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

dc.contributor.authorLancaster, Jasonen
dc.contributor.authorKhrimian, Ashoten
dc.contributor.authorYoung, Sharonen
dc.contributor.authorLehner, Bryanen
dc.contributor.authorLuck, Katrinen
dc.contributor.authorWallingford, Anna K.en
dc.contributor.authorGhosh, Saikat Kumar B.en
dc.contributor.authorZerbe, Philippen
dc.contributor.authorMuchlinski, Andrewen
dc.contributor.authorMarek, Paul E.en
dc.contributor.authorSparks, Michael E.en
dc.contributor.authorTokuhisa, James G.en
dc.contributor.authorTittiger, Clausen
dc.contributor.authorKöllner, Tobias G.en
dc.contributor.authorWeber, Donald C.en
dc.contributor.authorGundersen-Rindal, Dawn E.en
dc.contributor.authorKuhar, Thomas P.en
dc.contributor.authorTholl, Dorotheaen
dc.contributor.departmentBiochemistryen
dc.contributor.departmentBiological Sciencesen
dc.contributor.departmentEntomologyen
dc.date.accessioned2019-09-10T19:24:30Zen
dc.date.available2019-09-10T19:24:30Zen
dc.date.issued2018-09-11en
dc.description.abstractInsects use a diverse array of specialized terpene metabolites as pheromones in intraspecific 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 (15,6S,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 expression is highly specific to tissues lining the cuticle of the abdominal sternites of mature males. 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 an (E,E)-farnesyl diphosphate (FPP) synthase. Structure-guided mutagenesis revealed several residues critical to MhTPS and MhFPPS activity. 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 intraspecific communication.en
dc.description.notesWe thank Megan V. Herlihy and Jeremy K. Turner for assisting with harlequin bug rearing and volatile collection and Filadelfo Guzman for assisting with GC analyses. This work was supported by US Department of Agriculture National Institute of Food and Agriculture Grant 2016-67013-24759 (to D.T., D.E.G.-R., A.K., T.P.K., C.T., and D.C.W.) and the Virginia Polytechnic Institute and State University Departments of Biochemistry and Biological Sciences and the Translational Plant Sciences Program.en
dc.description.sponsorshipUS Department of Agriculture National Institute of Food and Agriculture [2016-67013-24759]; Virginia Polytechnic Institute; State University Department of Biochemistry; State University Department of Biological Sciences; Translational Plant Sciences Programen
dc.format.mimetypeapplication/pdfen
dc.identifier.doihttps://doi.org/10.1073/pnas.1800008115en
dc.identifier.issn0027-8424en
dc.identifier.issue37en
dc.identifier.pmid30139915en
dc.identifier.urihttp://hdl.handle.net/10919/93526en
dc.identifier.volume115en
dc.language.isoenen
dc.rightsCreative Commons Attribution-NonCommercial-NoDerivatives 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by-nc-nd/4.0/en
dc.subjectHemipteraen
dc.subjectPentatomidaeen
dc.subjectharlequin bugen
dc.subjectaggregation pheromoneen
dc.subjectterpene synthaseen
dc.titleDe novo formation of an aggregation pheromone precursor by an isoprenyl diphosphate synthase-related terpene synthase in the harlequin bugen
dc.title.serialProceedings of the National Academy of Sciences of the United States of Americaen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten
dc.type.dcmitypeStillImageen

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