Reconfiguration of DNA methylation at growth resumption after winter dormancy in Kiwifruit

DNA methylation is an epigenetic modification that plays a role in developmental transitions by regulating gene expression. In kiwifruit (Actinidia spp.), the transition from winter dormancy to growth in spring is a critical phase, which sets the stage for flowering and fruit development in the upcoming season. It is unclear if this process is associated with changes in DNA methylation. We found that applying a hypo-methylating agent, 5-azacytidine, to dormant buds at specific stages significantly accelerated shoot emergence in kiwifruit. Genome-wide identification and expression pattern analysis of kiwifruit DNA methyltransferase and demethylase gene families identified that some of these transcripts preferentially accumulated in axillary buds during dormancy in winter or growth resumption in spring. We generated a single-base resolution map of CG, CHG and CHH methylation by whole-genome bisulfite sequencing (BS-seq) and performed a transcriptome analysis to compare dormant and growth-resuming buds. We found genome-wide CHH hyper-methylation in dormant buds and dramatically reduced CHH methylation at the stages when vegetative growth and reproductive development were re-established. Many genes involved in growth and flowering were correlated with the amount of DNA methylation, with specific changes detected in promoter regions. Surprisingly, CHH hypomethylation during the transition from winter dormancy to growth resumption was accompanied by downregulation of transposable element expression. Therefore, alternative mechanisms exist to maintain genome stability and prevent harmful TE activity during growth resumption in kiwifruit buds.