CsPRMT5-mediated histone H4R3 dimethylation negatively regulates resistance to gray blight in tea plants (<i>Camellia sinensis</i> L.)

Gray blight is a serious foliar disease that significantly threatens tea plant cultivation. Although dynamic histone methylation was reported in regulating plant immunity, the specific roles of this epigenetic modification in tea plant disease resistance have yet to be fully elucidated. This study demonstrates that the protein arginine methyltransferase CsPRMT5, which catalyzes the symmetric dimethylation of histone H4R3 (H4R3sme2), is involved in the tea plant response to gray blight. Transcription of <i>CsPRMT5</i> and the level of histone H4R3 methylation in tea were downregulated following infection by the fungal pathogen <i>Pseudopestalotiopsis</i> (<i>Ps</i>). A negative correlation was observed between the resistance of tea plants to <i>Ps</i> and the expression level of <i>CsPRMT5</i> across various cultivars. Downregulation of <i>CsPRMT5</i> expression led to reduced H4R3sme2 levels, elevated expression of defense-related genes, and lower reactive oxygen species (ROS) production after <i>Ps</i> infection, thus enhancing pathogen resistance of tea. Furthermore, complementation of <i>Atprmt5</i> mutant with <i>CsPRMT5</i> restored the susceptibility to <i>Ps</i> infection in <i>Arabidopsis</i>. Chromatin Immunoprecipitation Sequencing (ChIP-seq)and Chromatin Immunoprecipitation quantitative PCR (ChIP-qPCR) analyses revealed that CsPRMT5 binds to defense-related genes, including <i>CsMAPK3</i>, and regulates their expression through H4R3sme2 modification. Collectively, the results indicate that CsPRMT5 negatively regulates the immune response to pathogens through repressing <i>CsMAPK3</i> expression in tea plants.