Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms.

A new allele of the coronatine-insensitive locus (COI1) was isolated in a screen for Arabidopsis thaliana mutants with enhanced resistance to the bacterial pathogen Pseudomonas syringae. This mutant, designated coi1-20, exhibits robust resistance to several P. syringae isolates but remains susceptible to the virulent pathogens Erisyphe and cauliflower mosaic virus. Resistance to P. syringae strain PstDC3000 in coi1-20 plants is correlated with hyperactivation of PR-1 expression and accumulation of elevated levels of salicylic acid (SA) following infection, suggesting that the SA-mediated defense response pathway is sensitized in this mutant. Restriction of growth of PstDC3000 in coi1-20 leaves is partially dependent on NPR1 and fully dependent on SA, indicating that SA-mediated defenses are required for restriction of PstDC3000 growth in coi1-20 plants. Surprisingly, despite high levels of PstDC3000 growth in coi1-20 plants carrying the salicylate hydroxylase (nahG) transgene, these plants do not exhibit disease symptoms. Thus resistance to P. syringae in coi1-20 plants is conferred by two different mechanisms: (i) restriction of pathogen growth via activation of the SA-dependent defense pathway; and (ii) an SA-independent inability to develop disease symptoms. These findings are consistent with the hypotheses that the P. syringae phytotoxin coronatine acts to promote virulence by inhibiting host defense responses and by promoting lesion formation.

[1]  M. Ullrich,et al.  Interactions of Pseudomonas syringae pv. glycinea with host and nonhost plants in relation to temperature and phytotoxin synthesis. , 2000, Molecular plant-microbe interactions : MPMI.

[2]  J. Greenberg,et al.  Uncoupling salicylic acid-dependent cell death and defense-related responses from disease resistance in the Arabidopsis mutant acd5. , 2000, Genetics.

[3]  R. Creelman,et al.  Jasmonic Acid Signaling Modulates Ozone-Induced Hypersensitive Cell Death , 2000, Plant Cell.

[4]  M. C. Heath.  Nonhost resistance and nonspecific plant defenses. , 2000, Current opinion in plant biology.

[5]  E. T. Palva,et al.  Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. , 2000, Molecular plant-microbe interactions : MPMI.

[6]  S. Somerville,et al.  Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[7]  D. Guttman,et al.  The Gain-of-Function Arabidopsis acd6 Mutant Reveals Novel Regulation and Function of the Salicylic Acid Signaling Pathway in Controlling Cell Death, Defenses, and Cell Growth , 1999, Plant Cell.

[8]  D. Gross,et al.  Pseudomonas syringae Phytotoxins: Mode of Action, Regulation, and Biosynthesis by Peptide and Polyketide Synthetases , 1999, Microbiology and Molecular Biology Reviews.

[9]  T. Boller,et al.  Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. , 1999, The Plant journal : for cell and molecular biology.

[10]  R. Dixon,et al.  Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory , 1999, Current Biology.

[11]  D. Klessig,et al.  The Arabidopsis ssi1 Mutation Restores Pathogenesis-Related Gene Expression in npr1 Plants and Renders Defensin Gene Expression Salicylic Acid Dependent , 1999, Plant Cell.

[12]  B. Thomma,et al.  Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  J. Boch,et al.  Analysis of Resistance Gene-Mediated Defense Responses in Arabidopsis thaliana Plants Carrying a Mutation in CPR5 , 1998 .

[14]  P. Reymond,et al.  Jasmonate and salicylate as global signals for defense gene expression. , 1998, Current opinion in plant biology.

[15]  C. Pieterse,et al.  A Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis , 1998, Plant Cell.

[16]  Xinnian Dong,et al.  SA, JA, ethylene, and disease resistance in plants. , 1998, Current opinion in plant biology.

[17]  J. Browse,et al.  A role for jasmonate in pathogen defense of Arabidopsis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. Innes,et al.  An Arabidopsis Mutant with Enhanced Resistance to Powdery Mildew , 1998, Plant Cell.

[19]  Xin Li,et al.  Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  D. Xie,et al.  COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. , 1998, Science.

[21]  I. Mitsuhara,et al.  Antagonistic Effect of Salicylic Acid and Jasmonic Acid on the Expression of Pathogenesis-Related (PR) Protein Genes in Wounded Mature Tobacco Leaves , 1998 .

[22]  D. Klessig,et al.  Uncoupling PR Gene Expression from NPR1 and Bacterial Resistance: Characterization of the Dominant Arabidopsis cpr6-1 Mutant , 1998, Plant Cell.

[23]  S. R. Turcinelli,et al.  Differential expression of a novel gene in response to coronatine, methyl jasmonate, and wounding in the Coi1 mutant of Arabidopsis. , 1998, Plant physiology.

[24]  Harry J. Klee,et al.  Ethylene Regulates the Susceptible Response to Pathogen Infection in Tomato , 1998, Plant Cell.

[25]  F. Ausubel,et al.  Use of Arabidopsis for genetic dissection of plant defense responses. , 1997, Annual review of genetics.

[26]  S. Somerville,et al.  Use of Arabidopsis recombinant inbred lines reveals a monogenic and a novel digenic resistance mechanism to Xanthomonas campestris pv campestris. , 1997, The Plant journal : for cell and molecular biology.

[27]  R. Creelman,et al.  Jasmonate is essential for insect defense in Arabidopsis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[28]  S. Dinesh-Kumar,et al.  Signaling in plant-microbe interactions. , 1997, Science.

[29]  R. Dixon,et al.  Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. , 1997, The Plant cell.

[30]  Jane Glazebrook,et al.  The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats , 1997, Cell.

[31]  J. Denecke,et al.  Salicylic acid and the plant pathogen Erwinia carotovora induce defense genes via antagonistic pathways , 1997 .

[32]  Jean-Benoit Morel,et al.  The hypersensitive response and the induction of cell death in plants , 1997, Cell Death and Differentiation.

[33]  Franky R. G. Terras,et al.  Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. , 1996, The Plant cell.

[34]  A. Collmer,et al.  Bacterial Pathogens in Plants: Life up against the Wall. , 1996, The Plant cell.

[35]  Jonathan D. G. Jones,et al.  Resistance gene-dependent plant defense responses. , 1996, The Plant cell.

[36]  J. Ryals,et al.  Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. , 1996, The Plant journal : for cell and molecular biology.

[37]  J. Browse,et al.  The Critical Requirement for Linolenic Acid Is Pollen Development, Not Photosynthesis, in an Arabidopsis Mutant. , 1996, The Plant cell.

[38]  S. Somerville,et al.  Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. , 1996, The Plant journal : for cell and molecular biology.

[39]  D. Xie,et al.  COI1-Dependent Expression of an Arabidopsis Vegetative Storage Protein in Flowers and Siliques and in Response to Coronatine or Methyl Jasmonate , 1995, Plant physiology.

[40]  E. Weiler,et al.  Salicylic Acid Inhibits Synthesis of Proteinase Inhibitors in Tomato Leaves Induced by Systemin and Jasmonic Acid , 1995, Plant physiology.

[41]  K. Davis,et al.  Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. , 1995, Molecular plant-microbe interactions : MPMI.

[42]  S. Somerville,et al.  Expression of defense-related and putative signaling genes during tolerant and susceptible interactions of Arabidopsis with Xanthomonas campestris pv. campestris , 1995 .

[43]  D. Klessig,et al.  A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. , 1994, The Plant cell.

[44]  E. Ward,et al.  A Central Role of Salicylic Acid in Plant Disease Resistance , 1994, Science.

[45]  Xinnian Dong,et al.  Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. , 1994, The Plant cell.

[46]  B. Feys,et al.  Arabidopsis Mutants Selected for Resistance to the Phytotoxin Coronatine Are Male Sterile, Insensitive to Methyl Jasmonate, and Resistant to a Bacterial Pathogen. , 1994, The Plant cell.

[47]  Leslie Friedrich,et al.  Requirement of Salicylic Acid for the Induction of Systemic Acquired Resistance , 1993, Science.

[48]  F. Ausubel,et al.  A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. , 1993, The Plant journal : for cell and molecular biology.

[49]  A. Bent,et al.  RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. , 1993, The Plant cell.

[50]  R. Martienssen,et al.  Arabidopsis thaliana DNA methylation mutants. , 1993, Science.

[51]  J. A. Smith,et al.  Suppression of Bean Defense Responses by Pseudomonas syringae. , 1993, The Plant cell.

[52]  J. Ecker,et al.  Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. , 1992, Molecular plant-microbe interactions : MPMI.

[53]  P. Staswick,et al.  Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[54]  S. Potter,et al.  Acquired resistance in Arabidopsis. , 1992, The Plant cell.

[55]  S. Howell,et al.  Symptom variation in different Arabidopsis thaliana ecotypes produced by cauliflower mosaic virus , 1992 .

[56]  J. Dangl,et al.  Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. , 1991, The Plant journal : for cell and molecular biology.

[57]  A. Bent,et al.  Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. , 1991, The Plant cell.

[58]  S. Somerville,et al.  Identification of a gene in Arabidopsis thaliana that controls resistance to Xanthomonas campestris pv. campestris , 1991 .

[59]  A. Starratt,et al.  Identification of a chromosomal region required for biosynthesis of the phytotoxin coronatine by Pseudomonas syringae pv. tomato , 1989 .

[60]  U. Melcher.  Symptoms of Cauliflower Mosaic Virus Infection in Arabidopsis thaliana and Turnip , 1989, Botanical Gazette.

[61]  R. Dixon,et al.  Signals and transduction mechanisms for activation of plant defenses against microbial attack , 1989, Cell.

[62]  C. Bender,et al.  Reduced pathogen fitness of Pseudomonas syringae pv. tomato Tn5 mutants defective in coronatine production , 1987 .

[63]  J. Schoelz,et al.  Region VI of cauliflower mosaic virus encodes a host range determinant , 1986, Molecular and cellular biology.

[64]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[65]  J. Messing,et al.  The complete nucleotide sequence of an infectious clone of cauliflower mosaic virus by M13mp7 shotgun sequencing. , 1981, Nucleic acids research.

[66]  F. Skoog,et al.  A revised medium for rapid growth and bio assays with tobacco tissue cultures , 1962 .

[67]  King Eo,et al.  Two simple media for the demonstration of pyocyanin and fluorescin. , 1954 .

[68]  E. King,et al.  Two simple media for the demonstration of pyocyanin and fluorescin. , 1954, The Journal of laboratory and clinical medicine.