Dynamic DNA Methylation Regulates Season-Dependent Secondary Metabolism in the New Shoots of Tea Plants

Plant
secondary metabolites are critical quality-conferring compositions
of plant-derived beverages, medicines, and industrial materials. The
accumulations of secondary metabolites are highly variable among seasons;
however, the underlying regulatory mechanism remains unclear, especially
in epigenetic regulation. Here, we used tea plants to explore an important
epigenetic mark DNA methylation (5mC)-mediated regulation of plant
secondary metabolism in different seasons. Multiple omics analyses
were performed on spring and summer new shoots. The results showed
that flavonoids and theanine metabolism dominated in the metabolic
response to seasons in the new shoots. In summer new shoots, the genes
encoding DNA methyltransferases and demethylases were up-regulated,
and the global CG and CHG methylation reduced and CHH methylation
increased. 5mC methylation in promoter and gene body regions influenced
the seasonal response of gene expression; the amplitude of 5mC methylation
was highly correlated with that of gene transcriptions. These differentially
methylated genes included those encoding enzymes and transcription
factors which play important roles in flavonoid and theanine metabolic
pathways. The regulatory role of 5mC methylation was further verified
by applying a DNA methylation inhibitor. These findings highlight
that dynamic DNA methylation plays an important role in seasonal-dependent
secondary metabolism and provide new insights for improving tea quality.