Multiple independent recombinations led to hermaphrodism in domesticated grapevine

Authors: ZOU, CHENG - Cornell University; MASSONNET, MELANIE - University Of California, Davis; MINIO, ANDREA - University Of California, Davis; PATEL, SAGAR - South Dakota State University; LLACA, VICTOR - Corteva Agriscience; AVI, KARN - Cornell University; Gouker, Fred; Cadle-Davidson, Lance; REISCH, BRUCE - Cornell University; FENNELL, ANNE - South Dakota State University; CANTU, DARIO - University Of California, Davis; SUN, QI - Cornell University; Londo, Jason

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/26/2021
Publication Date: 4/13/2021
Citation: Zou, C., Massonnet, M., Minio, A., Patel, S., Llaca, V., Avi, K., Gouker, F.E., Cadle Davidson, L.E., Reisch, B., Fennell, A., Cantu, D., Sun, Q., Londo, J.P. 2021. Multiple independent recombinations led to hermaphrodism in domesticated grapevine. Nature Genetics. https://doi.org/10.1073/pnas.2023548118.
DOI: https://doi.org/10.1073/pnas.2023548118

Interpretive Summary: Hermaphrodic (perfect) flowers were a key trait in grapevine domestication, enabling a drastic increase in yields due to the efficiency of self-pollination in the domesticated grapevine (Vitis vinifera L. ssp. Vinifera). In contrast, all wild grapevine species are dioecious, each plant having only male or female flowers. In this study, we determined the region of the grapevine genome that controls the flower sex phenotype in grapevine. We used a combination of whole genome sequencing, gene expression data from flow tissues, and genetic data from a total of 556 wild and domesticated grapevines representing much of the global diversity. Our results show that a specific region of chromosome 2 is responsible for flower sex in grapevine and support two specific grapevine genes as contributing to male or female flowers in wild grapes. In all female flowering grapes the gene VvINP1 carries a deletion mutation and results in male-sterile flowering. Male flowering grapes carry a specific gene copy of the gene VviYABB3, which results in flowers without the female tissues. We also discovered that in the domesticated species, genetic recombination has occurred between VviINP1 and VviYABBy3, creating a genetic pattern that leads to flowers with both male and female structures. Most interestingly, we discovered that this is recombination has occurred at least twice in grapevine and that the event occurred before domestication of grape, 8000 years ago. This data represents the most convincing genomic evidence to date for independent domestication events in the history of cultivated grapevine.

Technical Abstract: Hermaphrodic (perfect) flowers were a key trait in grapevine domestication, enabling a drastic increase in yields due to the efficiency of self-pollination in the domesticated grapevine (Vitis vinifera L. ssp. Vinifera). In contrast, all extant wild Vitis species are dioecious, each plant having only male or female flowers. In this study, we determined the sex determining region (SDR) in the wild grapevine species, V. cinereal, using whole-genome shotgun sequencing of bulked male and female individuals. A comparative genomic analysis using shotgun resequencing data of 556 wild and domesticated accessions demonstrated that the SDR is conserved across all wild species in North America, East Asia, and Europe and that the hermaphrodite haplotig is a chimera of male and female haplotypes. Coupled with allele-specific transcriptomic analysis, our data also support the VviINP1 and VviYABBy3 are candidate genes for male fertility and female sterility, respectively, in grape. In a survey of 363 cultivated accessions, we observed two distinct hermaphrodite haplotypes (H1 and H2) with different recombination signatures. Divergence time estimates between H1 and H2 (6 million years ago) predates the domestication of grape (~8,000 years ago). Our findings emphasize the important role of recombination suppression in maintain dioecy in wild species as well as support the hypothesis that at least two independent recombination events led to the formation of perfect flowers in domesticated grapevine.