which has been shown to mediate both anti-herbivore defence (Heil et al 2001, Thaler et al 2001, Heil 2008, Kost and Heil 2008, Ballaré 2011) and the sexual development of flowers (Acosta et al 2009, Wasternack et al 2013, Cai et al 2014, Yuan and Zhang 2015, Feng et al 2020.…”

“…Diploid populations are dioecious, with an XY chromosomal system of sex determination (Russell and Pannell 2015, Veltsos et al 2018, Li et al 2019. Males produce staminate flowers on pedunculate inflorescences held above the plant.…”

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

“…Diploid M. annua has an XY sex chromosome system, and crosses among several of the annual species suggest that they all have the same sex determination system and probably the same sex chromosomes [41]. Veltsos et al [42,43] studied the genome and sex chromosomes of diploid M. annua and found evidence for a large but only mildly degenerate sex-determining region, and Li et al [44] showed that YY males (that thus lacked an X chromosome) were fully viable, though partially sterile, consistent with the low divergence between the X and Y. Our study builds on this work by asking how the M. annua sex chromosomes relate to those in the other Mercurialis species with separate sexes.…”

Enhanced leaky sex expression in response to pollen limitation in the dioecious plant Mercurialis annua

“…Here, we demonstrate that leaky sex expression in the dioecious, wind‐pollinated annual herb Mercurialis annua is plastic and that the expression of enhanced leakiness under conditions of altered mate availability is likely adaptive. Dioecious M. annua has an XY system of sex determination in which the Y chromosome has a mildly degenerate nonrecombining region (Li et al., 2019; Veltsos et al., 2018, 2019). Sex ratios in wild populations are typically 1:1 (Russell & Pannell, 2015).…”