Integrated analyses of metabolome, leaf anatomy, epigenome, and transcriptome under different light intensities reveal dynamic regulation of histone modifications on the high light adaptation in Camellia sinensis.

Camellia sinensis is an industrial crop characterized by specific secondary metabolites, which provide numerous benefits to human health. Previous researches reveal that the secondary metabolism of tea plants is significantly affected by various environmental factors, especially light intensity. However, the epigenetic mechanism underlying these high light-induced changes remains systematic research. In this study, physiological analysis suggested that increased photosynthetic product was rapidly converted into other organic compounds in adaptation to high light. The metabolite landscape by widely targeted metabolome revealed 219 differentially accumulated metabolites (DAMs) in high light, with substantial upregulated DAMs accumulated in 'amino acids and derivatives' and 'alkaloids'. The landscape of nine crucial histone modifications showed the distribution diversity in the genome and the complex relationship with gene expression. Integrated analysis of stomatal development, metabolome, epigenome, and transcriptome indicated that the dynamics of histone modifications (H3K4ac, H3K4me3, H3K9ac, H3K9me2, H3K27ac, and H3K27me3) on gene regions were closely related to the expression of regulatory genes in stomatal development and enzyme genes in secondary metabolic pathways, leading to stomatal density and metabolite changes in high light. Furthermore, H3K27ac and H3K27me3 were identified as key histone modifications, regulating critical genes under high light, including CsEPFL9, CsYODAb, CsF3'Hb, CsCHSc, CsANRa, CsDFRb-2, CsAlaDC, CsAAP1, CsGGT2, CsXMPP, Cs7-NMT, CsPORC, and CsPSY. These results suggest the pivotal role of histone modifications in the high light-induced stomatal density and secondary metabolite changes of tea plants.