A small XY chromosomal region explains sex determination in wild dioecious V. vinifera and the reversal to hermaphroditism in domesticated grapevines

Abstract

BackgroundIn Vitis vinifera L., domestication induced a dramatic change in flower morphology: the wild sylvestris subspecies is dioecious while hermaphroditism is largely predominant in the domesticated subsp. V. v. vinifera. The characterisation of polymorphisms in genes underlying the sex-determining chromosomal region may help clarify the history of domestication in grapevine and the evolution of sex chromosomes in plants. In the genus Vitis, sex determination is putatively controlled by one major locus with three alleles, male M, hermaphrodite H and female F, with an allelic dominance M > H > F. Previous genetic studies located the sex locus on chromosome 2. We used DNA polymorphisms of geographically diverse V. vinifera genotypes to confirm the position of this locus, to characterise the genetic diversity and traces of selection in candidate genes, and to explore the origin of hermaphroditism.ResultsIn V. v. sylvestris, a sex-determining region of 154.8 kb, also present in other Vitis species, spans less than 1% of chromosome 2. It displays haplotype diversity, linkage disequilibrium and differentiation that typically correspond to a small XY sex-determining region with XY males and XX females. In male alleles, traces of purifying selection were found for a trehalose phosphatase, an exostosin and a WRKY transcription factor, with strikingly low polymorphism levels between distant geographic regions. Both diversity and network analysis revealed that H alleles are more closely related to M than to F alleles.ConclusionsHermaphrodite alleles appear to derive from male alleles of wild grapevines, with successive recombination events allowing import of diversity from the X into the Y chromosomal region and slowing down the expansion of the region into a full heteromorphic chromosome. Our data are consistent with multiple domestication events and show traces of introgression from other Asian Vitis species into the cultivated grapevine gene pool.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0229-z) contains supplementary material, which is available to authorized users.

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

“…Plant species with homomorphic sex chromosomes so far investigated have been found to have a SDR < 1% of the total length of the Y chromosome, e.g., Vitis vinifera [44,45], several Populus species [46,47], and Fragaria chiloensis [48]. Mercurialis annua thus appears to have a particularly large SDR for a species with homomorphic sex chromosomes.…”

“…Table S1: Summary of information on size and divergence in systems with homomorphic and heteromorphic sex chromosomes. References [10,17,18,19,22,45,46,47,48,50,51,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91] are cited in Supplementary Table S1. Table S2: Information on PCR primers.…”

Plant contributions to our understanding of sex chromosome evolution

“…This has recently been successful in the grape vine (Vitis vinifera), an XY system. The fully sex-linked genome region is only c. 150 kb, and includes only a few fully sex-linked genes, and so recombination suppression has clearly not yet extended across any substantial genome region (Picq et al, 2014), consistent with the lack of chromosomal heteromorphism.…”

The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations

“…Other species have few fully sex‐linked genes, for example the grape vine (Picq et al. ) and persimmon (Akagi et al. ), while some are intermediate between these extremes; for example, between 50 and 100 genes are sex‐linked in papaya, and about 50 have copies on both the X and the Y (Wang et al.…”

“…The fully sex-linked region of Silene latifolia includes hundreds of genes, many still present on the Y chromosome (Bergero and Charlesworth 2011;Chibalina and Filatov 2011). Other species have few fully sex-linked genes, for example the grape vine (Picq et al 2014) and persimmon (Akagi et al 2014), while some are intermediate between these extremes; for example, between 50 and 100 genes are sex-linked in papaya, and about 50 have copies on both the X and the Y (Wang et al 2012).…”