title: Differential Costs of Two Distinct Resistance Mechanisms Induced by Different Herbivore Species in Arabidopsis.
abstract: Plants respond to herbivory with the induction of resistance, mediated by distinct phytohormonal signaling pathways and their interactions. Phloem feeders are known to induce plant resistance via the salicylic acid pathway, whereas biting-chewing herbivores induce plant resistance mainly via the jasmonate pathway. Here, we show that a specialist caterpillar (biting-chewing herbivore) and a specialist aphid (phloem feeder) differentially induce resistance against Pieris brassicae caterpillars in Arabidopsis (Arabidopsis thaliana) plants. Caterpillar feeding induces resistance through the jasmonate signaling pathway that is associated with the induction of kaempferol 3,7-dirhamnoside, whereas aphid feeding induces resistance via a novel mechanism involving sinapoyl malate. The role of sinapoyl malate is confirmed through the use of a mutant compromised in the biosynthesis of this compound. Caterpillar-induced resistance is associated with a lower cost in terms of plant growth reduction than aphid-induced resistance. A strong constitutive resistance against P. brassicae caterpillars in combination with a strong growth attenuation in plants of a transfer DNA (T-DNA) insertion mutant of WRKY70 (wrky70) suggest that the WRKY70 transcription factor, a regulator of downstream responses mediated by jasmonate-salicylic acid signaling cross talk, is involved in the negative regulation of caterpillar resistance and in the tradeoff between growth and defense. In conclusion, different mechanisms of herbivore-induced resistance come with different costs, and a functional WRKY70 transcription factor is required for the induction of low-cost resistance.
authors.affiliation: Laboratory of Entomology, Wageningen University, 6700AA Wageningen, The Netherlands (N.O., M.D.);Department of Biochemistry, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.R.);Keygene, 6708OW, Wageningen, The Netherlands (A.v.D.); andPlant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH Amsterdam, The Netherlands (A.v.D., R.C.S.).
authors.forename: Nawaporn
authors.identifier: http://orcid.org/0000-0002-5094-5788
authors.initials: N
authors.lastname: Onkokesung
authors.affiliation: Laboratory of Entomology, Wageningen University, 6700AA Wageningen, The Netherlands (N.O., M.D.);Department of Biochemistry, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.R.);Keygene, 6708OW, Wageningen, The Netherlands (A.v.D.); andPlant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH Amsterdam, The Netherlands (A.v.D., R.C.S.).
authors.forename: Michael
authors.initials: M
authors.lastname: Reichelt
authors.affiliation: Laboratory of Entomology, Wageningen University, 6700AA Wageningen, The Netherlands (N.O., M.D.);Department of Biochemistry, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.R.);Keygene, 6708OW, Wageningen, The Netherlands (A.v.D.); andPlant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH Amsterdam, The Netherlands (A.v.D., R.C.S.).
authors.forename: Arjen
authors.initials: A
authors.lastname: van Doorn
authors.affiliation: Laboratory of Entomology, Wageningen University, 6700AA Wageningen, The Netherlands (N.O., M.D.);Department of Biochemistry, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.R.);Keygene, 6708OW, Wageningen, The Netherlands (A.v.D.); andPlant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH Amsterdam, The Netherlands (A.v.D., R.C.S.).
authors.forename: Robert C
authors.initials: RC
authors.lastname: Schuurink
authors.affiliation: Laboratory of Entomology, Wageningen University, 6700AA Wageningen, The Netherlands (N.O., M.D.);Department of Biochemistry, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.R.);Keygene, 6708OW, Wageningen, The Netherlands (A.v.D.); andPlant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098XH Amsterdam, The Netherlands (A.v.D., R.C.S.) marcel.dicke@wur.nl.
authors.forename: Marcel
authors.identifier: http://orcid.org/0000-0001-8565-8896
authors.initials: M
authors.lastname: Dicke
mesh_terms: D000818:Animals; D001042:Aphids / Q000502:physiology; D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000469:parasitology*; D029681:Arabidopsis Proteins / Q000378:metabolism; D018533:Biomass; D053898:Biosynthetic Pathways / Q000235:genetics; D003517:Cyclopentanes / Q000378:metabolism; D060467:Disease Resistance; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D005961:Glucosinolates / Q000378:metabolism; D060434:Herbivory / Q000502:physiology*; D044949:Kaempferols / Q000378:metabolism; D007814:Larva / Q000502:physiology; D008293:Malates / Q000378:metabolism; D054883:Oxylipins / Q000378:metabolism; D010666:Phenylpropionates / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D020156:Salicylic Acid / Q000378:metabolism; D015398:Signal Transduction; D014157:Transcription Factors / Q000378:metabolism
chemical_list: C079164:2-O-sinapoylmalate; D029681:Arabidopsis Proteins; D003517:Cyclopentanes; D005961:Glucosinolates; D044949:Kaempferols; D008293:Malates; D054883:Oxylipins; D010666:Phenylpropionates; D012333:RNA, Messenger; D014157:Transcription Factors; C487183:WRKY70 protein, Arabidopsis; C011006:jasmonic acid; D020156:Salicylic Acid; C042728:lespenefril