The Lesion-Mimic Mutant cpr22 Shows Alterations in Abscisic Acid Signaling and Abscisic Acid Insensitivity in a Salicylic Acid-Dependent Manner1[W][OA]

A number of Arabidopsis (Arabidopsis thaliana) lesion-mimic mutants exhibit alterations in both abiotic stress responses and pathogen resistance. One of these mutants, constitutive expresser of PR genes22 (cpr22), which has a mutation in two cyclic nucleotide-gated ion channels, is a typical lesion-mimic mutant exhibiting elevated levels of salicylic acid (SA), spontaneous cell death, constitutive expression of defense-related genes, and enhanced resistance to various pathogens; the majority of its phenotypes are SA dependent. These defense responses in cpr22 are suppressed under high-humidity conditions and enhanced by low humidity. After shifting plants from high to low humidity, the cpr22 mutant, but not the wild type, showed a rapid increase in SA levels followed by an increase in abscisic acid (ABA) levels. Concomitantly, genes for ABA metabolism were up-regulated in the mutant. The expression of a subset of ABA-inducible genes, such as RD29A and KIN1/2, was down-regulated, but that of other genes, like ABI1 and HAB1, was up-regulated in cpr22 after the humidity shift. cpr22 showed reduced responsiveness to ABA not only in abiotic stress responses but also in germination and stomatal closure. Double mutant analysis with nahG plants that degrade SA indicated that these alterations in ABA signaling were attributable to elevated SA levels. Furthermore, cpr22 displayed suppressed drought responses by long-term drought stress. Taken together, these results suggest an effect of SA on ABA signaling/abiotic stress responses during the activation of defense responses in cpr22.

[1]  W. Moeder,et al.  Environmental Sensitivity in Pathogen Resistant Arabidopsis Mutants , 2009 .

[2]  P. McCourt,et al.  Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins , 2009, Science.

[3]  Jonathan D. G. Jones,et al.  Hormone (Dis)harmony Moulds Plant Health and Disease , 2009, Science.

[4]  Ying Zhu,et al.  Analysis of temperature modulation of plant defense against biotrophic microbes. , 2009, Molecular plant-microbe interactions : MPMI.

[5]  Naohiro Kato,et al.  Identification of a functionally essential amino acid for Arabidopsis cyclic nucleotide gated ion channels using the chimeric AtCNGC11/12 gene. , 2008, The Plant journal : for cell and molecular biology.

[6]  Anna Wawrzyńska,et al.  Powdery Mildew Resistance Conferred by Loss of the ENHANCED DISEASE RESISTANCE1 Protein Kinase Is Suppressed by a Missense Mutation in KEEP ON GOING, a Regulator of Abscisic Acid Signaling1[W][OA] , 2008, Plant Physiology.

[7]  D. Klessig,et al.  Systemic acquired resistance: the elusive signal(s). , 2008, Current opinion in plant biology.

[8]  W. Moeder,et al.  Lesion mimic mutants , 2008, Plant signaling & behavior.

[9]  P. McCourt,et al.  A Novel Role for Protein Farnesylation in Plant Innate Immunity1[C][W][OA] , 2008, Plant Physiology.

[10]  K. Shinozaki,et al.  Antagonistic Interaction between Systemic Acquired Resistance and the Abscisic Acid–Mediated Abiotic Stress Response in Arabidopsis[W] , 2008, The Plant Cell Online.

[11]  George W Bassel,et al.  Elucidating the Germination Transcriptional Program Using Small Molecules1[W][OA] , 2008, Plant Physiology.

[12]  R. Ali,et al.  The chimeric cyclic nucleotide-gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner , 2007, Plant Molecular Biology.

[13]  David Mackey,et al.  Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. , 2007, Annual review of phytopathology.

[14]  Murray Grant,et al.  Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease , 2007, The EMBO journal.

[15]  P. Mohr,et al.  Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato , 2007, Functional & Integrative Genomics.

[16]  R. Vierstra,et al.  KEEP ON GOING, a RING E3 Ligase Essential for Arabidopsis Growth and Development, Is Involved in Abscisic Acid Signaling[W] , 2006, The Plant Cell Online.

[17]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[18]  Sheng Yang He,et al.  Plant Stomata Function in Innate Immunity against Bacterial Invasion , 2006, Cell.

[19]  Uwe Conrath,et al.  Systemic Acquired Resistance , 2006, Plant signaling & behavior.

[20]  S. J. Ambrose,et al.  Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. , 2006, The Plant journal : for cell and molecular biology.

[21]  K. Shinozaki,et al.  Functional Analysis of an Arabidopsis Transcription Factor, DREB2A, Involved in Drought-Responsive Gene Expression[W][OA] , 2006, The Plant Cell Online.

[22]  D. Klessig,et al.  The Chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 Activates Multiple Pathogen Resistance Responses[W][OA] , 2006, The Plant Cell Online.

[23]  C. Lamb,et al.  Systemic immunity. , 2006, Current opinion in plant biology.

[24]  T. Kuromori,et al.  ABA-Hypersensitive Germination3 Encodes a Protein Phosphatase 2C (AtPP2CA) That Strongly Regulates Abscisic Acid Signaling during Germination among Arabidopsis Protein Phosphatase 2Cs1[W] , 2005, Plant Physiology.

[25]  K. Shinozaki,et al.  A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. , 2005, The Plant journal : for cell and molecular biology.

[26]  Felix Mauch,et al.  The role of abscisic acid in plant-pathogen interactions. , 2005, Current opinion in plant biology.

[27]  Zhong Zheng,et al.  High humidity represses Cf-4/Avr4- and Cf-9/Avr9-dependent hypersensitive cell death and defense gene expression , 2005, Planta.

[28]  E. Nambara,et al.  Abscisic acid biosynthesis and catabolism. , 2005, Annual review of plant biology.

[29]  T. Kuromori,et al.  ABA-Hypersensitive Germination 3 Encodes a Protein Phosphatase 2 C ( AtPP 2 CA ) That Strongly Regulates Abscisic Acid Signaling during Germination among Arabidopsis Protein Phosphatase 2 Cs 1 [ W ] , 2005 .

[30]  Xiaojing Guo,et al.  The ABI2-dependent abscisic acid signalling controls HrpN-induced drought tolerance in Arabidopsis , 2005, Planta.

[31]  Jean YH Yang,et al.  Bioconductor: open software development for computational biology and bioinformatics , 2004, Genome Biology.

[32]  D. Klessig,et al.  High humidity suppresses ssi4-mediated cell death and disease resistance upstream of MAP kinase activation, H2O2 production and defense gene expression. , 2004, The Plant journal : for cell and molecular biology.

[33]  Rafael A. Irizarry,et al.  A Model-Based Background Adjustment for Oligonucleotide Expression Arrays , 2004 .

[34]  Heribert Hirt,et al.  Plant PP2C phosphatases: emerging functions in stress signaling. , 2004, Trends in plant science.

[35]  Shashi Sharma,et al.  Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the "defense, no death" phenotype. , 2004, Molecular plant-microbe interactions : MPMI.

[36]  Jing Li,et al.  The WRKY70 Transcription Factor: A Node of Convergence for Jasmonate-Mediated and Salicylate-Mediated Signals in Plant Defense On-line version contains Web-only data. , 2004, The Plant Cell Online.

[37]  M. C. Heath Hypersensitive response-related death , 2000, Plant Molecular Biology.

[38]  K. Shinozaki,et al.  Regulatory network of gene expression in the drought and cold stress responses. , 2003, Current opinion in plant biology.

[39]  J. Tumlinson,et al.  Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  T. McNellis,et al.  Regulation of Arabidopsis COPINE 1 Gene Expression in Response to Pathogens and Abiotic Stimuli1 , 2003, Plant Physiology.

[41]  P. Mohr,et al.  Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. , 2003, Functional plant biology : FPB.

[42]  D. Roby,et al.  HLM1, an Essential Signaling Component in the Hypersensitive Response, Is a Member of the Cyclic Nucleotide–Gated Channel Ion Channel Family Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006999. , 2003, The Plant Cell Online.

[43]  C. Brearley,et al.  Enhanced Transcription of the Arabidopsis Disease Resistance Genes RPW8.1 and RPW8.2 via a Salicylic Acid–Dependent Amplification Circuit Is Required for Hypersensitive Cell Death Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006940. , 2003, The Plant Cell Online.

[44]  M. Höfte,et al.  Abscisic Acid Determines Basal Susceptibility of Tomato toBotrytis cinerea and Suppresses Salicylic Acid-Dependent Signaling Mechanisms1 , 2002, Plant Physiology.

[45]  D. Klessig,et al.  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 , 2002 .

[46]  T. McNellis,et al.  A Humidity-Sensitive Arabidopsis Copine Mutant Exhibits Precocious Cell Death and Increased Disease Resistance , 2001, The Plant Cell Online.

[47]  D. Klessig,et al.  Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. , 2001, The Plant journal : for cell and molecular biology.

[48]  F. Ausubel,et al.  Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[49]  S. Beer,et al.  Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. , 1999, The Plant journal : for cell and molecular biology.

[50]  Jonathan D. G. Jones,et al.  EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[51]  S. Naito,et al.  Characterization of an Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABA-dependent and ABA-independent accumulation of free amino acids during dehydration. , 1998, Plant & cell physiology.

[52]  A. Bent,et al.  Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Jörg Durner,et al.  Salicylic acid and disease resistance in plants , 1997 .

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

[55]  P. McCourt,et al.  A Protein Farnesyl Transferase Involved in Abscisic Acid Signal Transduction in Arabidopsis , 1996, Science.

[56]  K. Hammond-Kosack,et al.  Race-Specific Elicitors of Cladosporium fulvum Induce Changes in Cell Morphology and the Synthesis of Ethylene and Salicylic Acid in Tomato Plants Carrying the Corresponding Cf Disease Resistance Gene , 1996, Plant physiology.

[57]  K. Hammond-Kosack,et al.  Involvement of Reactive Oxygen Species, Glutathione Metabolism, and Lipid Peroxidation in the Cf-Gene-Dependent Defense Response of Tomato Cotyledons Induced by Race-Specific Elicitors of Cladosporium fulvum , 1996, Plant physiology.

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

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

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

[61]  S. Sharma,et al.  Reversal of ABA-Induced Stomatal Closure by Phenolic Compounds , 1986 .

[62]  H H Flor,et al.  Current Status of the Gene-For-Gene Concept , 1971 .

[63]  G. Samuel Some Experiments On Inoculating Methods With Plant Viruses, And On Local Lesions , 1931 .