Salicylic Acid Induction–Deficient Mutants of Arabidopsis Express PR-2 and PR-5 and Accumulate High Levels of Camalexin after Pathogen Inoculation

Correspondence to: Christiane Nawrath, christiane.nawrath{at}unifr.ch (E-mail), 41-26-300-9740 (fax)

In Arabidopsis, systemic acquired resistance against pathogens has been associated with the accumulation of salicylic acid (SA) and the expression of the pathogenesis-related proteins PR-1, PR-2, and PR-5. We report here the isolation of two nonallelic mutants impaired in the pathway leading to SA biosynthesis. These SA induction–deficient (sid) mutants do not accumulate SA after pathogen inoculation and are more susceptible to both virulent and avirulent forms of Pseudomonas syringae and Peronospora parasitica. However, sid mutants are not as susceptible to these pathogens as are transgenic plants expressing the nahG gene encoding an SA hydroxylase that degrades SA to catechol. In contrast to NahG plants, only the expression of PR-1 is strongly reduced in sid mutants, whereas PR-2 and PR-5 are still expressed after pathogen attack. Furthermore, the accumulation of the phytoalexin camalexin is normal. These results indicate that SA-independent compensation pathways that do not operate in NahG plants are active in sid mutants. One of the mutants is allelic to eds5 (for enhanced disease susceptibility), whereas the other mutant has not been described previously.

This article has been cited by other articles:

				T. Yaeno and K. Iba BAH1/NLA, a RING-Type Ubiquitin E3 Ligase, Regulates the Accumulation of Salicylic Acid and Immune Responses to Pseudomonas syringae DC3000 Plant Physiology, October 1, 2008; 148(2): 1032 - 1041. [Abstract] [Full Text] [PDF]

				C. Garcion, A. Lohmann, E. Lamodiere, J. Catinot, A. Buchala, P. Doermann, and J.-P. Metraux Characterization and Biological Function of the ISOCHORISMATE SYNTHASE2 Gene of Arabidopsis Plant Physiology, July 1, 2008; 147(3): 1279 - 1287. [Abstract] [Full Text] [PDF]

				T. Griebel and J. Zeier Light Regulation and Daytime Dependency of Inducible Plant Defenses in Arabidopsis: Phytochrome Signaling Controls Systemic Acquired Resistance Rather Than Local Defense Plant Physiology, June 1, 2008; 147(2): 790 - 801. [Abstract] [Full Text] [PDF]

				C. Denoux, R. Galletti, N. Mammarella, S. Gopalan, D. Werck, G. De Lorenzo, S. Ferrari, F. M. Ausubel, and J. Dewdney Activation of Defense Response Pathways by OGs and Flg22 Elicitors in Arabidopsis Seedlings Mol Plant, May 22, 2008; (2008) ssn019v1. [Abstract] [Full Text] [PDF]

				N. Suzuki, S. Bajad, J. Shuman, V. Shulaev, and R. Mittler The Transcriptional Co-activator MBF1c Is a Key Regulator of Thermotolerance in Arabidopsis thaliana J. Biol. Chem., April 4, 2008; 283(14): 9269 - 9275. [Abstract] [Full Text] [PDF]

				M. Herde, K. Gartner, T. G. Kollner, B. Fode, W. Boland, J. Gershenzon, C. Gatz, and D. Tholl Identification and Regulation of TPS04/GES, an Arabidopsis Geranyllinalool Synthase Catalyzing the First Step in the Formation of the Insect-Induced Volatile C16-Homoterpene TMTT PLANT CELL, April 1, 2008; 20(4): 1152 - 1168. [Abstract] [Full Text] [PDF]

				O. Kourtchenko, M. X. Andersson, M. Hamberg, A. Brunnstrom, C. Gobel, K. L. McPhail, W. H. Gerwick, I. Feussner, and M. Ellerstrom Oxo-Phytodienoic Acid-Containing Galactolipids in Arabidopsis: Jasmonate Signaling Dependence Plant Physiology, December 1, 2007; 145(4): 1658 - 1669. [Abstract] [Full Text] [PDF]

				S. H. Spoel, J. S. Johnson, and X. Dong Regulation of tradeoffs between plant defenses against pathogens with different lifestyles PNAS, November 20, 2007; 104(47): 18842 - 18847. [Abstract] [Full Text] [PDF]

				A. M. Jones, S. E. Lindow, and M. C. Wildermuth Salicylic Acid, Yersiniabactin, and Pyoverdin Production by the Model Phytopathogen Pseudomonas syringae pv. tomato DC3000: Synthesis, Regulation, and Impact on Tomato and Arabidopsis Host Plants J. Bacteriol., October 1, 2007; 189(19): 6773 - 6786. [Abstract] [Full Text] [PDF]

				Z. Zhang, Q. Li, Z. Li, P. E. Staswick, M. Wang, Y. Zhu, and Z. He Dual Regulation Role of GH3.5 in Salicylic Acid and Auxin Signaling during Arabidopsis-Pseudomonas syringae Interaction Plant Physiology, October 1, 2007; 145(2): 450 - 464. [Abstract] [Full Text] [PDF]

				M. Nafisi, S. Goregaoker, C. J. Botanga, E. Glawischnig, C. E. Olsen, B. A. Halkier, and J. Glazebrook Arabidopsis Cytochrome P450 Monooxygenase 71A13 Catalyzes the Conversion of Indole-3-Acetaldoxime in Camalexin Synthesis PLANT CELL, June 1, 2007; 19(6): 2039 - 2052. [Abstract] [Full Text] [PDF]

				K. Nobuta, R.A. Okrent, M. Stoutemyer, N. Rodibaugh, L. Kempema, M.C. Wildermuth, and R.W. Innes The GH3 Acyl Adenylase Family Member PBS3 Regulates Salicylic Acid-Dependent Defense Responses in Arabidopsis Plant Physiology, June 1, 2007; 144(2): 1144 - 1156. [Abstract] [Full Text] [PDF]

				M. A. Strawn, S. K. Marr, K. Inoue, N. Inada, C. Zubieta, and M. C. Wildermuth Arabidopsis Isochorismate Synthase Functional in Pathogen-induced Salicylate Biosynthesis Exhibits Properties Consistent with a Role in Diverse Stress Responses J. Biol. Chem., February 23, 2007; 282(8): 5919 - 5933. [Abstract] [Full Text] [PDF]

				D. Little, C. Gouhier-Darimont, F. Bruessow, and P. Reymond Oviposition by Pierid Butterflies Triggers Defense Responses in Arabidopsis Plant Physiology, February 1, 2007; 143(2): 784 - 800. [Abstract] [Full Text] [PDF]

				L. Bulow, M. Schindler, and R. Hehl PathoPlant(R): a platform for microarray expression data to analyze co-regulated genes involved in plant defense responses Nucleic Acids Res., January 12, 2007; 35(suppl_1): D841 - D845. [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]

				T. Kariola, G. Brader, E. Helenius, J. Li, P. Heino, and E. T. Palva EARLY RESPONSIVE TO DEHYDRATION 15, a Negative Regulator of Abscisic Acid Responses in Arabidopsis Plant Physiology, December 1, 2006; 142(4): 1559 - 1573. [Abstract] [Full Text] [PDF]

				N. Journot-Catalino, I. E. Somssich, D. Roby, and T. Kroj The Transcription Factors WRKY11 and WRKY17 Act as Negative Regulators of Basal Resistance in Arabidopsis thaliana PLANT CELL, November 1, 2006; 18(11): 3289 - 3302. [Abstract] [Full Text] [PDF]

				M. De Vos, W. Van Zaanen, A. Koornneef, J. P. Korzelius, M. Dicke, L.C. Van Loon, and C. M.J. Pieterse Herbivore-Induced Resistance against Microbial Pathogens in Arabidopsis Plant Physiology, September 1, 2006; 142(1): 352 - 363. [Abstract] [Full Text] [PDF]

				T. E. Mishina and J. Zeier The Arabidopsis Flavin-Dependent Monooxygenase FMO1 Is an Essential Component of Biologically Induced Systemic Acquired Resistance Plant Physiology, August 1, 2006; 141(4): 1666 - 1675. [Abstract] [Full Text] [PDF]

				A. Mateo, D. Funck, P. Muhlenbock, B. Kular, P. M Mullineaux, and S. Karpinski Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis J. Exp. Bot., May 1, 2006; 57(8): 1795 - 1807. [Abstract] [Full Text] [PDF]

				X. Xu, C. Chen, B. Fan, and Z. Chen Physical and Functional Interactions between Pathogen-Induced Arabidopsis WRKY18, WRKY40, and WRKY60 Transcription Factors PLANT CELL, May 1, 2006; 18(5): 1310 - 1326. [Abstract] [Full Text] [PDF]

				T. Yaeno, B. Saito, T. Katsuki, and K. Iba Ozone-induced Expression of the Arabidopsis FAD7 Gene Requires Salicylic Acid, but not NPR1 and SID2 Plant Cell Physiol., March 1, 2006; 47(3): 355 - 362. [Abstract] [Full Text] [PDF]

				K. Yoshioka, W. Moeder, H.-G. Kang, P. Kachroo, K. Masmoudi, G. Berkowitz, and D. F. Klessig The Chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 Activates Multiple Pathogen Resistance Responses PLANT CELL, March 1, 2006; 18(3): 747 - 763. [Abstract] [Full Text] [PDF]

				M. Stein, J. Dittgen, C. Sanchez-Rodriguez, B.-H. Hou, A. Molina, P. Schulze-Lefert, V. Lipka, and S. Somerville Arabidopsis PEN3/PDR8, an ATP Binding Cassette Transporter, Contributes to Nonhost Resistance to Inappropriate Pathogens That Enter by Direct Penetration PLANT CELL, March 1, 2006; 18(3): 731 - 746. [Abstract] [Full Text] [PDF]

				A. C. Diener and F. M. Ausubel RESISTANCE TO FUSARIUM OXYSPORUM 1, a Dominant Arabidopsis Disease-Resistance Gene, Is Not Race Specific Genetics, September 1, 2005; 171(1): 305 - 321. [Abstract] [Full Text] [PDF]

				D. Tang, K. M. Christiansen, and R. W. Innes Regulation of Plant Disease Resistance, Stress Responses, Cell Death, and Ethylene Signaling in Arabidopsis by the EDR1 Protein Kinase Plant Physiology, June 1, 2005; 138(2): 1018 - 1026. [Abstract] [Full Text] [PDF]

				K. Ramonell, M. Berrocal-Lobo, S. Koh, J. Wan, H. Edwards, G. Stacey, and S. Somerville Loss-of-Function Mutations in Chitin Responsive Genes Show Increased Susceptibility to the Powdery Mildew Pathogen Erysiphe cichoracearum Plant Physiology, June 1, 2005; 138(2): 1027 - 1036. [Abstract] [Full Text] [PDF]

				P. Brodersen, F. G. Malinovsky, K. Hematy, M.-A. Newman, and J. Mundy The Role of Salicylic Acid in the Induction of Cell Death in Arabidopsis acd11 Plant Physiology, June 1, 2005; 138(2): 1037 - 1045. [Abstract] [Full Text] [PDF]

				R. A. Salzman, J. A. Brady, S. A. Finlayson, C. D. Buchanan, E. J. Summer, F. Sun, P. E. Klein, R. R. Klein, L. H. Pratt, M.-M. Cordonnier-Pratt, et al. Transcriptional Profiling of Sorghum Induced by Methyl Jasmonate, Salicylic Acid, and Aminocyclopropane Carboxylic Acid Reveals Cooperative Regulation and Novel Gene Responses Plant Physiology, May 1, 2005; 138(1): 352 - 368. [Abstract] [Full Text] [PDF]

				Y. Zhang and X. Li A Putative Nucleoporin 96 Is Required for Both Basal Defense and Constitutive Resistance Responses Mediated by suppressor of npr1-1,constitutive 1 PLANT CELL, April 1, 2005; 17(4): 1306 - 1316. [Abstract] [Full Text] [PDF]

				J. Ton, G. Jakab, V. Toquin, V. Flors, A. Iavicoli, M. N. Maeder, J.-P. Metraux, and B. Mauch-Mani Dissecting the {beta}-Aminobutyric Acid-Induced Priming Phenomenon in Arabidopsis PLANT CELL, March 1, 2005; 17(3): 987 - 999. [Abstract] [Full Text] [PDF]

				Z. Huang, J. M. Yeakley, E. W. Garcia, J. D. Holdridge, J.-B. Fan, and S. A. Whitham Salicylic Acid-Dependent Expression of Host Genes in Compatible Arabidopsis-Virus Interactions Plant Physiology, March 1, 2005; 137(3): 1147 - 1159. [Abstract] [Full Text] [PDF]

				H. Takahashi, Y. Kanayama, M. S. Zheng, T. Kusano, S. Hase, M. Ikegami, and J. Shah Antagonistic Interactions between the SA and JA Signaling Pathways in Arabidopsis Modulate Expression of Defense Genes and Gene-for-Gene Resistance to Cucumber Mosaic Virus Plant Cell Physiol., June 15, 2004; 45(6): 803 - 809. [Abstract] [Full Text] [PDF]

				I. M. Scott, S. M. Clarke, J. E. Wood, and L. A.J. Mur Salicylate Accumulation Inhibits Growth at Chilling Temperature in Arabidopsis Plant Physiology, June 1, 2004; 135(2): 1040 - 1049. [Abstract] [Full Text] [PDF]

				A. Nandi, R. Welti, and J. Shah The Arabidopsis thaliana Dihydroxyacetone Phosphate Reductase Gene SUPPRESSOR OF FATTY ACID DESATURASE DEFICIENCY1 Is Required for Glycerolipid Metabolism and for the Activation of Systemic Acquired Resistance PLANT CELL, February 1, 2004; 16(2): 465 - 477. [Abstract] [Full Text] [PDF]

				J. T. Song, H. Lu, and J. T. Greenberg Divergent Roles in Arabidopsis thaliana Development and Defense of Two Homologous Genes, ABERRANT GROWTH AND DEATH2 and AGD2-LIKE DEFENSE RESPONSE PROTEIN1, Encoding Novel Aminotransferases PLANT CELL, February 1, 2004; 16(2): 353 - 366. [Abstract] [Full Text] [PDF]

				J. Li, G. Brader, and E. T. Palva The WRKY70 Transcription Factor: A Node of Convergence for Jasmonate-Mediated and Salicylate-Mediated Signals in Plant Defense PLANT CELL, February 1, 2004; 16(2): 319 - 331. [Abstract] [Full Text] [PDF]

				H. Suzuki, Y. Xia, R. Cameron, G. Shadle, J. Blount, C. Lamb, and R. A. Dixon Signals for local and systemic responses of plants to pathogen attack J. Exp. Bot., January 2, 2004; 55(395): 169 - 179. [Abstract] [Full Text] [PDF]

				Y. Zhang, M. J. Tessaro, M. Lassner, and X. Li Knockout Analysis of Arabidopsis Transcription Factors TGA2, TGA5, and TGA6 Reveals Their Redundant and Essential Roles in Systemic Acquired Resistance PLANT CELL, November 1, 2003; 15(11): 2647 - 2653. [Abstract] [Full Text] [PDF]

				Y. Zhang, S. Goritschnig, X. Dong, and X. Li A Gain-of-Function Mutation in a Plant Disease Resistance Gene Leads to Constitutive Activation of Downstream Signal Transduction Pathways in suppressor of npr1-1, constitutive 1 PLANT CELL, November 1, 2003; 15(11): 2636 - 2646. [Abstract] [Full Text] [PDF]

				A. Nandi, K. Krothapalli, C. M. Buseman, M. Li, R. Welti, A. Enyedi, and J. Shah Arabidopsis sfd Mutants Affect Plastidic Lipid Composition and Suppress Dwarfing, Cell Death, and the Enhanced Disease Resistance Phenotypes Resulting from the Deficiency of a Fatty Acid Desaturase PLANT CELL, October 1, 2003; 15(10): 2383 - 2398. [Abstract] [Full Text] [PDF]

				C. Despres, C. Chubak, A. Rochon, R. Clark, T. Bethune, D. Desveaux, and P. R. Fobert The Arabidopsis NPR1 Disease Resistance Protein Is a Novel Cofactor That Confers Redox Regulation of DNA Binding Activity to the Basic Domain/Leucine Zipper Transcription Factor TGA1 PLANT CELL, September 1, 2003; 15(9): 2181 - 2191. [Abstract] [Full Text] [PDF]

				D. Lieberherr, U. Wagner, P.-H. Dubuis, J.-P. Metraux, and F. Mauch The Rapid Induction of Glutathione S-Transferases AtGSTF2 and AtGSTF6 by Avirulent Pseudomonas syringae is the Result of Combined Salicylic Acid and Ethylene Signaling Plant Cell Physiol., July 15, 2003; 44(7): 750 - 757. [Abstract] [Full Text] [PDF]

				S. C.M. van Wees, H.-S. Chang, T. Zhu, and J. Glazebrook Characterization of the Early Response of Arabidopsis to Alternaria brassicicola Infection Using Expression Profiling Plant Physiology, June 1, 2003; 132(2): 606 - 617. [Abstract] [Full Text] [PDF]

				P. Wick, X. Gansel, C. Oulevey, V. Page, I. Studer, M. Durst, and L. Sticher The Expression of the t-SNARE AtSNAP33 Is Induced by Pathogens and Mechanical Stimulation Plant Physiology, May 1, 2003; 132(1): 343 - 351. [Abstract] [Full Text] [PDF]

				G. M. Pastori, G. Kiddle, J. Antoniw, S. Bernard, S. Veljovic-Jovanovic, P. J. Verrier, G. Noctor, and C. H. Foyer Leaf Vitamin C Contents Modulate Plant Defense Transcripts and Regulate Genes That Control Development through Hormone Signaling PLANT CELL, April 1, 2003; 15(4): 939 - 951. [Abstract] [Full Text] [PDF]

				S. H. Spoel, A. Koornneef, S. M. C. Claessens, J. P. Korzelius, J. A. Van Pelt, M. J. Mueller, A. J. Buchala, J.-P. Metraux, R. Brown, K. Kazan, et al. NPR1 Modulates Cross-Talk between Salicylate- and Jasmonate-Dependent Defense Pathways through a Novel Function in the Cytosol PLANT CELL, March 1, 2003; 15(3): 760 - 770. [Abstract] [Full Text] [PDF]

				Y. Tao, Z. Xie, W. Chen, J. Glazebrook, H.-S. Chang, B. Han, T. Zhu, G. Zou, and F. Katagiri Quantitative Nature of Arabidopsis Responses during Compatible and Incompatible Interactions with the Bacterial Pathogen Pseudomonas syringae PLANT CELL, February 1, 2003; 15(2): 317 - 330. [Abstract] [Full Text] [PDF]

				E. E. Rogers and M. L. Guerinot FRD3, a Member of the Multidrug and Toxin Efflux Family, Controls Iron Deficiency Responses in Arabidopsis PLANT CELL, August 1, 2002; 14(8): 1787 - 1799. [Abstract] [Full Text] [PDF]

				J. Cui, G. Jander, L. R. Racki, P. D. Kim, N. E. Pierce, and F. M. Ausubel Signals Involved in Arabidopsis Resistance to Trichoplusia ni Caterpillars Induced by Virulent and Avirulent Strains of the Phytopathogen Pseudomonas syringae Plant Physiology, June 1, 2002; 129(2): 551 - 564. [Abstract] [Full Text] [PDF]

				C. Nawrath, S. Heck, N. Parinthawong, and J.-P. Metraux EDS5, an Essential Component of Salicylic Acid-Dependent Signaling for Disease Resistance in Arabidopsis, Is a Member of the MATE Transporter Family PLANT CELL, January 1, 2002; 14(1): 275 - 286. [Abstract] [Full Text] [PDF]

				C. Rusterucci, D. H. Aviv, B. F. Holt III, J. L. Dangl, and J. E. Parker The Disease Resistance Signaling Components EDS1 and PAD4 Are Essential Regulators of the Cell Death Pathway Controlled by LSD1 in Arabidopsis PLANT CELL, October 1, 2001; 13(10): 2211 - 2224. [Abstract] [Full Text] [PDF]

				N. Jambunathan, J. M. Siani, and T. W. McNellis A Humidity-Sensitive Arabidopsis Copine Mutant Exhibits Precocious Cell Death and Increased Disease Resistance PLANT CELL, October 1, 2001; 13(10): 2225 - 2240. [Abstract] [Full Text] [PDF]

				T. Genoud, M. B. Trevino Santa Cruz, and J.-P. Metraux Numeric Simulation of Plant Signaling Networks Plant Physiology, August 1, 2001; 126(4): 1430 - 1437. [Abstract] [Full Text] [PDF]

				C. P. Selitrennikoff Antifungal Proteins Appl. Envir. Microbiol., July 1, 2001; 67(7): 2883 - 2894. [Full Text] [PDF]

				J. Chong, M.-A. Pierrel, R. Atanassova, D. Werck-Reichhart, B. Fritig, and P. Saindrenan Free and Conjugated Benzoic Acid in Tobacco Plants and Cell Cultures. Induced Accumulation upon Elicitation of Defense Responses and Role as Salicylic Acid Precursors Plant Physiology, January 1, 2001; 125(1): 318 - 328. [Abstract] [Full Text]

				E. Mayda, B. Mauch-Mani, and P. Vera Arabidopsis dth9 Mutation Identifies a Gene Involved in Regulating Disease Susceptibility without Affecting Salicylic Acid-Dependent Responses PLANT CELL, November 1, 2000; 12(11): 2119 - 2128. [Abstract] [Full Text]