Investigation of mechanisms underlying seedlessness in a Sangiovese somatic variant through comparative genomic and histological analyses

Background: Both parthenocarpy and stenospermocarpy lead to seedless grapes. Only parthenocarpy, which is rather rare, generates berries with a complete absence of seed tissues. Stenospermocarpy, which is instead more common, produces berries with seed traces because seed development is promoted by embryo formation and then arrested by its abortion. In viticulture, parthenocarpic varieties account for a minority of the production of seedless table grapes, while they are more commonly used for raisins and very rarely for winemaking. Parthenocarpy is the putative cause of seedlessness in Corinto Nero, a bud sport of the seeded winegrape Sangiovese. In our previous studies, embryo sac abnormalities arising from meiotic disorders were accompanied by transcriptional changes in gene functions linked to gametophyte development and ovule fertilization. Here, with the aim of elucidating the cause of parthenocarpy in Corinto Nero, comparative histological and genomic analyses were performed. Results: Histologically, Corinto Nero showed abnormalities in megasporogenesis and the arrest of female gametophyte development very early during the megagametogenesis, compared to seeded Sangiovese. Genetically, Corinto Nero showed putative private mutations in candidate genes with functions related to cell cycle, meiosis and mitosis, compared to ten Sangiovese bud sports, which differed phenotypically from one another and from Corinto Nero for diverse traits, but they all were seeded. One of these mutations was validated in a Disrupted Meiotic cDNA1 homolog gene, which has a missense variant and a significant lower expression at key reproductive developmental stages in Corinto Nero. Conclusions: This work provided a list of candidate genes with somatic mutations in Corinto Nero that possibly impair sporogenesis and gametogenesis, preventing seed development. Sangiovese has a genetic predisposition to develop ovary disorders, and to forcibly set fruit in absence of pollination, which may have been turned into full expression of parthenocarpy in Corinto Nero by further mutations. A systematic genome editing of the candidate genes in the seeded Sangiovese will be required for their functional validation.