ArticlePlant physiology2015
A Physiological and Behavioral Mechanism for Leaf Herbivore-Induced Systemic Root Resistance.
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Article in Plant physiology, 2015. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 17 papers.
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17citing papers in PubMed
8.7field-weighted citation impact, top 2% of its field
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Who cites it
17 citing papers in PubMed, 51 citations in OpenAlex.
- Review
- Contrasting plant transcriptome responses between a pierce-sucking and a chewing herbivore go beyond the infestation site.BMC plant biology · 2024Article
- Leaf herbivory counteracts nematode-triggered repression of jasmonate-related defenses in tomato roots.Plant physiology · 2021Article
- Herbivory-induced systemic signals are likely to be evolutionarily conserved in euphyllophytes.Journal of experimental botany · 2021Article
- Plant-associated COeLife · 2021Article
- The plant metabolome guides fitness-relevant foraging decisions of a specialist herbivore.PLoS biology · 2021Article
- Induced Local and Systemic Defense Responses in Tomato Underlying Interactions Between the Root-Knot NematodeFrontiers in plant science · 2021Article
- Foliar herbivory by caterpillars and aphids differentially affects phytohormonal signalling in roots and plant defence to a root herbivore.Plant, cell & environment · 2020Article
- Article
- Distinct defense strategies allow different grassland species to cope with root herbivore attack.Oecologia · 2019Article
- TheFrontiers in plant science · 2018Article
- A mechanism for sequence specificity in plant-mediated interactions between herbivores.The New phytologist · 2017Article
- A Herbivore Tag-and-Trace System Reveals Contact- and Density-Dependent Repellence of a Root Toxin.Journal of chemical ecology · 2017Article
- Nematode Root Herbivory in Tomato Increases Leaf Defenses and Reduces Leaf Miner Oviposition and Performance.Journal of chemical ecology · 2017Article
- Biological Control beneath the Feet: A Review of Crop Protection against Insect Root Herbivores.Insects · 2016Review
- Intraplant communication in maize contributes to defense against insects.Plant signaling & behavior · 2016Article
- A conserved pattern in plant-mediated interactions between herbivores.Ecology and evolution · 2016Article
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Authors and funding
11 authors at 5 institutions in 3 countries.
Matthias ErbInstitute 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.
Christelle A M RobertInstitute 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.).
Guillaume MartiInstitute 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.).
Jing LuInstitute 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.).
Gwladys R DoyenInstitute 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.).
Neil VillardInstitute 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.).
Yves BarrièreInstitute 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.).
B Wade FrenchInstitute 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.).ORCID http://orcid.org/0000-0002-8017-5024
Jean-Luc WolfenderInstitute 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.).
Ted C J TurlingsInstitute 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.).
Jonathan GershenzonInstitute 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.).ORCID http://orcid.org/0000-0002-1812-1551
Hôpital Lapeyronie · FRNorth Central College · USUnité de Recherche Pluridisciplinaire Prairies et Plantes Fourragères · FRUniversité Toulouse III - Paul Sabatier · FRUniversity of Geneva · CH
Funding
No grant is acknowledged in the PubMed record.
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.
Indexed as
AnimalsAvoidance LearningChromatography, High Pressure LiquidColeopteraEcosystemFeeding BehaviorGenotypeHerbivoryHost-Parasite InteractionsLarvaMass SpectrometryMutationPhenolsPlant LeavesPlant RootsSpodopteraPhenols
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