Although Al is not necessary or even toxic to most plants, it is beneficial for the growth of tea plants. However, the mechanism through which Al promotes root growth in tea plants remains unclear. In the present study, we found that flavonol glycoside levels in tea roots increased following Al treatment, and the Al-induced UDP glycosyltransferase CsUGT84J2 was involved in this mechanism. Enzyme activity assays revealed that rCsUGT84J2 exhibited catalytic activity on multiple types of substrates, including phenolic acids, flavonols, and auxins in vitro. Furthermore, metabolic analysis with UPLC-QqQ-MS/MS revealed significantly increased flavonol and auxin glycoside accumulation in CsUGT84J2-overexpressing Arabidopsis thaliana. In addition, the expression of genes involved in the flavonol pathway as well as in the auxin metabolism, transport, and signaling pathways was remarkably enhanced. Additionally, lateral root growth and exogenous Al stress tolerance were significantly improved in transgenic Arabidopsis thaliana. Moreover, gene expression and metabolic accumulation related to phenolic acids, flavonols, and auxin were upregulated in CsUGT84J2-overexpressing tea plants but downregulated in CsUGT84J2-silenced tea plants. In conclusion, Al treatment induced CsUGT84J2 expression, mediated flavonol and auxin glycosylation, and regulated endogenous auxin homeostasis in tea roots, thereby promoting the growth of tea plants. Our findings lay the foundation for studying the precise mechanisms through which Al promotes the growth of tea plants.

Polyphenol-rich tea plants are aluminum (Al) accumulators. Whether an association exists between polyphenols and Al accumulation in tea plants remains unclear. This study revealed that the accumulation of the total Al and bound Al contents were both higher in tea samples with high flavonol content than in low, and Al accumulation in tea plants was significantly and positively correlated with their flavonol content. Furthermore, the capability of flavonols combined with Al was higher than that of epigallocatechin gallate (EGCG) and root proanthocyanidins (PAs) under identical conditions. Flavonol–Al complexes signals (94 ppm) were detected in the tender roots and old leaves of tea plants through solid-state 27Al nuclear magnetic resonance (NMR) imaging, and the strength of the signals in the high flavonol content tea samples was considerably stronger than that in the low flavonol content tea samples. This study provides a new perspective for studying Al accumulation in different tea varieties.