A physiological and behavioral mechanism for leaf-herbivore induced systemic root resistance

Authors: ERB, MATTHIAS - University Of Bern; MARTI, GUILLAUME - University Of Geneva; ROBERT, CHRISTELLE - University Of Neuchatel; LU, JING - Max Planck Institute For Biogeochemistry; DOYEN, GWLADYS R. - University Of Neuchatel; VILLARD, NEIL - University Of Neuchatel; BARRIERE, YVES - Inra, Génétique Animale Et Biologie Intégrative , Jouy-En-josas, France; French, Bryan; WOLFENDER, JEAN-LUC - University Of Geneva; TURLINGS, TED C. - University Of Neuchatel

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/9/2015
Publication Date: 12/1/2015
Citation: Erb, M., Marti, G., Robert, C., Lu, J., Doyen, G., Villard, N., Barriere, Y., French, B.W., Wolfender, J., Turlings, T.J. 2015. A physiological and behavioral mechanism for leaf-herbivore induced systemic root resistance. Plant Physiology. 169: 2884-2894.

Interpretive Summary: Indirect plant-mediated interactions between herbivores, such as those between spatially separated leaf and root feeding insects sharing a host plant, are important drivers of community composition in terrestrial ecosystems. Although it is widely known that leaf-feeding insects often reduce the impact of root-feeding insects, little is known about the underlying systemic changes in root physiology and the associated behavioral responses of the root feeders. Here, we report the behavioral effects of a caterpillar feeding on corn leaves on the root-feeding beetle larvae of the western corn rootworm (WCR), a major pest of corn. WCR strongly avoided leaf-infested plants by recognizing physiological changes in soluble root components. The avoidance response occurred within 1 hour 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 WCR larvae. In addition, bioactivity guided fractionation revealed a direct link between the avoidance response of WCR 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. It also opens up the possibility to reduce WCR populations in the field by genetically mimicking leaf-herbivore induced changes in root phenylpropanoid patterns.

Technical 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 leaf-infestation by Spodoptera littoralis caterpillars for the root-feeding larvae of the beetle Diabrotica virgifera, a major pest of maize. Diabrotica virgifera strongly avoided leaf-infested plants by recognizing systemic changes in soluble root components. The avoidance response occurred within 1 hours 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 which 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.