De novo formation of an aggregation pheromone precursor by an isoprenyl diphosphate synthase-related terpene synthase in the harlequin bug

Authors: LANCASTER, JASON - Virginia Tech; Khrimian, Ashot; YOUNG, SHARON - University Of Nevada; LEHNER, BRYAN - Virginia Tech; LUCK, KATRIN - Max Planck Institute Of Chemical Ecology; WALLINGFORD, ANNA - Virginia Tech; Ghosh, Saikat Kumar; ZERBE, P - University Of California, Davis; MAREK, P - Virginia Tech; Sparks, Michael; TITTIGER, C - University Of Nevada; KOLLNER, T - Max Planck Institute Of Chemical Ecology; Weber, Donald; Gundersen-Rindal, Dawn; KUHAR, THOMAS - Virginia Tech; THOLL, DOROTHEA - Virginia Tech

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/23/2018
Publication Date: 8/23/2018
Citation: Lancaster, J., Khrimian, A., Young, S., Lehner, B., Luck, K., Wallingford, A., Ghosh, S.B., Zerbe, P., Marek, P., Sparks, M., Tittiger, C., Kollner, T.G., Weber, D.C., Gundersen, D.E., Kuhar, T., Tholl, D. 2018. De novo formation of an aggregation pheromone precursor by an isoprenyl diphosphate synthase-related terpene synthase in the harlequin bug. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.1800008115.
DOI: https://doi.org/10.1073/pnas.1800008115

Interpretive Summary: Stink bugs and other insects use volatile chemicals called pheromones for communication. If the communication systems of pest insects, and the way in which they make (synthesize) their pheromones, are known, pest managers might be able to suppress pest populations by trapping or disrupting mating and reproduction. This would provide a new strategy to reduce or eliminate pesticide applications for these pests. Males of the harlequin bug, a stink bug pest of crucifer crops such as cabbage, collards, and broccoli, produce a specific pheromone called murgantiol attractive to both males and females. In this study, we discovered an enzyme (called a terpene sythase) that is new to science, and unrelated to microbial or plant terpene synthases. This novel enzyme produces an important intermediate in the pheromone biosynthesis. Knowledge of pheromone biosynthesis in stink bugs may lead to the development of new controls of these pests. The study is of interest to researchers in entomology and biochemistry who are seeking practical, environmentally-friendly solutions for pest management.

Technical Abstract: Insects use a diverse array of terpene specialized metabolites as pheromones in intra-specific interactions. In contrast to plants and microbes, which employ enzymes called terpene synthases (TPSs) to synthesize terpene metabolites, limited information from few species is available about the enzymatic mechanisms underlying terpene pheromone biosynthesis in insects. Several stink bugs (Hemiptera: Pentatomidae), among them severe agricultural pests, release 15-carbon sesquiterpenes with a bisabolene skeleton as sex or aggregation pheromones. The harlequin bug, Murgantia histrionica, a specialist pest of crucifers, uses two stereoisomers of 10,11-epoxy-1-bisabolen-3-ol as a male-released aggregation pheromone called murgantiol. We show that MhTPS (MhIDS-1), an enzyme unrelated to plant and microbial TPSs but with similarity to trans-isoprenyl diphosphate synthases (IDS) of the core terpene biosynthetic pathway, catalyzes the formation of (1S,6S,7R)-(1,10-bisaboladien-1-ol) (sesquipiperitol) as a terpene intermediate in murgantiol biosynthesis. Sesquipiperitol, a so far unknown compound in animals, also occurs in plants, indicating convergent evolution in the biosynthesis of this sesquiterpene. RNAi-mediated knockdown of MhTPS mRNA confirmed the role of MhTPS in murgantiol biosynthesis. MhTPS activity is restricted to mature males and highly specific to tissues lining the cuticle of the abdominal sternites. Phylogenetic analysis suggests that MhTPS is derived from a trans-IDS progenitor and diverged from bona fide trans-IDS proteins including MhIDS-2, which functions as a (E,E)-farnesyl diphosphate (FPP) synthase. The emergence of an IDS-like protein with TPS activity in M. histrionica demonstrates that de novo terpene biosynthesis evolved in the Hemiptera in an adaptation for intra-specific communication.