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PLANT CELL 19 (3): 1096-1122

Copyright © 2007 by the American Society of Plant Physiologists.

Herbivory Rapidly Activates MAPK Signaling in Attacked and Unattacked Leaf Regions but Not between Leaves of Nicotiana attenuata[W]

Jianqiang Wu, Christian Hettenhausen, Stefan Meldau, and Ian T. Baldwin1

Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, D-07745 Jena, Germany

1 To whom correspondence should be addressed. E-mail baldwin{at}; fax 49-3641-571102.

Abstract: Mitogen-activated protein kinase (MAPK) signaling plays a central role in transducing extracellular stimuli into intracellular responses, but its role in mediating plant responses to herbivore attack remains largely unexplored. When Manduca sexta larvae attack their host plant, Nicotiana attenuata, the plant's wound response is reconfigured at transcriptional, phytohormonal, and defensive levels due to the introduction of oral secretions (OS) into wounds during feeding. We show that OS dramatically amplify wound-induced MAPK activity and that fatty acid–amino acid conjugates in M. sexta OS are the elicitors. Virus-induced gene silencing of salicylic acid–induced protein kinase (SIPK) and wound-induced protein kinase revealed their importance in mediating wound and OS-elicited hormonal responses and transcriptional regulation of defense-related genes. We found that after applying OS to wounds created in one portion of a leaf, SIPK is activated in both wounded and specific unwounded regions of the leaf but not in phylotactically connected adjacent leaves. We propose that M. sexta attack elicits a mobile signal that travels to nonwounded regions of the attacked leaf where it activates MAPK signaling and, thus, downstream responses; subsequently, a different signal is transported by the vascular system to systemic leaves to initiate defense responses without activating MAPKs in systemic leaves.

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   Abstract »    Full Text »    PDF »
The HERBIVORE ELICITOR-REGULATED1 Gene Enhances Abscisic Acid Levels and Defenses against Herbivores in Nicotiana attenuata Plants.
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Plant Physiology 162, 2106-2124
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Dimethyl Disulfide Produced by the Naturally Associated Bacterium Bacillus sp B55 Promotes Nicotiana attenuata Growth by Enhancing Sulfur Nutrition.
D. G. Meldau, S. Meldau, L. H. Hoang, S. Underberg, H. Wunsche, and I. T. Baldwin (2013)
PLANT CELL 25, 2731-2747
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Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany.
C. Wasternack and B. Hause (2013)
Ann. Bot. 111, 1021-1058
   Abstract »    Full Text »    PDF »
Transcriptome Analysis of WIPK/SIPK-Suppressed Plants Reveals Induction by Wounding of Disease Resistance-Related Genes Prior to the Accumulation of Salicylic Acid.
S. Katou, N. Asakura, T. Kojima, I. Mitsuhara, and S. Seo (2013)
Plant Cell Physiol. 54, 1005-1015
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Deciphering Herbivory-Induced Gene-to-Metabolite Dynamics in Nicotiana attenuata Tissues Using a Multifactorial Approach.
J. Gulati, S.-G. Kim, I. T. Baldwin, and E. Gaquerel (2013)
Plant Physiology 162, 1042-1059
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Honing in on phenotypes: comprehensive two-dimensional gas chromatography of herbivory-induced volatile emissions and novel opportunities for system-level analyses.
E. Gaquerel and I. T. Baldwin (2013)
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ML3: a novel regulator of herbivory-induced responses in Arabidopsis thaliana.
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J. Exp. Bot. 64, 935-948
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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
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HSPRO Controls Early Nicotiana attenuata Seedling Growth during Interaction with the Fungus Piriformospora indica.
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Silencing Nicotiana attenuata Calcium-Dependent Protein Kinases, CDPK4 and CDPK5, Strongly Up-Regulates Wound- and Herbivory-Induced Jasmonic Acid Accumulations.
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Silencing MPK4 in Nicotiana attenuata Enhances Photosynthesis and Seed Production But Compromises Abscisic Acid-Induced Stomatal Closure and Guard Cell-Mediated Resistance to Pseudomonas syringae pv tomato DC3000.
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The Chloroplast-Localized Phospholipases D {alpha}4 and {alpha}5 Regulate Herbivore-Induced Direct and Indirect Defenses in Rice.
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Nicotiana attenuata LECTIN RECEPTOR KINASE1 Suppresses the Insect-Mediated Inhibition of Induced Defense Responses during Manduca sexta Herbivory.
P. A. Gilardoni, C. Hettenhausen, I. T. Baldwin, and G. Bonaventure (2011)
PLANT CELL 23, 3512-3532
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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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Lipase Activity in Insect Oral Secretions Mediates Defense Responses in Arabidopsis.
M. Schafer, C. Fischer, S. Meldau, E. Seebald, R. Oelmuller, and I. T. Baldwin (2011)
Plant Physiology 156, 1520-1534
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The Bphi008a Gene Interacts with the Ethylene Pathway and Transcriptionally Regulates MAPK Genes in the Response of Rice to Brown Planthopper Feeding.
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Plant Physiology 156, 856-872
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Two mitogen-activated protein kinase kinases, MKK1 and MEK2, are involved in wounding- and specialist lepidopteran herbivore Manduca sexta-induced responses in Nicotiana attenuata.
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BAK1 regulates the accumulation of jasmonic acid and the levels of trypsin proteinase inhibitors in Nicotiana attenuata's responses to herbivory.
D.-H. Yang, C. Hettenhausen, I. T. Baldwin, and J. Wu (2011)
J. Exp. Bot. 62, 641-652
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Variation in Antiherbivore Defense Responses in Synthetic Nicotiana Allopolyploids Correlates with Changes in Uniparental Patterns of Gene Expression.
S. Anssour and I. T. Baldwin (2010)
Plant Physiology 153, 1907-1918
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Jasmonic Acid and Ethylene Modulate Local Responses to Wounding and Simulated Herbivory in Nicotiana attenuata Leaves.
N. Onkokesung, I. Galis, C. C. von Dahl, K. Matsuoka, H.-P. Saluz, and I. T. Baldwin (2010)
Plant Physiology 153, 785-798
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R2R3-NaMYB8 Regulates the Accumulation of Phenylpropanoid-Polyamine Conjugates, Which Are Essential for Local and Systemic Defense against Insect Herbivores in Nicotiana attenuata.
H. Kaur, N. Heinzel, M. Schottner, I. T. Baldwin, and I. Galis (2010)
Plant Physiology 152, 1731-1747
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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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Nicotiana attenuata SIPK, WIPK, NPR1, and Fatty Acid-Amino Acid Conjugates Participate in the Induction of Jasmonic Acid Biosynthesis by Affecting Early Enzymatic Steps in the Pathway.
M. Kallenbach, F. Alagna, I. T. Baldwin, and G. Bonaventure (2010)
Plant Physiology 152, 96-106
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Transcriptomic profiling of heat-stress response in potato periderm.
I. Ginzberg, G. Barel, R. Ophir, E. Tzin, Z. Tanami, T. Muddarangappa, W. de Jong, and E. Fogelman (2009)
J. Exp. Bot. 60, 4411-4421
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Pectin methylesterase NaPME1 contributes to the emission of methanol during insect herbivory and to the elicitation of defence responses in Nicotiana attenuata.
E. Korner, C. C. von Dahl, G. Bonaventure, and I. T. Baldwin (2009)
J. Exp. Bot. 60, 2631-2640
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Different Lepidopteran Elicitors Account for Cross-Talk in Herbivory-Induced Phytohormone Signaling.
C. Diezel, C. C. von Dahl, E. Gaquerel, and I. T. Baldwin (2009)
Plant Physiology 150, 1576-1586
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Silencing the Hydroxyproline-Rich Glycopeptide Systemin Precursor in Two Accessions of Nicotiana attenuata Alters Flower Morphology and Rates of Self-Pollination.
B. Berger and I. T. Baldwin (2009)
Plant Physiology 149, 1690-1700
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Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphigidae) and Its Natural Host Nicotiana attenuata. VIII. An Unbiased GCxGC-ToFMS Analysis of the Plant's Elicited Volatile Emissions.
E. Gaquerel, A. Weinhold, and I. T. Baldwin (2009)
Plant Physiology 149, 1408-1423
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Induced Plant Defenses in the Natural Environment: Nicotiana attenuata WRKY3 and WRKY6 Coordinate Responses to Herbivory.
M. Skibbe, N. Qu, I. Galis, and I. T. Baldwin (2008)
PLANT CELL 20, 1984-2000
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RNA-Directed RNA Polymerase3 from Nicotiana attenuata Is Required for Competitive Growth in Natural Environments.
S. P. Pandey, E. Gaquerel, K. Gase, and I. T. Baldwin (2008)
Plant Physiology 147, 1212-1224
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Plant Defense Priming against Herbivores: Getting Ready for a Different Battle.
C. J. Frost, M. C. Mescher, J. E. Carlson, and C. M. De Moraes (2008)
Plant Physiology 146, 818-824
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Recognition of Herbivory-Associated Molecular Patterns.
A. Mithofer and W. Boland (2008)
Plant Physiology 146, 825-831
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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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A Comparison of Two Nicotiana attenuata Accessions Reveals Large Differences in Signaling Induced by Oral Secretions of the Specialist Herbivore Manduca sexta.
J. Wu, C. Hettenhausen, M. C. Schuman, and I. T. Baldwin (2008)
Plant Physiology 146, 927-939
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Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences.
M. R Kant, M. W Sabelis, M. A Haring, and R. C Schuurink (2008)
Proc R Soc B 275, 443-452
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Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects.
P. K. Kandoth, S. Ranf, S. S. Pancholi, S. Jayanty, M. D. Walla, W. Miller, G. A. Howe, D. E. Lincoln, and J. W. Stratmann (2007)
PNAS 104, 12205-12210
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