Size and Content of the Sex-Determining Region of the Y Chromosome in Dioecious Mercurialis annua, a Plant with Homomorphic Sex Chromosomes

Abstract

Dioecious plants vary in whether their sex chromosomes are heteromorphic or homomorphic, but even homomorphic sex chromosomes may show divergence between homologues in the non-recombining, sex-determining region (SDR). Very little is known about the SDR of these species, which might represent particularly early stages of sex-chromosome evolution. Here, we assess the size and content of the SDR of the diploid dioecious herb Mercurialis annua, a species with homomorphic sex chromosomes and mild Y-chromosome degeneration. We used RNA sequencing (RNAseq) to identify new Y-linked markers for M. annua. Twelve of 24 transcripts showing male-specific expression in a previous experiment could be amplified by polymerase chain reaction (PCR) only from males, and are thus likely to be Y-linked. Analysis of genome-capture data from multiple populations of M. annua pointed to an additional six male-limited (and thus Y-linked) sequences. We used these markers to identify and sequence 17 sex-linked bacterial artificial chromosomes (BACs), which form 11 groups of non-overlapping sequences, covering a total sequence length of about 1.5 Mb. Content analysis of this region suggests that it is enriched for repeats, has low gene density, and contains few candidate sex-determining genes. The BACs map to a subset of the sex-linked region of the genetic map, which we estimate to be at least 14.5 Mb. This is substantially larger than estimates for other dioecious plants with homomorphic sex chromosomes, both in absolute terms and relative to their genome sizes. Our data provide a rare, high-resolution view of the homomorphic Y chromosome of a dioecious plant.

The wild grape genome sequence provides insights into the transition from dioecy to hermaphroditism during grape domestication

“…The two genes at the opposite limits of the non-recombining region had a dS of 0.03, suggesting that suppression of recombination occurred very recently and in a single step in V. sylvestris . The maximum dS was 0.0424, which is to our knowledge lower than any of the other systems dated in plants ( Mercurialis annuua has a maximum dS of 0.05 15 ). To identify deletions in the Y haplotype, we compared the X haplotype and two BAC contigs covering the Y haplotype (Supplementary Figures 2-5).…”

Low siring success of females with an acquired male function illustrates the legacy of sexual dimorphism in constraining the breakdown of dioecy

“…XY) (Russell & Pannell ; Veltsos et al . ). Progeny sired by males will thus be 50% male and 50% monoecious.…”

“…In M. annua, males are determined by the expression of a dominant allele at a single locus, so that males are heterozygous (i.e. XY) (Russell & Pannell 2015;Veltsos et al 2018). Progeny sired by males will thus be 50% male and 50% monoecious.…”

Sex‐chrom, a database on plant sex chromosomes

“…It would be interesting to see if this or a similar mechanism evolved in other species. There are unexpectedly high proportions of nonrecombining loci, recently found by high throughput sequencing, in the sex chromosomes of Mercurialis (c. 30%) (Veltsos et al, 2018) and Cannabis (c. 70%) (Prentout et al, 2020). These examples show the importance of multidisciplinary approaches (including more genetic maps), as these species were supposed to have recent homomorphic sex chromosomes that are now revealed as more ancient and differentiated (but see Divashuk et al, 2014 on Cannabis).…”