3 years ago

Jasmonate promotes artemisinin biosynthesis by activating the TCP14-ORA complex in Artemisia annua

Ke-xuan Tang, Xiao-fen Sun, Li-da Zhang, Jing-ya Zhao, Yue-li Tang, Yi-jun Zhong, Li-hui Xie, Qian He, Pin Liu, Ming-hui Chen, Ting-xiang Yan, Xiao-long Hao, Pu Shi, Qi-fang Pan, Zhang-kuanyu Wu, Xue-ying Lyu, Qian Shen, Xue-qing Fu, Fei Zhang, Ling Li, Dong-bei Xu, Ya-nan Ma

Artemisia annua produces the valuable medicinal component, artemisinin, which is a sesquiterpene lactone widely used in malaria treatment. AaORA, a homolog of CrORCA3, which is involved in activating terpenoid indole alkaloid biosynthesis in Catharanthus roseus, is a jasmonate (JA)–responsive and trichome-specific APETALA2/ETHYLENE-RESPONSE FACTOR that plays a pivotal role in artemisinin biosynthesis. However, the JA signaling mechanism underlying AaORA-mediated artemisinin biosynthesis remains enigmatic. Here, we report that AaORA forms a transcriptional activator complex with AaTCP14 (TEOSINTE BRANCHED 1/CYCLOIDEA/PROLIFERATING CELL FACTOR 14), which is also predominantly expressed in trichomes. AaORA and AaTCP14 synergistically bind to and activate the promoters of two genes, double bond reductase 2 (DBR2) and aldehyde dehydrogenase 1 (ALDH1), both of which encode enzymes vital for artemisinin biosynthesis. AaJAZ8, a repressor of the JA signaling pathway, interacts with both AaTCP14 and AaORA and represses the ability of the AaTCP14-AaORA complex to activate the DBR2 promoter. JA treatment induces AaJAZ8 degradation, allowing the AaTCP14-AaORA complex to subsequently activate the expression of DBR2, which is essential for artemisinin biosynthesis. These data suggest that JA activation of the AaTCP14-AaORA complex regulates artemisinin biosynthesis. Together, our findings reveal a novel artemisinin biosynthetic pathway regulatory network and provide new insight into how specialized metabolism is modulated by the JA signaling pathway in plants.

Publisher URL: http://advances.sciencemag.org/cgi/content/short/4/11/eaas9357

DOI: 10.1126/sciadv.aas9357

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