title: A Physiological and Behavioral Mechanism for Leaf Herbivore-Induced Systemic Root Resistance.
abstract: Indirect plant-mediated interactions between herbivores are important drivers of community composition in terrestrial ecosystems. Among the most striking examples are the strong indirect interactions between spatially separated leaf- and root-feeding insects sharing a host plant. Although leaf feeders generally reduce the performance of root herbivores, little is known about the underlying systemic changes in root physiology and the associated behavioral responses of the root feeders. We investigated the consequences of maize (Zea mays) leaf infestation by Spodoptera littoralis caterpillars for the root-feeding larvae of the beetle Diabrotica virgifera virgifera, a major pest of maize. D. virgifera strongly avoided leaf-infested plants by recognizing systemic changes in soluble root components. The avoidance response occurred within 12 h and was induced by real and mimicked herbivory, but not wounding alone. Roots of leaf-infested plants showed altered patterns in soluble free and soluble conjugated phenolic acids. Biochemical inhibition and genetic manipulation of phenolic acid biosynthesis led to a complete disappearance of the avoidance response of D. virgifera. Furthermore, bioactivity-guided fractionation revealed a direct link between the avoidance response of D. virgifera and changes in soluble conjugated phenolic acids in the roots of leaf-attacked plants. Our study provides a physiological mechanism for a behavioral pattern that explains the negative effect of leaf attack on a root-feeding insect. Furthermore, it opens up the possibility to control D. virgifera in the field by genetically mimicking leaf herbivore-induced changes in root phenylpropanoid patterns.
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.) matthias.erb@ips.unibe.ch.
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: Christelle A M
authors.initials: CA
authors.lastname: Robert
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: Guillaume
authors.initials: G
authors.lastname: Marti
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: Jing
authors.initials: J
authors.lastname: Lu
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: Gwladys R
authors.initials: GR
authors.lastname: Doyen
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: Neil
authors.initials: N
authors.lastname: Villard
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: Yves
authors.initials: Y
authors.lastname: Barrière
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: B Wade
authors.identifier: http://orcid.org/0000-0002-8017-5024
authors.initials: BW
authors.lastname: French
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: Jean-Luc
authors.initials: JL
authors.lastname: Wolfender
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: Ted C J
authors.initials: TC
authors.lastname: Turlings
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland (M.E., C.A.M.R.);Root-Herbivore Interactions Group, Department of Biochemistry (M.E., C.A.M.R., J.L.), and Department of Biochemistry (J.G.), Max Planck Institute for Chemical Ecology, DE-07745 Jena, Germany;Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, CH-2009 Neuchatel, Switzerland (M.E., C.A.M.R., G.R.D., N.V., T.C.J.T.);Phytochemistry and Bioactive Natural Products, School of Pharmaceutical Sciences, University of Geneva, University of Lausanne, CH-1211 Geneva 4, Switzerland (G.M., J.-L.W.);Unité de Génétique et d'Amélioration des Plantes Fourragères, INRA, 86600 Lusignan, France (Y.B.); andUnited States Department of Agriculture, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, South Dakota 57006 (B.W.F.).
authors.forename: Jonathan
authors.identifier: http://orcid.org/0000-0002-1812-1551
authors.initials: J
authors.lastname: Gershenzon
mesh_terms: D000818:Animals; D001362:Avoidance Learning / Q000502:physiology*; D002851:Chromatography, High Pressure Liquid; D001517:Coleoptera / Q000502:physiology*; D017753:Ecosystem; D005247:Feeding Behavior / Q000502:physiology; D005838:Genotype; D060434:Herbivory / Q000502:physiology*; D006790:Host-Parasite Interactions; D007814:Larva / Q000502:physiology; D013058:Mass Spectrometry / Q000379:methods; D009154:Mutation; D010636:Phenols / Q000378:metabolism; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism / Q000469:parasitology*; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism / Q000469:parasitology*; D018411:Spodoptera / Q000502:physiology*; D003313:Zea mays / Q000235:genetics / Q000378:metabolism / Q000469:parasitology
chemical_list: D010636:Phenols