Early Sex-Chromosome Evolution in the Diploid Dioecious PlantMercurialis annua

Abstract

Suppressed recombination allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. The genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. Genetic mapping and exome resequencing of individuals across the species range both identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about one-third of the Y chromosome, containing 568 transcripts and spanning 22.3 cM in the corresponding female map, has ceased recombining. Nevertheless, we found limited evidence for Y-chromosome degeneration in terms of gene loss and pseudogenization, and most X- and Y-linked genes appear to have diverged in the period subsequent to speciation between M. annua and its sister species M. huetii, which shares the same sex-determining region. Taken together, our results suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining ∼1 MYA. Patterns of gene expression within the nonrecombining region are consistent with the idea that sexually antagonistic selection may have played a role in favoring suppressed recombination.

Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion

“…S2), reinforcing the conclusion that either recombination was suppressed very recently in this region, or is not yet entirely complete. These estimates are comparatively lower than those obtained in many other plant systems [67,68]. With the exception of the higher d S in stratum I, they are also similar to those One-to-one orthologous alignments between S. viminalis scaffolds and chromosome 15 of S. purpurea, with forward alignments drawn in blue and reverse alignments drawn in red.…”

How to identify sex chromosomes and their turnover

“…This method has been used to identify sex‐linked regions in several plant species (Martin et al, ; Muyle et al, , ; Veltsos et al, ; Zemp et al, ), but there are a number of important points to consider. This approach requires family data and is therefore limited to species for which pedigree information is available.…”

The Diversity of Plant Sex Chromosomes Highlighted through Advances in Genome Sequencing

“…This latter result contradicts the often-thought pattern that TEs will build up after recombination has been suppressed on the SDR. Indeed, other characteristic patterns of degeneration and gene loss thought to affect sex-specific chromosomes, or at the very least the tempo of these processes, are questioned in several recent analyses [65,87,203]. Much of this is likely due to haploid gene expression [205], which occurs in gametophyte stages in plants and exposes genes to purifying selection.…”

“…Multiple recombination-suppression events thus show a stepwise pattern of Ks along the SDR, with lower Ks for more-recent captures and higher Ks for older-captured genes. Indeed, evidence of evolutionary strata has been found in several plant species [ 69 , 87 , 109 ], suggesting plants may experience similar selective pressures that drive gene gain as animals [ 203 ]. The structural changes that cause suppressed recombination have classically been shown to be chromosomal inversions and several recent papers have found evidence in plants to also support this [ 109 , 204 ].…”