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A novel sex-specific and inducible monoterpene synthase activity associated with a pine bark beetle, the pine engraver, Ips pini

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Abstract

Ecological interactions of conifers and coniferophagous bark beetles are determined in part by terpenoids (isoprenoids), which are major defense metabolites of conifer oleoresin. Curiously, similar compounds are important aggregation pheromones of conifer-attacking bark beetles. Terpene synthases are responsible for generating the enormous variety of terpenoid carbon skeletons found in nature. These catalysts convert short-chain prenyl diphosphates to a diverse assortment of hemiterpene, monoterpene, sesquiterpene, and diterpene natural products. While terpene synthases have frequently been characterized from plant and microbial sources, they have not yet been described in animals. Here we report the discovery of a monoterpene synthase activity in an insect, the pine engraver, Ips pini (Say) (Coleoptera: Scolytidae). Cell-free assays of I. pini revealed that geranyl diphosphate (GDP) is converted to the acyclic monoterpene myrcene in whole-body extracts from males, but not females. Furthermore, the monoterpene synthase activity in males can be induced by prior treatment with juvenile hormone III (JH III) or by feeding on phloem from the host trees, Jeffrey pine (Pinus jeffreyi Grev. & Balf.) or red pine (Pinus resinosa Ait.). The sex-specificity and endocrine induction of this activity argue for its involvement in the biosynthesis of monoterpenoid pheromones mediated by enzymes from insect tissue. This discovery is the first example of a monoterpene synthase in the Metazoa and evokes exciting new questions about the origin, evolution, and occurrence of terpene synthases.

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Acknowledgements

This work was supported by grants No. 97-35302-4223 and No. 98-35302-6997 from the United States Department of Agriculture NRI-CGP and the University of Minnesota Grant-In-Aid Program (to S.J.S.), by a research grant from the Natural Sciences and Engineering Research Council (NSERC) of Canada (to J.B.), by grant RGY0382 from the Human Frontier Science Program (HFSP) (to S.J.S. and J.B.), and funds from the Max Planck Society (to J.G.). We thank B.D. Ayres (Woods Run Forest Products, Colfax, Wis.), F. Lu (University of Nevada, Reno), E.J. Gartrell (University of Minnesota), S.L. Smith and R. Peterson (USDA Forest Service, Susanville, Calif.) and W.R. McNee and D.L. Wood (University of California at Berkeley) for technical assistance, and J.A. Tillman (University of Minnesota) for drafting the graphics.

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Author notes

  1. Steven J. Seybold

    Present address: Chemical Ecology of Forest Insects, USDA Forest Service Pacific Southwest Research Station, 720 Olive Drive Suite D, Davis, CA 95616, USA

Authors and Affiliations

  1. Biotechnology Laboratory and Departments of Botany and Forest Sciences, University of British Columbia, 6174 University Boulevard, Vancouver, BC, V6T 1Z3, Canada

    Diane Martin & Jörg Bohlmann

  2. Max-Planck-Institut für Chemische Oekologie, Winzerlaer Strasse 10, 07745, Jena, Germany

    Diane Martin, Jörg Bohlmann & Jonathan Gershenzon

  3. Institut für Organische Chemie, Universität Hamburg, Martin-Luther-King-Platz 6, 20146, Hamburg, Germany

    Wittko Francke

  4. Departments of Entomology and Forest Resources, University of Minnesota, 219 Hodson Hall, 1980 Folwell Avenue, St. Paul, MN 55108-6125, USA

    Steven J. Seybold

Authors
  1. Diane Martin
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  2. Jörg Bohlmann
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  4. Wittko Francke
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Correspondence to Steven J. Seybold.

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J. Bohlmann and S.J. Seybold contributed equally to this study as senior investigators.

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Martin, D., Bohlmann, J., Gershenzon, J. et al. A novel sex-specific and inducible monoterpene synthase activity associated with a pine bark beetle, the pine engraver, Ips pini . Naturwissenschaften 90, 173–179 (2003). https://doi.org/10.1007/s00114-003-0410-y

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