The UDP-glycosyltransferase MtUGT84A1 regulates anthocyanin accumulation and plant growth via JA signaling in Medicago truncatula

Anthocyanins confer plants beneficial qualities and play protective roles under extreme light conditions. Here, we characterized a novel UDP flavonoid 3-O-glucosyltransferase (UFGT) gene MtUGT84A1 and demonstrated its involvement in anthocyanin accumulation and feedback inhibition of JA signaling in M. truncatula. The loss-of-function mutants mtugt84a1–1 and mtugt84a1–2 exhibited emerald hypocotyls and dwarfism. In vitro and in vivo assays revealed that MtUGT84A1 glycosylated peonidin and delphinidin at the 3-OH position. Constitutive expression of MtUGT84A1 rescued the phenotypic abnormalities of mtugt84a1 and significantly increased the anthocyanin content in the MtUGT84A1-overexpression plants. Moreover, in mtugt84a1, the contents of JA and JA isoleucine (JA-Ile) were doubled. The transcription level of MtMYC2 was significantly increased in mtugt84a1, while decreased in the MtUGT84A1-overexpression plants, indicating MtUGT84A1 inhibits JA pathway. Under high-intensity light or MeJA treatment, MtUGT84A1 was elevated causing drastic accumulation of anthocyanins in the wildtype, but the pigments in mtugt84a1 did not alter clearly. Therefore, MtUGT84A1 not only functions as a structural gene for the final step of anthocyanin biosynthesis, but also regulates JA signaling by feedback inhibition. The findings unveil the critical roles of MtUGT84A1-modulated glycosylation of anthocyanidins and shed light on the feedback regulatory loop of MtUGT84A1 in JA-mediated biosynthesis of natural products.