A specialist root herbivore exploits defensive metabolites to locate nutritious tissues

Authors

  • Christelle A. M. Robert,

    1. University of Neuchâtel, Laboratory for Fundamental and Applied Research in Chemical Ecology (FARCE), Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
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  • Nathalie Veyrat,

    1. University of Neuchâtel, Laboratory for Fundamental and Applied Research in Chemical Ecology (FARCE), Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
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  • Gaétan Glauser,

    1. University of Neuchâtel, Laboratory for Fundamental and Applied Research in Chemical Ecology (FARCE), Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
    2. Chemical Analytical Service of the Swiss Plant Science Web, University of Neuchâtel, Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
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  • Guillaume Marti,

    1. Phytochemistry & Bioactive Natural Products and Pharmacognosy, University of Geneva, Quai Ernest-Ansermet 30, 1211 Geneva, Switzerland
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  • Gwladys R. Doyen,

    1. University of Neuchâtel, Laboratory for Fundamental and Applied Research in Chemical Ecology (FARCE), Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
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  • Neil Villard,

    1. University of Neuchâtel, Laboratory for Fundamental and Applied Research in Chemical Ecology (FARCE), Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
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  • Mickaël D. P. Gaillard,

    1. University of Neuchâtel, Laboratory for Fundamental and Applied Research in Chemical Ecology (FARCE), Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
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  • Tobias G. Köllner,

    1. Department of Biochemistry, Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans-Knöll-Str. 8, 07745 Jena, Germany
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  • David Giron,

    1. Physical Ecology and Multitrophic Interactions Group, Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 6035 UFR Sciences et Techniques, Avenue Monge-Parc Grandmont, 37200 Tours, France
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  • Mélanie Body,

    1. Physical Ecology and Multitrophic Interactions Group, Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 6035 UFR Sciences et Techniques, Avenue Monge-Parc Grandmont, 37200 Tours, France
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  • Benjamin A. Babst,

    1. Medical Department, Brookhaven National Laboratory, Upton, NY 11973, USA
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  • Richard A. Ferrieri,

    1. Medical Department, Brookhaven National Laboratory, Upton, NY 11973, USA
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  • Ted C. J. Turlings,

    1. University of Neuchâtel, Laboratory for Fundamental and Applied Research in Chemical Ecology (FARCE), Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
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  • Matthias Erb

    Corresponding author
    1. University of Neuchâtel, Laboratory for Fundamental and Applied Research in Chemical Ecology (FARCE), Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
    2. Current address: Max Planck Institute for Chemical Ecology, Shoot-Root Communication Group, Hans-Knöll-Str. 8, 07745 Jena, Germany
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E-mail: merb@ice.mpg.de

Abstract

Ecology Letters (2011) 14: 55–64

Abstract

The most valuable organs of plants are often particularly rich in essential elements, but also very well defended. This creates a dilemma for herbivores that need to maximise energy intake while minimising intoxication. We investigated how the specialist root herbivore Diabrotica virgifera solves this conundrum when feeding on wild and cultivated maize plants. We found that crown roots of maize seedlings were vital for plant development and, in accordance, were rich in nutritious primary metabolites and contained higher amounts of the insecticidal 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and the phenolic compound chlorogenic acid. The generalist herbivores Diabrotica balteata and Spodoptera littoralis were deterred from feeding on crown roots, whereas the specialist D. virgifera preferred and grew best on these tissues. Using a 1,4-benzoxazin-3-one-deficient maize mutant, we found that D. virgifera is resistant to DIMBOA and other 1,4-benzoxazin-3-ones and that it even hijacks these compounds to optimally forage for nutritious roots.

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