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Plant Cell, Vol. 11, 273-288, February 1999, Copyright © 1999, American Society of Plant Physiologists
Rapid Avr 9- and Cf-9 –Dependent Activation of MAP Kinases in Tobacco Cell Cultures and Leaves: Convergence of Resistance Gene, Elicitor, Wound, and Salicylate Responses
Tina Romeisa,
Pedro Piedrasa,
Shuqun Zhangb,
Daniel F. Klessigb,
Heribert Hirtc, and
Jonathan D. G. Jonesa
a Sainsbury Laboratory, John Innes Centre, Colney Lane, Norwich NR4 7UH, United Kingdom
b Waksman Institute and Department of Molecular Biology and Biochemistry, Rutgers, The State University of New Jersey, 190 Frelinghuysen Road, Piscataway, New Jersey 08854-8020
c Institute of Microbiology and Genetics, Vienna Biocenter, Dr. Bohrgasse 9, 1030 Vienna, Austria
Correspondence to:
Jonathan D. G. Jones, jonesj{at}bbsrc.ac.uk (E-mail), 44-1603-250024 (fax)
The Cf-9 resistance (R) gene from tomato confers resistance to the fungal pathogen Cladosporium fulvum expressing the corresponding, pathogen-derived avirulence gene product Avr9. To understand how an initial R/Avr recognition event is transmitted and triggers the induction of plant defenses, we investigated early Avr9/Cf-9–dependent activation of protein kinases in transgenic tobacco expressing the Cf-9 gene. We identified two protein kinases of 46 and 48 kD, using myelin basic protein as substrate, that became rapidly activated in a strictly gene-for-gene manner within 2 to 5 min after Avr9 elicitation in both Cf9 tobacco plants and derived cell cultures. Studies with pharmacological inhibitors and effectors revealed that Ca2+ influx and a phosphorylation event(s) are required for kinase activation, but neither enzyme is involved in the Avr9-dependent synthesis of active oxygen species. The activation of both kinases is achieved via post-translational mechanisms, and the activation but not inactivation step includes tyrosine phosphorylation. Using specific antibodies, we found that the 46- and 48-kD kinases were similiar to WIPK (for wound-induced protein kinase) and SIPK (for salicylic acid–induced protein kinase), two previously characterized mitogen-activated protein (MAP) kinases from tobacco. In addition, Cf9 tobacco plants and cell cultures showed an Avr9-dependent accumulation of the WIPK transcript. Cf9 tobacco suspension cultures are thus a unique system in which to analyze the earliest events in R gene function. These data indicate that (1) the R/Avr–mediated induction of plant defense is accomplished via several parallel signaling mechanisms, and (2) R/Avr–dependent signal transduction pathways are interlinked at MAP kinases with responses of plants not only to non-race-specific elicitors but also to abiotic stimuli, such as wounding and mechanical stress.
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S. G. Cessna, V. E. Sears, M. B. Dickman, and P. S. Low
Oxalic Acid, a Pathogenicity Factor for Sclerotinia sclerotiorum, Suppresses the Oxidative Burst of the Host Plant
PLANT CELL,
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S. Kiegerl, F. Cardinale, C. Siligan, A. Gross, E. Baudouin, A. Liwosz, S. Eklöf, S. Till, L. Bögre, H. Hirt, et al.
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M. S. Dixon, C. Golstein, C. M. Thomas, E. A. van der Biezen, and J. D. G. Jones
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D. F. Klessig, J. Durner, R. Noad, D. A. Navarre, D. Wendehenne, D. Kumar, J. M. Zhou, J. Shah, S. Zhang, P. Kachroo, et al.
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A. H. van der Luit, T. Piatti, A. van Doorn, A. Musgrave, G. Felix, T. Boller, and T. Munnik
Elicitation of Suspension-Cultured Tomato Cells Triggers the Formation of Phosphatidic Acid and Diacylglycerol Pyrophosphate
Plant Physiology,
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123(4):
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S. J. Clough, K. A. Fengler, I-c. Yu, B. Lippok, R. K. Smith Jr., and A. F. Bent
The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel
PNAS,
July 12, 2000;
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W. E. Durrant, O. Rowland, P. Piedras, K. E. Hammond-Kosack, and J. D. G. Jones
cDNA-AFLP Reveals a Striking Overlap in Race-Specific Resistance and Wound Response Gene Expression Profiles
PLANT CELL,
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J. R. Koch, R. A. Creelman, S. M. Eshita, M. Seskar, J. E. Mullet, and K. R. Davis
Ozone Sensitivity in Hybrid Poplar Correlates with Insensitivity to Both Salicylic Acid and Jasmonic Acid. The Role of Programmed Cell Death in Lesion Formation
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T. Romeis, P. Piedras, and J. D. G. Jones
Resistance Gene-Dependent Activation of a Calcium-Dependent Protein Kinase in the Plant Defense Response
PLANT CELL,
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Y. Huang, H. Li, R. Gupta, P. C. Morris, S. Luan, and J. J. Kieber
ATMPK4, an Arabidopsis Homolog of Mitogen-Activated Protein Kinase, Is Activated in Vitro by AtMEK1 through Threonine Phosphorylation
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M. E. Hoyos and S. Zhang
Calcium-Independent Activation of Salicylic Acid-Induced Protein Kinase and a 40-Kilodalton Protein Kinase by Hyperosmotic Stress
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H. Hirt
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PNAS,
March 14, 2000;
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T. S. Nuhse, S. C. Peck, H. Hirt, and T. Boller
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J. Narváez-Vásquez, J. Florin-Christensen, and C. A. Ryan
Positional Specificity of a Phospholipase A Activity Induced by Wounding, Systemin, and Oligosaccharide Elicitors in Tomato Leaves
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F. Cardinale, C. Jonak, W. Ligterink, K. Niehaus, T. Boller, and H. Hirt
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O. E. Blasing, P. Westhoff, and P. Svensson
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C. A. Frye, D. Tang, and R. W. Innes
From the Cover: Negative regulation of defense responses in plants by a conserved MAPKK kinase
PNAS,
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E. Ono, H. L. Wong, T. Kawasaki, M. Hasegawa, O. Kodama, and K. Shimamoto
Essential role of the small GTPase Rac in disease resistance of rice
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[Abstract]
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S. J. Clough, K. A. Fengler, I-c. Yu, B. Lippok, R. K. Smith Jr., and A. F. Bent
The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel
PNAS,
August 1, 2000;
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[Abstract]
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M. Frey, C. Stettner, P. W. Pare, E. A. Schmelz, J. H. Tumlinson, and A. Gierl
An herbivore elicitor activates the gene for indole emission in maize
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S. Rivas, T. Romeis, and J. D. G. Jones
The Cf-9 Disease Resistance Protein Is Present in an ~420-Kilodalton Heteromultimeric Membrane-Associated Complex at One Molecule per Complex
PLANT CELL,
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[Abstract]
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P. J. Rushton, A. Reinstadler, V. Lipka, B. Lippok, and I. E. Somssich
Synthetic Plant Promoters Containing Defined Regulatory Elements Provide Novel Insights into Pathogen- and Wound-Induced Signaling
PLANT CELL,
April 1, 2002;
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[Abstract]
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