A dirigent protein redirects extracellular terpenoid metabolism for defense against biotic challenges

Jia-Ling Lin, Wen-Kai Wu, Gui-Bin Nie, Jian-Xu Li, Xin Fang, Yin-Guo Sheng, Meng-Meng Wang, Qi-Yue Zheng, Xiao-Xiang Guo, Jia-Fa Huang, Li-Ying Ma, Ling-Jian Wang, Jia-Xin Liu, Shan-Shan Wang, Baofu Xu, Yiqun Gao, Yan Li, Dong Wang, Cathie Martin, Xiao-Ya Chen and Jin-Quan Huang ()
Additional contact information
Jia-Ling Lin: Chinese Academy of Sciences
Wen-Kai Wu: Chinese Academy of Sciences
Gui-Bin Nie: Chinese Academy of Sciences
Jian-Xu Li: Chinese Academy of Sciences
Xin Fang: Chinese Academy of Sciences
Yin-Guo Sheng: Chinese Academy of Sciences
Meng-Meng Wang: Chinese Academy of Sciences
Qi-Yue Zheng: Chinese Academy of Sciences
Xiao-Xiang Guo: Chinese Academy of Sciences
Jia-Fa Huang: Chinese Academy of Sciences
Li-Ying Ma: Chinese Academy of Sciences
Ling-Jian Wang: Chinese Academy of Sciences
Jia-Xin Liu: Chinese Academy of Sciences
Shan-Shan Wang: Chinese Academy of Sciences
Baofu Xu: Bohai Rim Advanced Research Institute for Drug Discovery
Yiqun Gao: Shenzhen University
Yan Li: Bohai Rim Advanced Research Institute for Drug Discovery
Dong Wang: Ltd
Cathie Martin: John Innes Centre
Xiao-Ya Chen: Chinese Academy of Sciences
Jin-Quan Huang: Chinese Academy of Sciences

Nature Communications, 2025, vol. 16, issue 1, 1-19

Abstract: Abstract Plants have evolved an extensive repertoire of specialized metabolites to adapt to complex environmental changes. Here, we identify two paralogous dirigent proteins (DPs) in cotton that serve as gatekeepers of extracellular terpenoid phytoalexin production in green organs, directing the transition of hemigossypol away from gossypol synthesis toward a hydroxylation pathway that leads to the biosynthesis of highly toxic hemigossypolone and heliocides. Under oxidative conditions, these proteins function synergistically with aldo-keto reductases to catalyze the hydroxylation of hemigossypol, followed by spontaneous oxidation that yields hemigossypolone, revealing a noncanonical role for aldo-keto reductases in extracellular terpenoid metabolism. Notably, mutants lacking these dirigent proteins produce gossypol but are devoid of hemigossypolone and heliocides in green organs exhibit heightened susceptibility to multiple biotic stresses, underscoring the enhanced protective role of these metabolites. This study describes a DPs-mediated mechanism of extracellular hydroxylation and highlights the potential ecological advantages of redirecting specialized metabolism extracellularly for enhanced defense against varying types of pathogens and herbivores.

Date: 2025
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DOI: 10.1038/s41467-025-64323-z

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