Abstract Ultraviolet-B (UV-B) irradiation is an effective elicitor for the biosynthesis of pharmaceutically relevant monoterpenoid indole alkaloids (MIAs). Uncaria rhynchophylla (UR) produces numerous valuable MIAs, such as rhynchophylline and isorhynchophylline, which have huge chemotherapeutic potential. However, the mechanism underlying UV-B-induced MIAs remains elusive in MIA-producing plants. Here, we performed integrative transcriptome and metabolome analyses and found that UV-B distinctly induced MIA accumulation in UR leaves. Furthermore, we report that two UV-B-responsive transcription factors, UrWRKY40 and ELONGATED HYPOCOTYL 5 (UrHY5), cooperatively promote UV-B-induced MIA biosynthesis by activating MIA structural genes (UrSTR1, UrCPR1) via binding to their promoters (W-box and T/G-box elements). Comparative interactomics and dual-luciferase assays demonstrated that UrWRKY40 physically interacts with UrHY5 and represses its transcriptional activity under normal white light conditions. However, UV-B disrupted the formation of the UrWRKY40-UrHY5 complex and attenuated the repressive effects of UrWRKY40 on UrHY5 activity, thereby enhancing UrHY5-driven transactivation of downstream MIA structural genes. In addition, UV-B stimulated limited ABA production, which partially repressed UrWRKY40 expression, but not enough to override its induction by UV-B. In the presence of ABA, the UrWRKY40-UrHY5 interaction dissolved, which in turn released UrHY5 from repression, allowing it to activate MIA biosynthesis. These findings uncover a mechanism by which the UrWRKY40-UrHY5 module positively regulates UV-B-induced MIA biosynthesis by coordinating UV-B and ABA signaling, and provide a strategic framework for enhancing high-value MIA production through genetic manipulation.
Yang et al. (Tue,) studied this question.