CHH hypermethylation contributes to the early ripening of grapes revealed by DNA methylome landscape of ‘Kyoho’ and its bud mutant

Abstract DNA methylation is a stable epigenetic mark that plays a crucial role in plant life processes. However, the specific functions of DNA methylation in grape berry development remain largely unknown. In this study, we performed whole-genome bisulfite sequencing on ‘Kyoho’ grape and its early-ripening bud mutant ‘Fengzao’ at different developmental stages. Our results revealed that transposons (TEs) and gene flanking regions exhibited high levels of methylation, particularly in ‘Fengzao’, attributed to CHH site methylation. Interestingly, the methylation patterns in these two cultivars showed distinct dynamics during berry development. While methylation levels of genes and TEs increased gradually in ‘Kyoho’ throughout berry development, ‘Fengzao’ did not display consistent changes. Notably, ‘Fengzao’ exhibited higher methylation levels in promoters compared to ‘Kyoho’, suggesting that hypermethylation of promoters may contribute to its early ripening phenotype. Integration of methylome and transcriptome data highlighted differentially methylated genes (DMGs) and expressed genes (DEGs) associated with secondary metabolite biosynthesis, with 38 genes identified as potential candidates involved in grape berry development. Furthermore, the study identified a jasmonate-induced oxygenase gene (JOX1) as a negative regulator of ripening in Arabidopsis and grapes, indicating that hypermethylation of JOX1 may play a role in the early ripening of ‘Fengzao’. Overall, our findings provide insights into the distinct DNA methylation patterns during grape berry development, shedding light on the epigenetic regulatory mechanisms underlying the early-ripening bud mutant.