Background: Grapevine has a major economical and cultural importance since antiquity. A key step in domestication was the transition from separate sexes (dioecy) in wild Vitis vinifera ssp. sylvestris (V. sylvestris) to hermaphroditism in cultivated Vitis vinifera ssp. sativa (V. vinifera). It is known that V. sylvestris has a XY system and V. vinifera a modified Y haplotype (called here Yh) and that the sex locus is small, but its precise boundaries, gene content and the sex-determining genes are unknown. Results: We generated a high-quality de novo reference genome for V. sylvestris, on which we mapped whole-genome re-sequencing data of a cross to locate the 111 Kb sex locus on chromosome 2. We used BAC sequences to have full assemblies of the X, Y and Yh haplotypes of V. sylvestris and V. vinifera sex locus. Studying the sex locus’ gene content and expression profiles during flower development in wild and cultivated accessions, we found that truncation and deletion of tapetum and pollen development genes (e.g pollen surface apertures gene INP1) on the X haplotype likely determine male-sterility, while the up-regulation of a Y allele of a cytokinin regulator (APRT3) may cause female-sterility. The down-regulation of this cytokinin regulator in the Yh haplotype may be sufficient to trigger reversal to hermaphroditism. Using a molecular clock, we found that the divergence between the X and Y haplotypes is consistent with the sex locus being as old as the Vitis genus. The alignment of the X and Y haplotypes revealed no inversion, the sex locus became non-recombining through another undetermined mechanism.Conclusions: We provide a genomic and evolutionary characterization of a plant sex locus, a coherent model for sex determination in wild grapevine and for the transition from dioecy to hermaphroditism during domestication, and a genome resource for studying genetic diversity and domestication in grapevine.
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