Cheng Zou, Mélanie Massonnet, Andrea Minio, Sagar Patel, Victor Llaca, Avinash Karn, Fred Gouker, Lance Cadle-Davidson, Bruce Reisch, Anne Fennell, Dario Cantu, Qi Sun, and Jason P. Londo

PNAS April 13, 2021 118 (15) e2023548118

Significance

We studied the grape sex-determining region (SDR) in 12 Vitis genomes and demonstrated its conservation across 556 genotypes including 193 accessions from 47 world-wide wild grapevine species and 363 accessions of cultivated grapevine. Although the grape SDR is recombination free in all wild species, we found two distinct hermaphrodite (H) haplotypes (H1 and H2) among the cultivated grapevines, both chimeras of male (M) and female (f) haplotypes. The two independent recombinations carry different genetic signatures which long predate the domestication of grapevine, suggesting independent evolutions of this trait in wild European grapevine gene pools prior to human domestication.

Abstract

Hermaphroditic (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 identified the male (M) and female (f) haplotypes of the sex-determining region (SDR) in the wild grapevine species V. cinerea and confirmed the boundaries of the SDR. We also demonstrated that the SDR and its boundaries are precisely conserved across the Vitis genus using shotgun resequencing data of 556 wild and domesticated accessions from North America, East Asia, and Europe. A high linkage disequilibrium was found at the SDR in all wild grape species, while different recombination signatures were observed along the hermaphrodite (H) haplotype of 363 cultivated accessions, revealing two distinct H haplotypes, named H1 and H2. To further examine the H2 haplotype, we sequenced the genome of two grapevine cultivars, 'Riesling' and 'Chardonnay'. By reconstructing the first two H2 haplotypes, we estimated the divergence time between H1 and H2 haplotypes at ∼6 million years ago, which predates the domestication of grapevine (∼8,000 y ago). Our findings emphasize the important role of recombination suppression in maintaining dioecy in wild grape species and lend additional support to the hypothesis that at least two independent recombination events led to the reversion to hermaphroditism in grapevine.

See https://www.pnas.org/content/118/15/e2023548118

Figure 1: Identification of the two SDRs of Vitis cinerea ‘B9’ genome using bulk-sampled whole-genome sequencing. Sequencing depths of uniquely mapped reads from male and female bulked libraries per 500 bp window are plotted along with the two SDR haplotypes. Twofold mapping in female individuals and singlefold mapping in male individuals delineate the SDR from upstream of VviYABBY3 and to VviAPT3 (left to right) in both haplotypes. Genes and TEs are illustrated as colored arrows and color-coded blocks, respectively. Sequence similarities between conserved regions are illustrated with gray blocks.