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

Abstract

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.

Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass

“…Our functional analyses showed the enrichment of H3K4me3 around the TSS and 5’end of the transcriptionally active genes, which is consistent with the distribution of histone modifications in other plants (Arabidopsis [ 55 ], rice [ 44 , 51 ], sorghum [ 49 ], apple, [ 56 ], soybean [ 57 ], eucalyptus [ 58 ]), implying a conserved regulatory role of H3K4me3. In addition, we assigned the functions associated with the genes marked by H3K4me3.…”

MADS-box protein PpDAM6 regulates chilling requirement-mediated dormancy and bud break in peach

“…S4A ), as demonstrated in hybrid aspen and peach in the process of low temperature accumulation ( Singh et al 2018 ; Zhu et al 2020 ; Canton et al 2022 ). Following this consideration, we speculated there are two possible reasons for this phenomenon, H3K4me3 modification may be involved in the expression of PpDAM6, just occurred at DAMs locus in apple ( Chen et al 2022 ) or H3K27me3 deposition may occur at nondormant stages after CR fulfillment, specifically in nondormant buds in sweet cherry and peach ( Vimont et al 2020 ; Zhu et al 2020 ), while flower buds were collected during chilling accumulation in our case.…”

Silencing of a raspberry homologue ofVRN1is associated with disruption of dormancy induction and misregulation of subsets of dormancy-associated genes

“…These processes likely initiate silencing of gene expression that would lead to growth arrest. Involvement of histone and DNA methylation in the establishment of winter dormancy has been widely described in other temperate species (Rothkegel et al 2020; W. Chen et al 2022; Conde et al 2013; Ríos et al 2014). The role of RNAi mechanisms in the process is less studied, although variations in the miRNA linked to QTL controlling chilling requirements have been reported in peach (Barakat et al 2012).…”