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

Abstract

Background: A key step in domestication of the grapevine 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 an XY system and V. vinifera a modified Y haplotype (Yh) and that the sex locus is small, but it has not previously been precisely characterized. Results: We generate a high-quality de novo reference genome for V. sylvestris, onto which we map whole-genome re-sequencing data of a cross to locate the sex locus. Assembly of the full X, Y, and Yh haplotypes of V. sylvestris and V. vinifera sex locus and examining their gene content and expression profiles during flower development in wild and cultivated accessions show that truncation and deletion of tapetum and pollen development genes on the X haplotype likely causes male sterility, while the upregulation of a Y allele of a cytokinin regulator (APRT3) may cause female sterility. The downregulation of this cytokinin regulator in the Yh haplotype may be sufficient to trigger reversal to hermaphroditism. Molecular dating of X and Y haplotypes is consistent with the sex locus being as old as the Vitis genus, but the mechanism by which recombination was suppressed remains undetermined. Conclusions: We describe the genomic and evolutionary characterization of the sex locus of cultivated and wild grapevine, providing a coherent model of sex determination in the latter and for transition from dioecy to hermaphroditism during domestication.

The Diversity and Dynamics of Sex Determination in Dioecious Plants

“…In contrast, all individuals with male flowers carried one functional and one non-functional copy of VviINP1 . Convincing candidate genes for the dominant female suppressor include the ADENINEPHOSPHORIBOSYL TRANSFERASE ( APRT3) , a cytokinin regulator ( Coito et al, 2018 ; Badouin et al, 2020 ) and the transcription factor YABBY3 ( Massonnet et al, 2020 ) that belongs to a gene family previously implicated in the development of carpels in A. thaliana ( Villanueva et al, 1999 ). While future studies are necessary to understand the specific roles and connections of these different factors, the current data provide strong evidence for sex determination via (at least) two genes.…”

“…Interestingly, in species that determine sex via two genes, several of the genes encoding suppressors of female development ( Su F ) are involved in cytokinin signaling as well. These genes include, among others, SyGI in kiwifruit, which encodes a cytokinin response regulator ( Akagi et al, 2018 ), the candidate gene LOG in date palm ( Torres et al, 2018 ), which encodes a cytokinin-activating enzyme, and the candidate gene APRT3 in grapes ( Badouin et al, 2020 ), which encodes an enzyme involved in the inactivation of cytokinin. Finally, two cytokinin response regulators are located in the SDR of Ginkgo ( Zhang et al, 2019 ).…”

Multiple independent recombinations led to hermaphroditism in grapevine

“…sylvestris (hereafter V. sylvestris), the wild ancestor of the domesticated species (7). A region spanning ∼150 kb region on chromosome 2 has been identified in multiple genetic studies as the sex-determining region (SDR) in grapevine (4,(8)(9)(10)(11)(12)(13)(14). However, due to long divergence time (>40 million years ago, MYA) and high heterozygosity among Vitis species, determining the mechanism for the origin of dioecy in the Vitis genus and the reversion to hermaphroditism to produce perfect flowers requires further effort.…”

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

“…The gene inaperaturate pollen1 ( VviINP1 ) likely plays a role in pollen aperture formation [ 139 ] and thus male fertility. Two strong candidates for the female-sterility gene are a YABBY3 gene ( VviYABBY3 ) and an adenine phosphoribosyltransferase ( APT ) gene ( VviAPT3 ) [ 84 , 140 ]. YABBY3 genes have been shown to play a role in flower and lateral organ development [ 141 ] and APT genes are involved in the cytokinin pathway and may be involved in suppressing carpel development [ 140 , 142 ].…”

“…Two strong candidates for the female-sterility gene are a YABBY3 gene ( VviYABBY3 ) and an adenine phosphoribosyltransferase ( APT ) gene ( VviAPT3 ) [ 84 , 140 ]. YABBY3 genes have been shown to play a role in flower and lateral organ development [ 141 ] and APT genes are involved in the cytokinin pathway and may be involved in suppressing carpel development [ 140 , 142 ]. However, functional follow-ups are necessary to confirm these roles in grapes.…”