beta-Hydroxybutyrate Boosts Plant Immunity through Enhanced H3K9bhb Levels and Gene Expression Regulation

Metabolism-mediated epigenetic changes represent an adapted mechanism for cellular signaling, specifically the beta-hydroxybutyrate-mediated histone lysine beta-hydroxybutyrylation (Kbhb) epigenetic pathway, which couples metabolism to gene expression in animals. However, the Kbhb status of proteins in plants remains unclear. Here, we systematically characterized H3K9bhb in plants, highlighting its enrichment in the TSS region in rice and its role as an active marker for gene expression. We demonstrated functional differences between H3K9bhb and the well-studied H3K9ac, particularly in regulating immune-response genes in rice. Moreover, we show that exogenous application of beta-hydroxybutyrate enhances disease resistance in rice by inducing H3K9bhb deposition and stimulating the expression of defense-related genes. Furthermore, we identified SRT1, SRT2, and HDA705 as key players in the removal of histone Kbhb in rice plants. In addition, we identified 2,159 Kbhb sites on 1,128 proteins by Kbhb-proteomic analyses, serving as a valuable resource for future studies on Kbhb. Overall, this research advances our understanding of plant epigenetic regulation by establishing Kbhb as a cellular post-translational modification with the potential to regulate plant immune responses.