Activation of the Tobacco SIP Kinase by Both a Cell Wall–Derived Carbohydrate Elicitor and Purified Proteinaceous Elicitins from Phytophthora spp

Correspondence to: Daniel F. Klessig, klessig{at}mbcl.rutgers.edu (E-mail), 732-445-5735 (fax).

Two purified proteinaceous fungal elicitors, parasiticein (an elicitin) and cryptogein (a ß elicitin), as well as a fungal cell wall–derived carbohydrate elicitor all rapidly activated a 48-kD kinase in tobacco suspension cells. The maximum activation of this kinase paralleled or preceded medium alkalization and activation of the defense gene phenylalanine ammonia–lyase (PAL). In addition, the two elicitins, which also induced hypersensitive cell death, activated a 44- and a 40-kD kinase with delayed kinetics. By contrast, the cell wall–derived elicitor only weakly activated the 44-kD kinase and failed to activate the 40-kD kinase. The size and substrate preference of the 48-kD kinase are reminiscent of the recently purified and cloned salicylic acid–induced protein (SIP) kinase, which is a member of the mitogen-activated protein kinase family. Antibodies raised against a peptide corresponding to the unique N terminus of SIP kinase immunoreacted with the 48-kD kinase activated by all three elicitors from Phytophthora spp. In addition, the cell wall elicitor and the salicylic acid–activated 48-kD kinase copurified through several chromatography steps and comigrated on two-dimensional gels. Based on these results, all three fungal elicitors appear to activate the SIP kinase. In addition, inhibition of SIP kinase activation by kinase inhibitors correlated with the suppression of cell wall elicitor–induced medium alkalization and PAL gene activation, suggesting a regulatory function for the SIP kinase in these defense responses.

This article has been cited by other articles:

				T. Stanislas, D. Bouyssie, M. Rossignol, S. Vesa, J. Fromentin, J. Morel, C. Pichereaux, B. Monsarrat, and F. Simon-Plas Quantitative Proteomics Reveals a Dynamic Association of Proteins to Detergent-resistant Membranes upon Elicitor Signaling in Tobacco Mol. Cell. Proteomics, September 1, 2009; 8(9): 2186 - 2198. [Abstract] [Full Text] [PDF]

				S. AbuQamar, M.-F. Chai, H. Luo, F. Song, and T. Mengiste Tomato Protein Kinase 1b Mediates Signaling of Plant Responses to Necrotrophic Fungi and Insect Herbivory PLANT CELL, July 1, 2008; 20(7): 1964 - 1983. [Abstract] [Full Text] [PDF]

				F. Takahashi, R. Yoshida, K. Ichimura, T. Mizoguchi, S. Seo, M. Yonezawa, K. Maruyama, K. Yamaguchi-Shinozaki, and K. Shinozaki The Mitogen-Activated Protein Kinase Cascade MKK3-MPK6 Is an Important Part of the Jasmonate Signal Transduction Pathway in Arabidopsis PLANT CELL, March 1, 2007; 19(3): 805 - 818. [Abstract] [Full Text] [PDF]

				K. Ichimura, C. Casais, S. C. Peck, K. Shinozaki, and K. Shirasu MEKK1 Is Required for MPK4 Activation and Regulates Tissue-specific and Temperature-dependent Cell Death in Arabidopsis J. Biol. Chem., December 1, 2006; 281(48): 36969 - 36976. [Abstract] [Full Text] [PDF]

				M. Shoresh, A. Gal-On, D. Leibman, and I. Chet Characterization of a Mitogen-Activated Protein Kinase Gene from Cucumber Required for Trichoderma-Conferred Plant Resistance Plant Physiology, November 1, 2006; 142(3): 1169 - 1179. [Abstract] [Full Text] [PDF]

				Y. Kadota, S. Fujii, Y. Ogasawara, Y. Maeda, K. Higashi, and K. Kuchitsu Continuous Recognition of the Elicitor Signal for Several Hours is Prerequisite for Induction of Cell Death and Prolonged Activation of Signaling Events in Tobacco BY-2 Cells Plant Cell Physiol., September 1, 2006; 47(9): 1337 - 1342. [Abstract] [Full Text] [PDF]

				D. Ren, K.-Y. Yang, G.-J. Li, Y. Liu, and S. Zhang Activation of Ntf4, a Tobacco Mitogen-Activated Protein Kinase, during Plant Defense Response and Its Involvement in Hypersensitive Response-Like Cell Death Plant Physiology, August 1, 2006; 141(4): 1482 - 1493. [Abstract] [Full Text] [PDF]

				A. Zhang, M. Jiang, J. Zhang, M. Tan, and X. Hu Mitogen-Activated Protein Kinase Is Involved in Abscisic Acid-Induced Antioxidant Defense and Acts Downstream of Reactive Oxygen Species Production in Leaves of Maize Plants Plant Physiology, June 1, 2006; 141(2): 475 - 487. [Abstract] [Full Text] [PDF]

				S. Katou, H. Yoshioka, K. Kawakita, O. Rowland, J. D.G. Jones, H. Mori, and N. Doke Involvement of PPS3 Phosphorylated by Elicitor-Responsive Mitogen-Activated Protein Kinases in the Regulation of Plant Cell Death Plant Physiology, December 1, 2005; 139(4): 1914 - 1926. [Abstract] [Full Text] [PDF]

				D. Lieberherr, N. P. Thao, A. Nakashima, K. Umemura, T. Kawasaki, and K. Shimamoto A Sphingolipid Elicitor-Inducible Mitogen-Activated Protein Kinase Is Regulated by the Small GTPase OsRac1 and Heterotrimeric G-Protein in Rice Plant Physiology, July 1, 2005; 138(3): 1644 - 1652. [Abstract] [Full Text] [PDF]

				D. Takemoto, A. R. Hardham, and D. A. Jones Differences in Cell Death Induction by Phytophthora Elicitins Are Determined by Signal Components Downstream of MAP Kinase Kinase in Different Species of Nicotiana and Cultivars of Brassica rapa and Raphanus sativus Plant Physiology, July 1, 2005; 138(3): 1491 - 1504. [Abstract] [Full Text] [PDF]

				Y. Kadota, T. Watanabe, S. Fujii, Y. Maeda, R. Ohno, K. Higashi, T. Sano, S. Muto, S. Hasezawa, and K. Kuchitsu Cell Cycle Dependence of Elicitor-induced Signal Transduction in Tobacco BY-2 Cells Plant Cell Physiol., January 15, 2005; 46(1): 156 - 165. [Abstract] [Full Text] [PDF]

				Y. Liu and S. Zhang Phosphorylation of 1-Aminocyclopropane-1-Carboxylic Acid Synthase by MPK6, a Stress-Responsive Mitogen-Activated Protein Kinase, Induces Ethylene Biosynthesis in Arabidopsis PLANT CELL, December 1, 2004; 16(12): 3386 - 3399. [Abstract] [Full Text] [PDF]

				M. Boudsocq, H. Barbier-Brygoo, and C. Lauriere Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana J. Biol. Chem., October 1, 2004; 279(40): 41758 - 41766. [Abstract] [Full Text] [PDF]

				J. Lee, J. J. Rudd, V. K. Macioszek, and D. Scheel Dynamic Changes in the Localization of MAPK Cascade Components Controlling Pathogenesis-related (PR) Gene Expression during Innate Immunity in Parsley J. Biol. Chem., May 21, 2004; 279(21): 22440 - 22448. [Abstract] [Full Text] [PDF]

				M. Mayrose, A. Bonshtien, and G. Sessa LeMPK3 Is a Mitogen-activated Protein Kinase with Dual Specificity Induced during Tomato Defense and Wounding Responses J. Biol. Chem., April 9, 2004; 279(15): 14819 - 14827. [Abstract] [Full Text] [PDF]

				F. L.H. Menke, J. A. van Pelt, C. M.J. Pieterse, and D. F. Klessig Silencing of the Mitogen-Activated Protein Kinase MPK6 Compromises Disease Resistance in Arabidopsis PLANT CELL, April 1, 2004; 16(4): 897 - 907. [Abstract] [Full Text] [PDF]

				I. J. Tetlow, R. Wait, Z. Lu, R. Akkasaeng, C. G. Bowsher, S. Esposito, B. Kosar-Hashemi, M. K. Morell, and M. J. Emes Protein Phosphorylation in Amyloplasts Regulates Starch Branching Enzyme Activity and Protein-Protein Interactions PLANT CELL, March 1, 2004; 16(3): 694 - 708. [Abstract] [Full Text] [PDF]

				C. Norman, K. A. Howell, A. H. Millar, J. M. Whelan, and D. A. Day Salicylic Acid Is an Uncoupler and Inhibitor of Mitochondrial Electron Transport Plant Physiology, January 1, 2004; 134(1): 492 - 501. [Abstract] [Full Text] [PDF]

				C. Y. Kim, Y. Liu, E. T. Thorne, H. Yang, H. Fukushige, W. Gassmann, D. Hildebrand, R. E. Sharp, and S. Zhang Activation of a Stress-Responsive Mitogen-Activated Protein Kinase Cascade Induces the Biosynthesis of Ethylene in Plants PLANT CELL, November 1, 2003; 15(11): 2707 - 2718. [Abstract] [Full Text] [PDF]

				N. J. Price, C. Pinheiro, C. M. Soares, D. A. Ashford, C. P. Ricardo, and P. A. Jackson A Biochemical and Molecular Characterization of LEP1, an Extensin Peroxidase from Lupin J. Biol. Chem., October 17, 2003; 278(42): 41389 - 41399. [Abstract] [Full Text] [PDF]

				K. I. Ivanov, P. Puustinen, R. Gabrenaite, H. Vihinen, L. Ronnstrand, L. Valmu, N. Kalkkinen, and K. Makinen Phosphorylation of the Potyvirus Capsid Protein by Protein Kinase CK2 and Its Relevance for Virus Infection PLANT CELL, September 1, 2003; 15(9): 2124 - 2139. [Abstract] [Full Text] [PDF]

				Y. H. Cheong, B. C. Moon, J. K. Kim, C. Y. Kim, M. C. Kim, I. H. Kim, C. Y. Park, J. C. Kim, B. O. Park, S. C. Koo, et al. BWMK1, a Rice Mitogen-Activated Protein Kinase, Locates in the Nucleus and Mediates Pathogenesis-Related Gene Expression by Activation of a Transcription Factor Plant Physiology, August 1, 2003; 132(4): 1961 - 1972. [Abstract] [Full Text] [PDF]

				S. C. Chang, M. H. Cho, S.-K. Kim, J. S. Lee, A. Kirakosyan, and P. B. Kaufman Changes in phosphorylation of 50 and 53 kDa soluble proteins in graviresponding oat (Avena sativa) shoots J. Exp. Bot., March 1, 2003; 54(384): 1013 - 1022. [Abstract] [Full Text] [PDF]

				H. Yoshioka, N. Numata, K. Nakajima, S. Katou, K. Kawakita, O. Rowland, J. D. G. Jones, and N. Doke Nicotiana benthamiana gp91phox Homologs NbrbohA and NbrbohB Participate in H2O2 Accumulation and Resistance to Phytophthora infestans PLANT CELL, March 1, 2003; 15(3): 706 - 718. [Abstract] [Full Text] [PDF]

				M. E. Zanetti, F. A. Blanco, G. R. Daleo, and C. A. Casalongue Phosphorylation of a member of the MBF1 transcriptional co-activator family, StMBF1, is stimulated in potato cell suspensions upon fungal elicitor challenge J. Exp. Bot., February 1, 2003; 54(383): 623 - 632. [Abstract] [Full Text] [PDF]

				T. Kroj, J. J. Rudd, T. Nurnberger, Y. Gabler, J. Lee, and D. Scheel Mitogen-activated Protein Kinases Play an Essential Role in Oxidative Burst-independent Expression of Pathogenesis-related Genes in Parsley J. Biol. Chem., January 17, 2003; 278(4): 2256 - 2264. [Abstract] [Full Text] [PDF]

				T. Roitsch, M. E. Balibrea, M. Hofmann, R. Proels, and A. K. Sinha Extracellular invertase: key metabolic enzyme and PR protein J. Exp. Bot., January 3, 2003; 54(382): 513 - 524. [Abstract] [Full Text] [PDF]

				A. K. Sinha, M. G. Hofmann, U. Romer, W. Kockenberger, L. Elling, and T. Roitsch Metabolizable and Non-Metabolizable Sugars Activate Different Signal Transduction Pathways in Tomato Plant Physiology, April 1, 2002; 128(4): 1480 - 1489. [Abstract] [Full Text] [PDF]

				D. Ren, H. Yang, and S. Zhang Cell Death Mediated by MAPK Is Associated with Hydrogen Peroxide Production in Arabidopsis J. Biol. Chem., January 4, 2002; 277(1): 559 - 565. [Abstract] [Full Text]

				J. M. Chico, M. Raices, M. T. Tellez-Inon, and R. M. Ulloa A Calcium-Dependent Protein Kinase Is Systemically Induced upon Wounding in Tomato Plants Plant Physiology, January 1, 2002; 128(1): 256 - 270. [Abstract] [Full Text] [PDF]

				V. L. Link, M. G. Hofmann, A. K. Sinha, R. Ehness, M. Strnad, and T. Roitsch Biochemical Evidence for the Activation of Distinct Subsets of Mitogen-Activated Protein Kinases by Voltage and Defense-Related Stimuli Plant Physiology, January 1, 2002; 128(1): 271 - 281. [Abstract] [Full Text] [PDF]

				T. Yuasa, K. Ichimura, T. Mizoguchi, and K. Shinozaki Oxidative Stress Activates ATMPK6, an Arabidopsis Homologue of MAP Kinase Plant Cell Physiol., September 1, 2001; 42(9): 1012 - 1016. [Abstract] [Full Text] [PDF]

				S. Zhang and Y. Liu Activation of Salicylic Acid-Induced Protein Kinase, a Mitogen-Activated Protein Kinase, Induces Multiple Defense Responses in Tobacco PLANT CELL, August 1, 2001; 13(8): 1877 - 1889. [Abstract] [Full Text] [PDF]

				R. Desikan, J. T. Hancock, K. Ichimura, K. Shinozaki, and S. J. Neill Harpin Induces Activation of the Arabidopsis Mitogen-Activated Protein Kinases AtMPK4 and AtMPK6 Plant Physiology, August 1, 2001; 126(4): 1579 - 1587. [Abstract] [Full Text] [PDF]

				S. C. Peck, T. S. Nuhse, D. Hess, A. Iglesias, F. Meins, and T. Boller Directed Proteomics Identifies a Plant-Specific Protein Rapidly Phosphorylated in Response to Bacterial and Fungal Elicitors PLANT CELL, June 1, 2001; 13(6): 1467 - 1475. [Abstract] [Full Text] [PDF]

				J. Lee, D. F. Klessig, and T. Nurnberger A Harpin Binding Site in Tobacco Plasma Membranes Mediates Activation of the Pathogenesis-Related Gene HIN1 Independent of Extracellular Calcium but Dependent on Mitogen-Activated Protein Kinase Activity PLANT CELL, May 1, 2001; 13(5): 1079 - 1093. [Abstract] [Full Text]

				K.-Y. Yang, Y. Liu, and S. Zhang Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco PNAS, January 16, 2001; 98(2): 741 - 746. [Abstract] [Full Text] [PDF]

				K. Sugimoto, S. Takeda, and H. Hirochika MYB-Related Transcription Factor NtMYB2 Induced by Wounding and Elicitors is a Regulator of the Tobacco Retrotransposon Tto1 and Defense-Related Genes PLANT CELL, December 1, 2000; 12(12): 2511 - 2528. [Abstract] [Full Text]

				F. Kieffer, J. Lherminier, F. Simon-Plas, M. Nicole, M. Paynot, T. Elmayan, and J.-P. Blein The fungal elicitor cryptogein induces cell wall modifications on tobacco cell suspension J. Exp. Bot., November 1, 2000; 51(352): 1799 - 1811. [Abstract] [Full Text] [PDF]

				S. Kiegerl, F. Cardinale, C. Siligan, A. Gross, E. Baudouin, A. Liwosz, S. Eklof, S. Till, L. Bogre, H. Hirt, et al. SIMKK, a Mitogen-Activated Protein Kinase (MAPK) Kinase, Is a Specific Activator of the Salt Stress-Induced MAPK, SIMK PLANT CELL, November 1, 2000; 12(11): 2247 - 2258. [Abstract] [Full Text]

				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. Nitric oxide and salicylic acid signaling in plant defense PNAS, August 1, 2000; 97(16): 8849 - 8855. [Abstract] [Full Text] [PDF]

				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, August 1, 2000; 123(4): 1507 - 1516. [Abstract] [Full Text]

				S. Seo, M. Okamoto, T. Iwai, M. Iwano, K. Fukui, A. Isogai, N. Nakajima, and Y. Ohashi Reduced Levels of Chloroplast FtsH Protein in Tobacco Mosaic Virus-Infected Tobacco Leaves Accelerate the Hypersensitive Reaction PLANT CELL, June 1, 2000; 12(6): 917 - 932. [Abstract] [Full Text]

				Y.-Q. Gu, C. Yang, V. K. Thara, J. Zhou, and G. B. Martin Pti4 Is Induced by Ethylene and Salicylic Acid, and Its Product Is Phosphorylated by the Pto Kinase PLANT CELL, May 1, 2000; 12(5): 771 - 786. [Abstract] [Full Text]

				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, May 1, 2000; 12(5): 803 - 816. [Abstract] [Full Text]

				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 Plant Physiology, April 1, 2000; 122(4): 1301 - 1310. [Abstract] [Full Text]

				M. E. Hoyos and S. Zhang Calcium-Independent Activation of Salicylic Acid-Induced Protein Kinase and a 40-Kilodalton Protein Kinase by Hyperosmotic Stress Plant Physiology, April 1, 2000; 122(4): 1355 - 1364. [Abstract] [Full Text]

				T. S. Nuhse, S. C. Peck, H. Hirt, and T. Boller Microbial Elicitors Induce Activation and Dual Phosphorylation of the Arabidopsis thaliana MAPK 6 J. Biol. Chem., March 10, 2000; 275(11): 7521 - 7526. [Abstract] [Full Text] [PDF]

				M. Mikolajczyk, O. S. Awotunde, G. Muszynska, D. F. Klessig, and G. Dobrowolska Osmotic Stress Induces Rapid Activation of a Salicylic Acid-Induced Protein Kinase and a Homolog of Protein Kinase ASK1 in Tobacco Cells PLANT CELL, January 1, 2000; 12(1): 165 - 178. [Abstract] [Full Text] [PDF]

				S. Bourque, M.-N. Binet, M. Ponchet, A. Pugin, and A. Lebrun-Garcia Characterization of the Cryptogein Binding Sites on Plant Plasma Membranes J. Biol. Chem., December 3, 1999; 274(49): 34699 - 34705. [Abstract] [Full Text] [PDF]

				J. Shi, K.-N. Kim, O. Ritz, V. Albrecht, R. Gupta, K. Harter, S. Luan, and J. Kudla Novel Protein Kinases Associated with Calcineurin B-like Calcium Sensors in Arabidopsis PLANT CELL, December 1, 1999; 11(12): 2393 - 2406. [Abstract] [Full Text]

				K. Suzuki, A. Yano, and H. Shinshi Slow and Prolonged Activation of the p47 Protein Kinase during Hypersensitive Cell Death in a Culture of Tobacco Cells Plant Physiology, April 1, 1999; 119(4): 1465 - 1472. [Abstract] [Full Text]

				T. Romeis, P. Piedras, S. Zhang, D. F. Klessig, H. Hirt, and J. D. G. Jones 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 PLANT CELL, February 1, 1999; 11(2): 273 - 288. [Abstract] [Full Text]

				S. Seo, H. Sano, and Y. Ohashi Jasmonate-Based Wound Signal Transduction Requires Activation of WIPK, a Tobacco Mitogen-Activated Protein Kinase PLANT CELL, February 1, 1999; 11(2): 289 - 298. [Abstract] [Full Text]

				S. Zhang and D. F. Klessig Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection PNAS, June 23, 1998; 95(13): 7433 - 7438. [Abstract] [Full Text] [PDF]

				S. Zhang and D. F. Klessig The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK PNAS, June 9, 1998; 95(12): 7225 - 7230. [Abstract] [Full Text] [PDF]

				O Calderini, L Bogre, O Vicente, P Binarova, E Heberle-Bors, and C Wilson A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells J. Cell Sci., January 10, 1998; 111(20): 3091 - 3100. [Abstract] [PDF]

				F. Cardinale, C. Jonak, W. Ligterink, K. Niehaus, T. Boller, and H. Hirt Differential Activation of Four Specific MAPK Pathways by Distinct Elicitors J. Biol. Chem., November 17, 2000; 275(47): 36734 - 36740. [Abstract] [Full Text] [PDF]

				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, January 2, 2001; 98(1): 373 - 378. [Abstract] [Full Text] [PDF]