Histone H3K4 demethyltransferase VvJMJ14 promotes H₂O₂ inducing fruit ripening in grape

Fruit ripening is regulated by a complex regulatory network, including internal factors and epigenetic modification. Until now, the role of histone methylation in grape fruit ripening is unclear, especially for H3K4me3 modification. H₂O₂ treatment promotes the ripening of grape berries, but how it regulates fruit ripening and whether it affects H3K4me3 modification is poorly understood. Here, to study the relationship between H₂O₂ and H3K4me3 modification in fruit ripening, a comprehensive analysis of anti-H3K4me3 ChIP-seq and RNA-seq of grape berries after H₂O₂ treatment was performed. The results revealed that H₂O₂ treatment led to changes in expression patterns and H3K4me3 modification in heat shock protein 18.2 (VvHSP18.2), ethylene-responsive transcription factor 75 (VvERF75), and E3 ubiquitin-protein ligase PUB23 (VvPUB23). Overexpression of VvHSP18.2 promoted grape fruit ripening. Among them, VvHSP18.2 positively regulates grape fruit ripening. The potential histone H3K4 demethyltransferase (lysine-specific demethylase JMJ14) with reduced expression after H₂O₂ treatment was further identified. VvJMJ14 is located in the cytoplasm and negatively regulates grape fruit ripening. VvJMJ14 does not directly interact with VvHSP18.2, VvERF75, and VvPUB23, but promotes their transcription by affecting the H3K4me3 levels in their promoter region after H₂O₂ treatment. Overall, these results demonstrate that VvJMJ14 is a H3K4 demethyltransferase that promotes the expression of VvHSP18.2, VvERF75, and VvPUB23 by regulating H3K4me3 levels, thereby accelerating H₂O₂-induced fruit ripening in grape. This study provides a reference for the study of H₂O₂ regulation of fruit ripening at the epigenetic regulation level.