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Science 305 (5684): 665-668

Copyright © 2004 by the American Association for the Advancement of Science

Silencing the Jasmonate Cascade: Induced Plant Defenses and Insect Populations

André Kessler, Rayko Halitschke, Ian T. Baldwin*

Abstract: We transformed the native tobacco, Nicotiana attenuata, to silence its lipoxygenase, hydroperoxide lyase, and allene oxide synthase genes in order to inhibit oxylipin signaling, known to mediate the plant's direct and indirect defenses. When planted into native habitats, lipoxygenase-deficient plants were more vulnerable to N. attenuata's adapted herbivores but also attracted novel herbivore species, which fed and reproduced successfully. In addition to highlighting the value of genetically silencing plants to study ecological interactions in nature, these results show that lipoxygenase-dependent signaling determines host selection for opportunistic herbivores and that induced defenses influence herbivore community composition.

Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, Hans-Knöll-Strasse 8, Jena 07745, Germany.

* To whom correspondence should be addressed. E-mail: baldwin{at}

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Terpene Down-Regulation Triggers Defense Responses in Transgenic Orange Leading to Resistance against Fungal Pathogens.
A. Rodriguez, T. Shimada, M. Cervera, B. Alquezar, J. Gadea, A. Gomez-Cadenas, C. J. De Ollas, M. J. Rodrigo, L. Zacarias, and L. Pena (2014)
Plant Physiology 164, 321-339
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Structure and interaction with phospholipids of a prokaryotic lipoxygenase from Pseudomonas aeruginosa.
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FASEB J 27, 4811-4821
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Pathogen-Triggered Ethylene Signaling Mediates Systemic-Induced Susceptibility to Herbivory in Arabidopsis.
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Disarming the Jasmonate-Dependent Plant Defense Makes Nonhost Arabidopsis Plants Accessible to the American Serpentine Leafminer.
H. Abe, K. Tateishi, S. Seo, S. Kugimiya, M. Y. Hirai, Y. Sawada, Y. Murata, K. Yara, T. Shimoda, and M. Kobayashi (2013)
Plant Physiology 163, 1242-1253
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The HERBIVORE ELICITOR-REGULATED1 Gene Enhances Abscisic Acid Levels and Defenses against Herbivores in Nicotiana attenuata Plants.
S. T. Dinh, I. T. Baldwin, and I. Galis (2013)
Plant Physiology 162, 2106-2124
   Abstract »    Full Text »    PDF »
Negative Feedback Control of Jasmonate Signaling by an Alternative Splice Variant of JAZ10.
J. E. Moreno, C. Shyu, M. L. Campos, L. C. Patel, H. S. Chung, J. Yao, S. Y. He, and G. A. Howe (2013)
Plant Physiology 162, 1006-1017
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E. Gaquerel and I. T. Baldwin (2013)
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   Abstract »    Full Text »    PDF »
Herbivore induction of jasmonic acid and chemical defences reduce photosynthesis in Nicotiana attenuata.
P. D. Nabity, J. A. Zavala, and E. H. DeLucia (2013)
J. Exp. Bot. 64, 685-694
   Abstract »    Full Text »    PDF »
Alternative Oxidase in Resistance to Biotic Stresses: Nicotiana attenuata AOX Contributes to Resistance to a Pathogen and a Piercing-Sucking Insect But Not Manduca sexta Larvae.
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Plant Physiology 160, 1453-1467
   Abstract »    Full Text »    PDF »
Community Ecology and the Evolution of Molecules of Keystone Significance.
R. P. Ferrer and R. K. Zimmer (2012)
Biol. Bull. 223, 167-177
   Abstract »    Full Text »    PDF »
Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations.
M. Kallenbach, G. Bonaventure, P. A. Gilardoni, A. Wissgott, and I. T. Baldwin (2012)
PNAS 109, E1548-E1557
   Abstract »    Full Text »    PDF »
Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature.
M. C. Schuman, K. Barthel, and I. T. Baldwin (2012)
eLife Sci 1, e00007
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Microbiology 158, 155-165
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Insect oral secretions suppress wound-induced responses in Arabidopsis.
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J. Exp. Bot. 63, 727-737
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The Chloroplast-Localized Phospholipases D {alpha}4 and {alpha}5 Regulate Herbivore-Induced Direct and Indirect Defenses in Rice.
J. Qi, G. Zhou, L. Yang, M. Erb, Y. Lu, X. Sun, J. Cheng, and Y. Lou (2011)
Plant Physiology 157, 1987-1999
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Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis.
A. Sugio, H. N. Kingdom, A. M. MacLean, V. M. Grieve, and S. A. Hogenhout (2011)
PNAS 108, E1254-E1263
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S-Nitrosoglutathione reductase (GSNOR) mediates the biosynthesis of jasmonic acid and ethylene induced by feeding of the insect herbivore Manduca sexta and is important for jasmonate-elicited responses in Nicotiana attenuata.
H. Wunsche, I. T. Baldwin, and J. Wu (2011)
J. Exp. Bot. 62, 4605-4616
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Community genetics: what have we accomplished and where should we be going?.
E. I. Hersch-Green, N. E. Turley, and M. T. J. Johnson (2011)
Phil Trans R Soc B 366, 1453-1460
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PNAS 108, 5891-5896
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Pithy Protection: Nicotiana attenuata's Jasmonic Acid-Mediated Defenses Are Required to Resist Stem-Boring Weevil Larvae.
C. Diezel, D. Kessler, and I. T. Baldwin (2011)
Plant Physiology 155, 1936-1946
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Serine Protease Inhibitors Specifically Defend Solanum nigrum against Generalist Herbivores but Do Not Influence Plant Growth and Development.
M. Hartl, A. P. Giri, H. Kaur, and I. T. Baldwin (2010)
PLANT CELL 22, 4158-4175
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Natural variation in herbivore-induced volatiles in Arabidopsis thaliana.
T. A. L. Snoeren, I. F. Kappers, C. Broekgaarden, R. Mumm, M. Dicke, and H. J. Bouwmeester (2010)
J. Exp. Bot. 61, 3041-3056
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Intraspecific variation in herbivore community composition and transcriptional profiles in field-grown Brassica oleracea cultivars.
C. Broekgaarden, E. H. Poelman, R. E. Voorrips, M. Dicke, and B. Vosman (2010)
J. Exp. Bot. 61, 807-819
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Jasmonate-Dependent and -Independent Pathways Mediate Specific Effects of Solar Ultraviolet B Radiation on Leaf Phenolics and Antiherbivore Defense.
P. V. Demkura, G. Abdala, I. T. Baldwin, and C. L. Ballare (2010)
Plant Physiology 152, 1084-1095
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Jasmonate and ppHsystemin Regulate Key Malonylation Steps in the Biosynthesis of 17-Hydroxygeranyllinalool Diterpene Glycosides, an Abundant and Effective Direct Defense against Herbivores in Nicotiana attenuata.
S. Heiling, M. C. Schuman, M. Schoettner, P. Mukerjee, B. Berger, B. Schneider, A. R. Jassbi, and I. T. Baldwin (2010)
PLANT CELL 22, 273-292
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Positively Selected Disease Response Orthologous Gene Sets in the Cereals Identified Using Sorghum bicolor L. Moench Expression Profiles and Comparative Genomics.
A. Zamora, Q. Sun, M. T. Hamblin, C. F. Aquadro, and S. Kresovich (2009)
Mol. Biol. Evol. 26, 2015-2030
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Spodoptera littoralis-Induced Lectin Expression in Tobacco.
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Plant Cell Physiol. 50, 1142-1155
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J. Exp. Bot. 60, 1231-1240
   Abstract »    Full Text »    PDF »
Jasmonate: Preventing the Maize Tassel from Getting in Touch with His Feminine Side.
J. Browse (2009)
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Detritivorous crustaceans become herbivores on jasmonate-deficient plants.
E. E. Farmer and L. Dubugnon (2009)
PNAS 106, 935-940
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Phytohormone-based activity mapping of insect herbivore-produced elicitors.
E. A. Schmelz, J. Engelberth, H. T. Alborn, J. H. Tumlinson III, and P. E. A. Teal (2009)
PNAS 106, 653-657
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Jasmonate Perception Regulates Jasmonate Biosynthesis and JA-Ile Metabolism: The Case of COI1 in Nicotiana attenuata.
A. Paschold, G. Bonaventure, M. R. Kant, and I. T. Baldwin (2008)
Plant Cell Physiol. 49, 1165-1175
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Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects.
J. A. Zavala, C. L. Casteel, E. H. DeLucia, and M. R. Berenbaum (2008)
PNAS 105, 5129-5133
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Phosphoinositide and Inositolpolyphosphate Signalling in Defense Responses of Arabidopsis thaliana Challenged by Mechanical Wounding.
A. Mosblech, S. Konig, I. Stenzel, P. Grzeganek, I. Feussner, and I. Heilmann (2008)
Mol Plant 1, 249-261
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Ecological Genomics of Plant-Insect Interactions: From Gene to Community.
S.-J. Zheng and M. Dicke (2008)
Plant Physiology 146, 812-817
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New Weapons and a Rapid Response against Insect Attack.
J. Browse and G. A. Howe (2008)
Plant Physiology 146, 832-838
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Why Does Herbivore Attack Reconfigure Primary Metabolism?.
J. Schwachtje and I. T. Baldwin (2008)
Plant Physiology 146, 845-851
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Arthropod-Inducible Proteins: Broad Spectrum Defenses against Multiple Herbivores.
K. Zhu-Salzman, D. S. Luthe, and G. W. Felton (2008)
Plant Physiology 146, 852-858
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Silencing Threonine Deaminase and JAR4 in Nicotiana attenuata Impairs Jasmonic Acid-Isoleucine-Mediated Defenses against Manduca sexta.
J.-H. Kang, L. Wang, A. Giri, and I. T. Baldwin (2006)
PLANT CELL 18, 3303-3320
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SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots.
J. Schwachtje, P. E. H. Minchin, S. Jahnke, J. T. van Dongen, U. Schittko, and I. T. Baldwin (2006)
PNAS 103, 12935-12940
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From The Cover: Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut.
H. Chen, C. G. Wilkerson, J. A. Kuchar, B. S. Phinney, and G. A. Howe (2005)
PNAS 102, 19237-19242
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In Situ Modification of Herbivore-Induced Plant Odors: A Novel Approach to Study the Attractiveness of Volatile Organic Compounds to Parasitic Wasps.
M. D'Alessandro and T. C.J. Turlings (2005)
Chem Senses 30, 739-753
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Genetic Engineering of Terpenoid Metabolism Attracts Bodyguards to Arabidopsis.
I. F. Kappers, A. Aharoni, T. W. J. M. van Herpen, L. L. P. Luckerhoff, M. Dicke, and H. J. Bouwmeester (2005)
Science 309, 2070-2072
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Keeping the Leaves Green Above Us.
A. Gfeller and E. E. Farmer (2004)
Science 306, 1515-1516
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ECOLOGY: Enhanced: Ecogenomics Benefits Community Ecology.
M. Dicke, J. J. A. van Loon, and P. W. de Jong (2004)
Science 305, 618-619
   Abstract »    Full Text »    PDF »

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