Staged and repeated drought-induced regulation of phenylpropanoid synthesis confers tolerance to a water deficit environment in Camellia sinensis

This year, more than four months of extreme drought caused a nearly 30% yield reduction in Chinese tea (Camellia sinensis, Theaceae) plantations. The related dicot plants potato (Solanum tuberosum, Solanaceae) and apple (Malus pumila, Rosaceae) deploy species specific, specialized metabolites as core stress defenses. In contrast, the specialized chemical defenses in tea plants are largely unknown. The high levels of polyphenols and theanine in tea plants are potential drought-resistant substances. Stress-related overreduction is known to cause a passive accumulation of plant metabolites to dissipate excess energy. To investigate specialized metabolic drought responses, we integrated tea plant physiological, transcriptomic, and metabolite analyses with different stress modes of staged and repeated drought. Under staged drought, tea leaves were subjected to more severe oxidative stress and photosynthetic system disruption after long-term drought. However, differentially expressed genes in response to the Calvin cycle and energy metabolism were significantly increased compared with short-term drought. Tea plants that experienced three rounds of drought exhibited more robust antioxidant defense and photosynthetic efficiency and lower energy requirements than those in their first drought. Metabolomic analyses identified carbohydrates, amino acids, and phenylpropanoid compounds that accumulated significantly in tea plants after drought. Consistent with altered transcriptomics, tea plants in the two drought modes were significantly enriched in 'phenylpropanoid biosynthesis', and several phenolic acid compounds exhibited significant accumulation. Exogenous irrigation of tea plants before drought with phenylpropanoid derivatives (tea polyphenols) extracted from tea leaves significantly reduced the malonaldehyde content in the roots. In summary, the passive transfer of metabolites and upregulation of biosynthesis rates combined to regulate metabolite levels in tea plants under drought, ultimately reducing the levels of toxic oxygen radicals.