H3K4me3 plays a key role in establishing permissive chromatin states during bud dormancy and bud break in apple

SUMMARY Bud dormancy helps woody perennials survive winter and activate robust plant development in the spring. For apple (Malus × domestica), short‐term chilling induces bud dormancy in autumn, then prolonged chilling leads to dormancy release and a shift to a quiescent state in winter, with subsequent warm periods promoting bud break in spring. Epigenetic regulation contributes to seasonal responses such as vernalization. However, how histone modifications integrate seasonal cues and internal signals during bud dormancy in woody perennials remains largely unknown. Here, we show that H3K4me3 plays a key role in establishing permissive chromatin states during bud dormancy and bud break in apple. The global changes in gene expression strongly correlated with changes in H3K4me3, but not H3K27me3. High expression of DORMANCY‐ASSOCIATED MADS‐box (DAM) genes, key regulators of dormancy, in autumn was associated with high H3K4me3 levels. In addition, known DAM/SHORT VEGETATIVE PHASE (SVP) target genes significantly overlapped with H3K4me3‐modified genes as bud dormancy progressed. These data suggest that H3K4me3 contributes to the central dormancy circuit, consisting of DAM/SVP and abscisic acid (ABA), in autumn. In winter, the lower expression and H3K4me3 levels at DAMs and gibberellin metabolism genes control chilling‐induced release of dormancy. Warming conditions in spring facilitate the expression of genes related to phytohormones, the cell cycle, and cell wall modification by increasing H3K4me3 toward bud break. Our study also revealed that activation of auxin and repression of ABA sensitivity in spring are conditioned at least partly through temperature‐mediated epigenetic regulation in winter. Significance Statement The active histone methylation mark H3K4me3 underpins the changes in expression of genes involved in metabolic pathways involving phytohormones, the cell cycle, and cell wall modification during bud dormancy and break in apple. This research uncovers an epigenetic mechanism that establishes a permissive chromatin state at critical regulators underlying floral bud dormancy progression and bud break in perennials.