Restoring a maize root signal that attracts insect-killing nematodes to control a major pest
- Jörg Degenhardta,1,2,
- Ivan Hiltpoldb,1,
- Tobias G. Köllnera,2,
- Monika Freyc,
- Alfons Gierlc,
- Jonathan Gershenzona,
- Bruce E. Hibbardd,
- Mark R. Ellersiecke and
- Ted C. J. Turlingsb,3
- aMax-Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745 Jena, Germany;
- bUniversity of Neuchâtel, Institute of Biology, Fundamental and Applied Research in Chemical Ecology, Case Postale 158, CH-2009 Neuchâtel, Switzerland;
- cLehrstuhl für Genetik, Technische Universität München, Am Hochanger 8, D-85350 Freising, Germany;
- dUnited States Department of Agriculture–Agricultural Research Service Plant Genetics Research Unit, 205 Curtis Hall, University of Missouri, Columbia, MO 65211; and
- eAgricultural Experiment Station, 307E Middlebush Hall, University of Missouri, Columbia, MO 65211
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↵2Present address: Institut für Pharmazie, Martin-Luther-Universität Halle, Hoher Weg 8, D-06120 Halle, Germany.
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Communicated by James H. Tumlinson III, Pennsylvania State University, University Park, PA, June 10, 2009
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↵1J.D. and I.H. contributed equally to this work. (received for review April 10, 2009)
Abstract
When attacked by herbivorous insects, plants emit volatile compounds that attract natural enemies of the insects. It has been proposed that these volatile signals can be manipulated to improve crop protection. Here, we demonstrate the full potential of this strategy by restoring the emission of a specific belowground signal emitted by insect-damaged maize roots. The western corn rootworm induces the roots of many maize varieties to emit (E)-β-caryophyllene, which attracts entomopathogenic nematodes that infect and kill the voracious root pest. However, most North American maize varieties have lost the ability to emit (E)-β-caryophyllene and may therefore receive little protection from the nematodes. To restore the signal, a nonemitting maize line was transformed with a (E)-β-caryophyllene synthase gene from oregano, resulting in constitutive emissions of this sesquiterpene. In rootworm-infested field plots in which nematodes were released, the (E)-β-caryophyllene-emitting plants suffered significantly less root damage and had 60% fewer adult beetles emerge than untransformed, nonemitting lines. This demonstration that plant volatile emissions can be manipulated to enhance the effectiveness of biological control agents opens the way for novel and ecologically sound strategies to fight a variety of insect pests.
Footnotes
- 3To whom correspondence should be addressed. E-mail: ted.turlings{at}unine.ch
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Author contributions: J.D., I.H., M.F., J.G., B.E.H., and T.C.J.T. designed research; J.D., I.H., T.G.K., M.F., and B.E.H. performed research; J.D., M.F., A.G., J.G., B.E.H., and T.C.J.T. contributed new reagents/analytic tools; J.D., I.H., T.G.K., J.G., B.E.H., M.R.E., and T.C.J.T. analyzed data; and J.D., I.H., J.G., B.E.H., and T.C.J.T. wrote the paper.
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Conflict of interest statement: A patent for the transformation with the oregano (E)-β-caryophyllene synthase gene has been filed. Some of the authors and their institutions may financially benefit from this patent.
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This article contains supporting information online at www.pnas.org/cgi/content/full/0906365106/DCSupplemental.
