Biosynthesis of bridged tricyclic sesquiterpenes in Inula lineariifolia

Author:

Wu Yingmei12,Chen Xueqing34,Hao Fuhua5,Liu Yu1,Luo Wei6,Zhu Yaru7,Li Li7,Han Fei7,Zhang Yunluo1,Jiang Ying7,Xiong Xingyao4,Ro Dae‐Kyun48,Shang Yi2,Huang Sanwen4,Gou Junbo19ORCID

Affiliation:

1. Hubei Shizhen Laboratory, Hubei Key Laboratory of Resources and Chemistry of Chinese Medicine College of Pharmacy, Hubei University of Chinese Medicine Wuhan 430065 China

2. Yunnan Key Laboratory of Potato Biology, The CAAS‐YNNU‐YINMORE Joint Academy of Potato Sciences Yunnan Normal University Kunming 650500 China

3. Shenzhen Hujia Technology Co., Ltd HBN Research Institute and Biological Laboratory Shenzhen 518000 China

4. Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Shenzhen Key Laboratory of Agricultural Synthetic Biology, Genome Analysis Laboratory of the Ministry of Agriculture Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences Shenzhen 518120 China

5. CAS Key Laboratory of Magnetic Resonance in Biological Systems, State Key Laboratory of Magnetic Resonance and Atomic Molecular Physics, National Center for Magnetic Resonance in Wuhan Wuhan Institute of Physics and Mathematics, Innovation Academy for Precision Measurement Science and Technology, Chinese Academy of Sciences Wuhan 430071 China

6. College of Life Science and Technology, Huazhong Agricultural University Wuhan 430070 China

7. CAS Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences Wuhan 430074 China

8. Department of Biological Sciences University of Calgary Calgary Alberta T2N1N4 Canada

9. Hubei Jiangxia Laboratory Wuhan 430070 China

Abstract

SUMMARYPresilphiperfolane‐type sesquiterpenes represent a unique group of atypical sesquiterpenoids characterized by their distinctive tricyclic structure. They have significant potential as lead compounds for pharmaceutical and agrochemical development. Herein, we utilized a transcriptomic approach to identify a terpene synthase (TPS) gene responsible for the biosynthesis of rare presilphiperfolane‐type sesquiterpenes in Inula lineariifolia, designated as IlTPS1. Through phylogenetic analysis, we have identified the evolutionary conservation of key motifs, including RR(x)8W, DDxxD, and NSE/DTE in IlTPS1, which are shared with other tricyclic sesquiterpene synthases in the TPS‐a subfamily of Asteraceae plants. Subsequent biochemical characterization of recombinant IlTPS1 revealed it to be a multiproduct enzyme responsible for the synthesis of various tricyclic sesquiterpene alcohols from farnesyl diphosphate (FPP), resulting in production of seven distinct sesquiterpenes. Mass spectrometry and nuclear magnetic resonance (NMR) spectrometry identified presilphiperfolan‐8β‐ol and presilphiperfol‐7‐ene as predominant products. Furthermore, biological activity assays revealed that the products from IlTPS1 exhibited a potent antifungal activity against Nigrospora oryzae. Our study represents a significant advancement as it not only functionally identifies the first step enzyme in presilphiperfolane biosynthesis but also establishes the heterologous bioproduction of these unique sesquiterpenes.

Funder

National Natural Science Foundation of China

Publisher

Wiley

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