Epigenetic activation of auxin signaling: coordinated CHH hypomethylation and histone modifications promote bud dormancy release in tea plants

Sprouting of overwintering buds is an important biological process in tea plants (Camellia sinensis) that determines spring shoot yield and economic benefits. Epigenetic modifications, such as DNA methylation and histone marks, regulate plant growth and development; however, their precise mechanisms in tea dormancy release remain unclear. This study aimed to highlight how epigenetic auxin (IAA) coordination regulates developmental phase transition. To this end, the distinct dormancy phases of tea buds were delineated through histological observations, transcriptome profiling, ChIP-seq analyses of two histone modifications (H3K4me3, H3K27ac), and whole-genome bisulfite sequencing revealing a dynamic coordination between CHH hypomethylation, H3K4me3, and H3K27ac in the activation of genes critical for sprouting. During spring bud break, the combined loss of CHH methylation and enrichment of H3K4me3/H3K27ac at promoters was associated with genes involved in starch or sucrose metabolism and phytohormone signaling, especially IAA, such as encoding IAA biosynthesis (CsYUC), cell cycle regulators (CsCYCDs and CsCDKs), and cell wall remodeling enzymes (CsEXP and CsXTH). Mechanistically, epigenetic derepression of a central IAA response factor 18 (CsARF18) orchestrated cell cycle activation and cell wall loosening by activating CsCYCD3.3 and CsEXP10. Treatment with the DNA methyltransferase inhibitor 5-Azacytidine (5Aza) promoted the bud break of dormant tea buds, implicating a role for DNA hypomethylation in dormancy release. These findings advance our understanding of the epigenetic mechanism underlying bud dormancy.