Jasmonate-regulated ERF109-MYB51-MYC3 ternary complexes control indolic glucosinolates biosynthesis

Jasmonates (JAs) are plant hormones which regulate biosynthesis of many secondary metabolites, such as glucosinolates (GLSs), through JAs-responsive transcription factors (TFs). The JAs-responsive CYP83B1 gene, has been shown to catalyze the conversion of indole-3-acetaldoxime (IAOx) to indolic glucosinolates (IGLSs). However, little is known about the regulatory mechanism of CYP83B1 gene expression by JAs. In yeast one-hybrid screens using the CYP83B1 promoter as bait we isolated two JAs-responsive TFs ERF109 and MYB51 that are involved in JAs-regulated IGLS biosynthesis. Furthermore, using a yeast two-hybrid assay, we identified ERF109 as an interacting partner of MYB51, and Jasmonate ZIM-domain (JAZ) proteins as interactors of MYB51, and BTB/POZ-MATH (BPM) proteins as interactors of ERF109. Both JAZ and BPM proteins are necessary for the full repression of the ERF109-MYB51-MYC3 ternary complex activity on CYP83B1 gene expression and JA-regulated IGLS biosynthesis. Biochemical analysis showed that the 26S proteasome-mediated degradation of ERF109 protein is mediated by a CRL3BPM E3 ligase independently of JA signaling. Genetic and physiological evidence shows that MYB51 acts as an adaptor and activator to bridge the interaction with the co-activators MYC3 and ERF109, for synergistically activating the CYP83B1 gene expression, and all three factors are essential and exert a coordinated control in JAs-induced IGLS biosynthesis. Overall, this study provides insights into the molecular mechanisms of JAs-responsive ERF109-MYB51-MYC3 ternary complexes in controlling JAs-regulated GLSs biosynthesis, which provides a better understanding of plant secondary metabolism. One-sentence summaryThe JA-responsive ERF109-MYB51-MYC3 ternary complex controls JAs-regulated GLSs biosynthesis.