A Physiological and Behavioral Mechanism for Leaf Herbivore-Induced Systemic Root Resistance1[OPEN]

Leaf herbivore attack changes free and conjugated phenolic acids in maize roots and thereby triggers an avoidance response in a specialist root herbivore. Indirect plant-mediated interactions between herbivores are important drivers of community composition in terrestrial ecosystems. Among the most...

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Published in:Plant physiology (Bethesda) 2015-10, Vol.169 (4), p.2884-2894
Main Authors: Erb, Matthias, Robert, Christelle A.M., Marti, Guillaume, Lu, Jing, Doyen, Gwladys R., Villard, Neil, Barrière, Yves, French, B. Wade, Wolfender, Jean-Luc, Turlings, Ted C.J., Gershenzon, Jonathan
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container_title Plant physiology (Bethesda)
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creator Erb, Matthias
Robert, Christelle A.M.
Marti, Guillaume
Lu, Jing
Doyen, Gwladys R.
Villard, Neil
Barrière, Yves
French, B. Wade
Wolfender, Jean-Luc
Turlings, Ted C.J.
Gershenzon, Jonathan
description Leaf herbivore attack changes free and conjugated phenolic acids in maize roots and thereby triggers an avoidance response in a specialist root herbivore. 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.
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Wade</creatorcontrib><creatorcontrib>Wolfender, Jean-Luc</creatorcontrib><creatorcontrib>Turlings, Ted C.J.</creatorcontrib><creatorcontrib>Gershenzon, Jonathan</creatorcontrib><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Erb, Matthias</au><au>Robert, Christelle A.M.</au><au>Marti, Guillaume</au><au>Lu, Jing</au><au>Doyen, Gwladys R.</au><au>Villard, Neil</au><au>Barrière, Yves</au><au>French, B. Wade</au><au>Wolfender, Jean-Luc</au><au>Turlings, Ted C.J.</au><au>Gershenzon, Jonathan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Physiological and Behavioral Mechanism for Leaf Herbivore-Induced Systemic Root Resistance1[OPEN]</atitle><jtitle>Plant physiology (Bethesda)</jtitle><date>2015-10-01</date><risdate>2015</risdate><volume>169</volume><issue>4</issue><spage>2884</spage><epage>2894</epage><pages>2884-2894</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><notes>Present address: Institute of Insect Sciences, Zijingang Campus, Zhejiang University, Hangzhou 310058, China.</notes><notes>These authors contributed equally to the article.</notes><notes>Present address: Faculté de Pharmacie-Université Paul Sabatier-Toulouse III, UMR-152 IRD-UPS, Chemin des Maraichers, 31400 Toulouse, France.</notes><notes>M.E. conceived the project; M.E., C.A.M.R., and G.M. planned the experiments; C.A.M.R., G.M., M.E., G.R.D., J.L., and N.V. performed the experiments; M.E., J.-L.W., T.C.J.T., J.G., and C.A.M.R. supervised the experiments; B.W.F. and Y.B. provided technical assistance; M.E., C.A.M.R., G.M., and G.D. analyzed the data; M.E. wrote the article with contributions of all the authors.</notes><notes>The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Matthias Erb (matthias.erb@ips.unibe.ch).</notes><notes>www.plantphysiol.org/cgi/doi/10.1104/pp.15.00759</notes><abstract>Leaf herbivore attack changes free and conjugated phenolic acids in maize roots and thereby triggers an avoidance response in a specialist root herbivore. 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.</abstract><pub>American Society of Plant Biologists</pub><pmid>26430225</pmid><doi>10.1104/pp.15.00759</doi></addata></record>
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title A Physiological and Behavioral Mechanism for Leaf Herbivore-Induced Systemic Root Resistance1[OPEN]
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