THE PLANT CELL, Vol 8, Issue 11 2033-2046, Copyright © 1996 by American Society of Plant Biologists

RESEARCH ARTICLE

Characterization of eds1, a Mutation in Arabidopsis Suppressing Resistance to Peronospora parasitica Specified by Several Different RPP Genes

J. E. Parker, E. B. Holub, L. N. Frost, A. Falk, N. D. Gunn and M. J. Daniels
Sainsbury Laboratory, Norwich Research Park, Colney Lane, Norwich NR4 7UH, United Kingdom

The interaction between Arabidopsis and the biotrophic oomycete Peronospora parasitica (downy mildew) provides an attractive model pathosystem to identify molecular components of the host that are required for genotype-specific recognition of the parasite. These components are the so-called RPP genes (for resistance to P. parasitica). Mutational analysis of the ecotype Wassilewskija (Ws-0) revealed an RPP-nonspecific locus called EDS1 (for enhanced disease susceptibility) that is required for the function of RPP genes on chromosomes 3 (RPP1/RPP14 and RPP10) and 4 (RPP12). Genetic analyses demonstrated that the eds1 mutation is recessive and is not a defective allele of any known RPP gene, mapping to the bottom arm of chromosome 3 (~13 centimorgans below RPP1/RPP14). Phenotypically, the Ws-eds1 mutant seedlings supported heavy sporulation by P. parasitica isolates that are each diagnostic for one of the RPP genes in wild-type Ws-0; none of the isolates is capable of sporulating on wild-type Ws-0. Ws-eds1 seedlings exhibited enhanced susceptibility to some P. parasitica isolates when compared with a compatible wild-type ecotype, Columbia, and the eds1 parental ecotype, Ws-0. This was observed as earlier initiation of sporulation and elevated production of conidiosporangia. Surprisingly, cotyledons of Ws-eds1 also supported low sporulation by five isolates of P. parasitica from Brassica oleracea. These isolates were unable to sporulate on >100 ecotypes of Arabidopsis, including wild-type Ws-0. An isolate of Albugo candida (white blister) from B. oleracea also sporulated on Ws-eds1, but the mutant exhibited no alteration in phenotype when inoculated with several oomycete isolates from other host species. The bacterial resistance gene RPM1, conferring specific recognition of the avirulence gene avrB from Pseudomonas syringae pv glycinea, was not compromised in Ws-eds1 plants. The mutant also retained full responsiveness to the chemical inducer of systemic acquired resistance, 2,6-dichloroisonicotinic acid; Ws-eds1 seedlings treated with 2,6-dichloroisonicotinic acid became resistant to the Ws-0-compatible and Ws-0-incompatible P. parasitica isolates Emwa1 and Noco2, respectively. In summary, the EDS1 gene appears to be a necessary component of the resistance response specified by several RPP genes and is likely to function upstream from the convergence of disease resistance pathways in Arabidopsis.

This article has been cited by other articles:

				M. Yasuda, A. Ishikawa, Y. Jikumaru, M. Seki, T. Umezawa, T. Asami, A. Maruyama-Nakashita, T. Kudo, K. Shinozaki, S. Yoshida, et al. Antagonistic Interaction between Systemic Acquired Resistance and the Abscisic Acid-Mediated Abiotic Stress Response in Arabidopsis PLANT CELL, June 1, 2008; 20(6): 1678 - 1692. [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]

				R. W.M. Fung, M. Gonzalo, C. Fekete, L. G. Kovacs, Y. He, E. Marsh, L. M. McIntyre, D. P. Schachtman, and W. Qiu Powdery Mildew Induces Defense-Oriented Reprogramming of the Transcriptome in a Susceptible But Not in a Resistant Grapevine Plant Physiology, January 1, 2008; 146(1): 236 - 249. [Abstract] [Full Text] [PDF]

				L. D. Noel, G. Cagna, J. Stuttmann, L. Wirthmuller, S. Betsuyaku, C.-P. Witte, R. Bhat, N. Pochon, T. Colby, and J. E. Parker Interaction between SGT1 and Cytosolic/Nuclear HSC70 Chaperones Regulates Arabidopsis Immune Responses PLANT CELL, December 1, 2007; 19(12): 4061 - 4076. [Abstract] [Full Text] [PDF]

				P. L. Nurmberg, K. A. Knox, B.-W. Yun, P. C. Morris, R. Shafiei, A. Hudson, and G. J. Loake The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response PNAS, November 20, 2007; 104(47): 18795 - 18800. [Abstract] [Full Text] [PDF]

				J. M. Lorang, T. A. Sweat, and T. J. Wolpert Plant disease susceptibility conferred by a "resistance" gene PNAS, September 11, 2007; 104(37): 14861 - 14866. [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]

				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]

				Y. Wang, B.-W. Yun, E. Kwon, J. K. Hong, J. Yoon, and G. J Loake S-Nitrosylation: an emerging redox-based post-translational modification in plants J. Exp. Bot., May 1, 2006; 57(8): 1777 - 1784. [Abstract] [Full Text] [PDF]

				J. Ellis Insights into nonhost disease resistance: can they assist disease control in agriculture? PLANT CELL, March 1, 2006; 18(3): 523 - 528. [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. Feechan, E. Kwon, B.-W. Yun, Y. Wang, J. A. Pallas, and G. J. Loake A central role for S-nitrosothiols in plant disease resistance PNAS, May 31, 2005; 102(22): 8054 - 8059. [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]

				S. Bieri, S. Mauch, Q.-H. Shen, J. Peart, A. Devoto, C. Casais, F. Ceron, S. Schulze, H.-H. Steinbiss, K. Shirasu, et al. RAR1 Positively Controls Steady State Levels of Barley MLA Resistance Proteins and Enables Sufficient MLA6 Accumulation for Effective Resistance PLANT CELL, December 1, 2004; 16(12): 3480 - 3495. [Abstract] [Full Text] [PDF]

				S. Lorrain, B. Lin, M. C. Auriac, T. Kroj, P. Saindrenan, M. Nicole, C. Balague, and D. Roby VASCULAR ASSOCIATED DEATH1, a Novel GRAM Domain-Containing Protein, Is a Regulator of Cell Death and Defense Responses in Vascular Tissues PLANT CELL, August 1, 2004; 16(8): 2217 - 2232. [Abstract] [Full Text] [PDF]

				M. Tor, D. Brown, A. Cooper, A. Woods-Tor, K. Sjolander, J. D.G. Jones, and E. B. Holub Arabidopsis Downy Mildew Resistance Gene RPP27 Encodes a Receptor-Like Protein Similar to CLAVATA2 and Tomato Cf-9 Plant Physiology, June 1, 2004; 135(2): 1100 - 1112. [Abstract] [Full Text] [PDF]

				X. Dong The Role of Membrane-Bound Ankyrin-Repeat Protein ACD6 in Programmed Cell Death and Plant Defense Sci. Signal., February 24, 2004; 2004(221): pe6 - pe6. [Abstract] [Full Text] [PDF]

				X.-C. Zhang and W. Gassmann RPS4-Mediated Disease Resistance Requires the Combined Presence of RPS4 Transcripts with Full-Length and Truncated Open Reading Frames PLANT CELL, October 1, 2003; 15(10): 2333 - 2342. [Abstract] [Full Text] [PDF]

				Y. Shirano, P. Kachroo, J. Shah, and D. F. Klessig A Gain-of-Function Mutation in an Arabidopsis Toll Interleukin1 Receptor-Nucleotide Binding Site-Leucine-Rich Repeat Type R Gene Triggers Defense Responses and Results in Enhanced Disease Resistance PLANT CELL, December 1, 2002; 14(12): 3149 - 3162. [Abstract] [Full Text] [PDF]

				N. A. Eckardt Plant Disease Susceptibility Genes? PLANT CELL, September 1, 2002; 14(9): 1983 - 1986. [Full Text] [PDF]

				G. J. Rairdan and T. P. Delaney Role of Salicylic Acid and NIM1/NPR1 in Race-Specific Resistance in Arabidopsis Genetics, June 1, 2002; 161(2): 803 - 811. [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]

				M. Tor, P. Gordon, A. Cuzick, T. Eulgem, E. Sinapidou, F. Mert-Turk, C. Can, J. L. Dangl, and E. B. Holub Arabidopsis SGT1b Is Required for Defense Signaling Conferred by Several Downy Mildew Resistance Genes PLANT CELL, May 1, 2002; 14(5): 993 - 1003. [Abstract] [Full Text] [PDF]

				P. Tornero, P. Merritt, A. Sadanandom, K. Shirasu, R. W. Innes, and J. L. Dangl RAR1 and NDR1 Contribute Quantitatively to Disease Resistance in Arabidopsis, and Their Relative Contributions Are Dependent on the R Gene Assayed PLANT CELL, May 1, 2002; 14(5): 1005 - 1015. [Abstract] [Full Text] [PDF]

				K. Maleck, U. Neuenschwander, R. M. Cade, R. A. Dietrich, J. L. Dangl, and J. A. Ryals Isolation and Characterization of Broad-Spectrum Disease-Resistant Arabidopsis Mutants Genetics, April 1, 2002; 160(4): 1661 - 1671. [Abstract] [Full Text] [PDF]

				P. Brodersen, M. Petersen, H. M. Pike, B. Olszak, S. Skov, N. Odum, L. B. Jorgensen, R. E. Brown, and J. Mundy Knockout of Arabidopsis ACCELERATED-CELL-DEATH11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense Genes & Dev., February 15, 2002; 16(4): 490 - 502. [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]

				P. V. Minorsky Plant Physiology, June 1, 2001; 126(2): 471 - 472. [Full Text] [PDF]

				M. Lu, X. Tang, and J.-M. Zhou Arabidopsis NHO1 Is Required for General Resistance against Pseudomonas Bacteria PLANT CELL, February 1, 2001; 13(2): 437 - 447. [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]

				Q. Pan, Y.-S. Liu, O. Budai-Hadrian, M. Sela, L. Carmel-Goren, D. Zamir, and R. Fluhr Comparative Genetics of Nucleotide Binding Site-Leucine Rich Repeat Resistance Gene Homologues in the Genomes of Two Dicotyledons: Tomato and Arabidopsis Genetics, May 1, 2000; 155(1): 309 - 322. [Abstract] [Full Text]

				D. Jirage, T. L. Tootle, T. L. Reuber, L. N. Frost, B. J. Feys, J. E. Parker, F. M. Ausubel, and J. Glazebrook Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling PNAS, November 9, 1999; 96(23): 13583 - 13588. [Abstract] [Full Text] [PDF]

				C. Nawrath and J.-P. Métraux Salicylic Acid Induction–Deficient Mutants of Arabidopsis Express PR-2 and PR-5 and Accumulate High Levels of Camalexin after Pathogen Inoculation PLANT CELL, August 1, 1999; 11(8): 1393 - 1404. [Abstract] [Full Text]

				R. F. Warren, P. M. Merritt, E. Holub, and R. W. Innes Identification of Three Putative Signal Transduction Genes Involved in R Gene-Specified Disease Resistance in Arabidopsis Genetics, May 1, 1999; 152(1): 401 - 412. [Abstract] [Full Text]

				A. Falk, B. J. Feys, L. N. Frost, J. D. G. Jones, M. J. Daniels, and J. E. Parker EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases PNAS, March 16, 1999; 96(6): 3292 - 3297. [Abstract] [Full Text] [PDF]

				J. Shah, P. Kachroo, and D. F. Klessig The Arabidopsis ssi1 Mutation Restores Pathogenesis-Related Gene Expression in npr1 Plants and Renders Defensin Gene Expression Salicylic Acid Dependent PLANT CELL, February 1, 1999; 11(2): 191 - 206. [Abstract] [Full Text]

				J.-B. Morel and J. L. Dangl Suppressors of the Arabidopsis lsd5 Cell Death Mutation Identify Genes Involved in Regulating Disease Resistance Responses Genetics, January 1, 1999; 151(1): 305 - 319. [Abstract] [Full Text]

				M. A. Botella, J. E. Parker, L. N. Frost, P. D. Bittner-Eddy, J. L. Beynon, M. J. Daniels, E. B. Holub, and J. D. G. Jones Three Genes of the Arabidopsis RPP1 Complex Resistance Locus Recognize Distinct Peronospora parasitica Avirulence Determinants PLANT CELL, November 1, 1998; 10(11): 1847 - 1860. [Abstract] [Full Text] [PDF]

				R. F. Warren, A. Henk, P. Mowery, E. Holub, and R. W. Innes A Mutation within the Leucine-Rich Repeat Domain of the Arabidopsis Disease Resistance Gene RPS5 Partially Suppresses Multiple Bacterial and Downy Mildew Resistance Genes PLANT CELL, September 1, 1998; 10(9): 1439 - 1452. [Abstract] [Full Text]

				N. Aarts, M. Metz, E. Holub, B. J. Staskawicz, M. J. Daniels, and J. E. Parker Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis PNAS, August 18, 1998; 95(17): 10306 - 10311. [Abstract] [Full Text] [PDF]

				K. E. Hammond-Kosack, S. Tang, K. Harrison, and J. D. G. Jones The Tomato Cf-9 Disease Resistance Gene Functions in Tobacco and Potato to Confer Responsiveness to the Fungal Avirulence Gene Product Avr 9 PLANT CELL, August 1, 1998; 10(8): 1251 - 1266. [Abstract] [Full Text]

				S. M. Volko, T. Boller, and F. M. Ausubel Isolation of New Arabidopsis Mutants With Enhanced Disease Susceptibility to Pseudomonas syringae by Direct Screening Genetics, June 1, 1998; 149(2): 537 - 548. [Abstract] [Full Text] [PDF]

				N. Zhou, T. L. Tootle, F. Tsui, D. F. Klessig, and J. Glazebrook PAD4 Functions Upstream from Salicylic Acid to Control Defense Responses in Arabidopsis PLANT CELL, June 1, 1998; 10(6): 1021 - 1030. [Abstract] [Full Text]

				K. S. Century, A. D. Shapiro, P. P. Repetti, D. Dahlbeck, E. Holub, and B. J. Staskawicz NDR1, a Pathogen-Induced Component Required for Arabidopsis Disease Resistance Science, December 12, 1997; 278(5345): 1963 - 1965. [Abstract] [Full Text]

				Y Yang, J Shah, and D F Klessig Signal perception and transduction in plant defense responses. Genes & Dev., July 1, 1997; 11(13): 1621 - 1639. [PDF]

				B. Baker, P. Zambryski, B. Staskawicz, and S. P. Dinesh-Kumar Signaling in Plant-Microbe Interactions Science, May 2, 1997; 276(5313): 726 - 733. [Abstract] [Full Text]