Evidence for Emergence of Sex-Determining Gene(s) in a Centromeric Region in Vasconcellea parviflora

Abstract

Sex chromosomes have been studied in many plant and animal species. However, few species are suitable as models to study the evolutionary histories of sex chromosomes. We previously demonstrated that papaya (Carica papaya) (2n = 2x = 18), a fruit tree in the family Caricaceae, contains recently emerged but cytologically heteromorphic X/Y chromosomes. We have been intrigued by the possible presence and evolution of sex chromosomes in other dioecious Caricaceae species. We selected a set of 22 bacterial artificial chromosome (BAC) clones that are distributed along the papaya X/Y chromosomes. These BACs were mapped to the meiotic pachytene chromosomes of Vasconcellea parviflora (2n = 2x = 18), a species that diverged from papaya 27 million years ago. We demonstrate that V. parviflora contains a pair of heteromorphic X/Y chromosomes that are homologous to the papaya X/Y chromosomes. The comparative mapping results revealed that the male-specific regions of the Y chromosomes (MSYs) probably initiated near the centromere of the Y chromosomes in both species. The two MSYs, however, shared only a small chromosomal domain near the centromere in otherwise rearranged chromosomes. The V. parviflora MSY expanded toward the short arm of the chromosome, whereas the papaya MSY expanded in the opposite direction. Most BACs mapped to papaya MSY were not located in V. parviflora MSY, revealing different DNA compositions in the two MSYs. These results suggest that mutation of gene(s) in the centromeric region may have triggered sex chromosome evolution in these plant species.KEYWORDS FISH; centromere; heterochromatin; sex chromosome H ETEROMORPHIC sex chromosomes (X/Y, Z/W) evolved from pairs of autosomes (Ming et al. 2011;Bachtrog 2013;Charlesworth 2013). It is generally accepted that sex chromosome evolution is initiated by the emergence of a sexdetermining locus. Suppression of recombination surrounding the sex-determining locus, which favored the linkage of the sex-determining alleles with sexually antagonistic alleles, caused the decay of the Y/W chromosomes and resulted in a pair of heteromorphic sex chromosomes (Ming et al. 2011;Bachtrog 2013;Charlesworth 2013). Sex chromosomes evolved independently in different eukaryotic lineages. The mammalian X chromosome and the bird Z chromosome evolved from different portions of the ancestral genome (Bellott et al. 2010;Cortez et al. 2014). Interestingly, all therian mammals have homologous XY systems and all birds have homologous ZW systems (Graves 2008). Thus, these sex chromosomes, surprisingly, appear to have evolved only once in each of these two major evolutionary clades.Compared to mammals and birds, sex chromosomes have emerged more frequently in several other eukaryotic lineages, including plants. Sex chromosomes have been reported in at least 48 plant species across 20 different families, including both X/Y and Z/W systems (Ming et al. 2011;Kumar et al. 2014). Sex chromosomes in some plant species were identified using genetic mapping-based approaches. However, cyto...

Plant contributions to our understanding of sex chromosome evolution

“…A dioecious close relative of papaya, Vasconcellea parviflora, has been shown to have a homologous SEX locus, based on cytogenetic detection of heterochromatin in the centromere-proximal regions of the homologous chromosomes of the two species. This result also shows that the papaya and V. parviflora sex chromosomes are not truly homomorphic (Iovene et al, 2015) their heteromorphism is minor, but detectable with refined modern cytological methods, consistent with the sequencing results showing that the papaya Y-linked region is larger than the X region (Wang et al, 2012).…”

Widespread Recombination Suppression Facilitates Plant Sex Chromosome Evolution

“…Thus, regions of the genome with low rates of recombination may be generally predisposed to evolve sex-linked regions (40). Indeed, evidence for a role for ancestrally low rates of recombination in the evolution of sex chromosomes has started to emerge in plants, as reported in papaya, Carica papaya , (43) and kiwifruit, Actinidia chinensis , (45). Analogously, self-incompatibility alleles in Petunia have been identified in a region of low recombination close to a centromere (45).…”

“…Low rates of recombination may allow for the invasion of recombination modifiers completely linking haploid-expressed (pollen) genes to the Y (50, 54). Therefore, there are theoretical reasons to expect that pre-existing low-recombination plays a crucial role in sex-chromosome formation (40), and in both kiwifruit and papaya, sex-determining regions originated in centromeric regions that were likely ancestrally recombination-suppressed (43, 44). In both of these systems, however, the sex chromosomes are small and homomorphic or micro-heteromorphic.…”

Gender‐specific expression of GIBBERELLIC ACID INSENSITIVE is critical for unisexual organ initiation in dioecious Spinacia oleracea

“…However, more importantly, single-locus, epistatic systems provide a rational bridge between the evolution of monoecy and the evolution of dioecy commonly found within single clades (Diggle et al, 2011;Renner, 2014;Ma & Pannell, 2016). As such, while some recent genome studies of the evolution of nonrecombining chromosomal regions are highly informative (Ming et al, 2007;Iovene et al, 2015), it may prove more productive to use combinations of transcriptomic, reverse-genetic, and functional testing approaches to dissect the origin of sex determination in the majority of unisexual-flowering species.…”