Integrative genomics reveals the polygenic basis of seedlessness in grapevine

Abstract Seedlessness is a crucial quality trait in table grape ( Vitis vinifera L.) breeding. However, the development of seeds involved intricate regulations, while the polygenic basis of seed abortion remains unclear. Here, we combine comparative genomics, population genetics, quantitative genetics, and integrative genomics to unravel the evolution and polygenic basis of seedlessness in grapes. We generated four haplotype-resolved telomere-to-telomere (T2T) genomes for two seedless grape cultivars, ‘Thompson Seedless’ (TS, syn. ‘Sultania’) and ‘Black Monukka’ (BM). Comparative genomics identified a ∼4.25 Mb hemizygous inversion on Chr10 specific in seedless cultivars, with seedless-associated genes VvTT16 and VvSUS2 located at breakpoints. Population genomic analyses of 548 grapevine accessions revealed two distinct clusters of seedless cultivars, tracing the origin of the seedlessness trait back to ‘Sultania’. Introgression, rather than convergent selection, shaped the evolutionary history of seedlessness in grape improvement. Genome-wide association study (GWAS) analysis identified 110 quantitative trait loci (QTLs) associated with 634 candidate genes, including novel candidate genes, such as three 11S GLOBULIN SEED STORAGE PROTEIN and two CYTOCHROME P450 genes, and well-known genes like VviAGL11 . Integrative genomic analyses resulted in 339 core candidate genes categorized into 13 groups related to seed development. Machine learning based genomic selection achieved a remarkable 99% precision in predicting grapevine seedlessness. Our findings highlight the polygenic nature of seedless and provide novel candidate genes for molecular genetics and an effective prediction for seedlessness in grape genomic breeding.