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Proc Natl Acad Sci U S A

Title:		De novo formation of an aggregation pheromone precursor by an isoprenyl diphosphate synthase-related terpene synthase in the harlequin bug
Author(s):		Lancaster J; Khrimian A; Young S; Lehner B; Luck K; Wallingford A; Ghosh SKB; Zerbe P; Muchlinski A; Marek PE; Sparks ME; Tokuhisa JG; Tittiger C; Kollner TG; Weber DC; Gundersen-Rindal DE; Kuhar TP; Tholl D;
Address:		"Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061. Invasive Insect Biocontrol and Behavior Laboratory, Agricultural Research Service, US Department of Agriculture, Beltsville, MD 20705. Department of Biochemistry and Molecular Biology, University of Nevada, Reno, NV 89557. Department of Biochemistry, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany. Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061. Department of Plant Biology, University of California, Davis, CA 95616. Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061. Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; tholl@vt.edu"
Journal Title:		Proc Natl Acad Sci U S A
Year:		2018
Volume:		20180823
Issue:		37
Page Number:		E8634 - E8641
DOI:		10.1073/pnas.1800008115
ISSN/ISBN:		1091-6490 (Electronic) 0027-8424 (Print) 0027-8424 (Linking)
Abstract:		"Insects 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 (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 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"
Keywords:		"Alkyl and Aryl Transferases/classification/genetics/*metabolism Animals Biosynthetic Pathways/genetics Heteroptera/enzymology/genetics/*metabolism Insect Proteins/chemistry/genetics/*metabolism Male Models, Molecular Molecular Structure Pheromones/chemist;"
Notes:		"MedlineLancaster, Jason Khrimian, Ashot Young, Sharon Lehner, Bryan Luck, Katrin Wallingford, Anna Ghosh, Saikat Kumar B Zerbe, Philipp Muchlinski, Andrew Marek, Paul E Sparks, Michael E Tokuhisa, James G Tittiger, Claus Kollner, Tobias G Weber, Donald C Gundersen-Rindal, Dawn E Kuhar, Thomas P Tholl, Dorothea eng Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. 2018/08/25 Proc Natl Acad Sci U S A. 2018 Sep 11; 115(37):E8634-E8641. doi: 10.1073/pnas.1800008115. Epub 2018 Aug 23"