Systemic Acquired Resistance and Salicylic Acid: Past, Present, and Future.

This article is part of the Distinguished Review Article Series in Conceptual and Methodological Breakthroughs in Molecular Plant-Microbe Interactions. Salicylic acid (SA) is a critical plant hormone that regulates numerous aspects of plant growth and development as well as the activation of defenses against biotic and abiotic stress. Here, we present a historical overview of the progress that has been made to date in elucidating the role of SA in signaling plant immune responses. The ability of plants to develop acquired immunity after pathogen infection was first proposed in 1933. However, most of our knowledge about plant immune signaling was generated over the last three decades, following the discovery that SA is an endogenous defense signal. During this timeframe, researchers have identified i) two pathways through which SA can be synthesized, ii) numerous proteins that regulate SA synthesis and metabolism, and iii) some of the signaling components that function downstream of SA, including a large number of SA targets or receptors. In addition, it has become increasingly evident that SA does not signal immune responses by itself but, rather, as part of an intricate network that involves many other plant hormones. Future efforts to develop a comprehensive understanding of SA-mediated immune signaling will therefore need to close knowledge gaps that exist within the SA pathway itself as well as clarify how crosstalk among the different hormone signaling pathways leads to an immune response that is both robust and optimized for maximal efficacy, depending on the identity of the attacking pathogen.

[1]  S. Yeh,et al.  Potyviral Gene-Silencing Suppressor HCPro Interacts with Salicylic Acid (SA)-Binding Protein 3 to Weaken SA-Mediated Defense Responses. , 2018, Molecular plant-microbe interactions : MPMI.

[2]  Yuelin Zhang,et al.  TGACG-BINDING FACTOR 1 (TGA1) and TGA4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) and CALMODULIN-BINDING PROTEIN 60g (CBP60g). , 2018, The New phytologist.

[3]  D. Klessig,et al.  Members of the abscisic acid co‐receptor PP2C protein family mediate salicylic acid–abscisic acid crosstalk , 2017, bioRxiv.

[4]  J. Steinbrenner,et al.  MORC Proteins: Novel Players in Plant and Animal Health , 2017, Front. Plant Sci..

[5]  Cristiana T Argueso,et al.  Towards engineering of hormonal crosstalk in plant immunity. , 2017, Current opinion in plant biology.

[6]  I. Somssich,et al.  Transcriptional events defining plant immune responses. , 2017, Current opinion in plant biology.

[7]  L. V. Cota,et al.  Comparative transcriptomic analysis indicates genes associated with local and systemic resistance to Colletotrichum graminicola in maize , 2017, Scientific Reports.

[8]  Elisabeth Georgii,et al.  Monoterpenes Support Systemic Acquired Resistance within and between Plants , 2017, Plant Cell.

[9]  Jonathan D. G. Jones,et al.  Protein-protein interactions in the RPS4/RRS1 immune receptor complex , 2017, PLoS pathogens.

[10]  Archana Singh,et al.  Transport of chemical signals in systemic acquired resistance. , 2017, Journal of integrative plant biology.

[11]  C. Abell,et al.  The biochemical properties of the two Arabidopsis thaliana isochorismate synthases , 2017, The Biochemical journal.

[12]  D. Klessig,et al.  How does the multifaceted plant hormone salicylic acid combat disease in plants and are similar mechanisms utilized in humans? , 2017, BMC Biology.

[13]  M. Hartmann,et al.  Biochemical Principles and Functional Aspects of Pipecolic Acid Biosynthesis in Plant Immunity1[OPEN] , 2017, Plant Physiology.

[14]  Daniel H. Huson,et al.  Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus , 2017, Nature.

[15]  Barbara Kracher,et al.  A core function of EDS1 with PAD4 is to protect the salicylic acid defense sector in Arabidopsis immunity. , 2017, The New phytologist.

[16]  Yaru Wang,et al.  TaRar1 Is Involved in Wheat Defense against Stripe Rust Pathogen Mediated by YrSu , 2017, Frontiers in plant science.

[17]  Ying-Tang Lu,et al.  CATALASE2 Coordinates SA-Mediated Repression of Both Auxin Accumulation and JA Biosynthesis in Plant Defenses. , 2017, Cell host & microbe.

[18]  J. E. Peters,et al.  Plant and Human MORC Proteins Have DNA-Modifying Activities Similar to Type II Topoisomerases, but Require One or More Additional Factors for Full Activity. , 2017, Molecular plant-microbe interactions : MPMI.

[19]  A. Mine,et al.  An incoherent feed‐forward loop mediates robustness and tunability in a plant immune network , 2017, EMBO reports.

[20]  Sophie Alvarez,et al.  Arabidopsis thaliana GH3.5 acyl acid amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis , 2016, Proceedings of the National Academy of Sciences.

[21]  S. Ghabrial,et al.  Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. , 2016, The New phytologist.

[22]  S. He,et al.  Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity , 2016, Nature Communications.

[23]  Xin Li,et al.  Characterization of a Pipecolic Acid Biosynthesis Pathway Required for Systemic Acquired Resistance , 2016, Plant Cell.

[24]  Cristiana T Argueso,et al.  No hormone to rule them all: Interactions of plant hormones during the responses of plants to pathogens. , 2016, Seminars in cell & developmental biology.

[25]  D. Klessig,et al.  Multiple Targets of Salicylic Acid and Its Derivatives in Plants and Animals , 2016, Front. Immunol..

[26]  J. Rose,et al.  Orthology Analysis and In Vivo Complementation Studies to Elucidate the Role of DIR1 during Systemic Acquired Resistance in Arabidopsis thaliana and Cucumis sativus , 2016, Front. Plant Sci..

[27]  Prakash P. Kumar,et al.  Plant hormone-mediated regulation of stress responses , 2016, BMC Plant Biology.

[28]  Keshun Yu,et al.  Plasmodesmata Localizing Proteins Regulate Transport and Signaling during Systemic Acquired Immunity in Plants. , 2016, Cell host & microbe.

[29]  Yezhang Ding,et al.  Abscisic acid promotes proteasome-mediated degradation of the transcription coactivator NPR1 in Arabidopsis thaliana. , 2016, The Plant journal : for cell and molecular biology.

[30]  D. Klessig,et al.  Activation of Plant Innate Immunity by Extracellular High Mobility Group Box 3 and Its Inhibition by Salicylic Acid , 2016, PLoS pathogens.

[31]  Stefan Schuck,et al.  Pipecolic Acid Orchestrates Plant Systemic Acquired Resistance and Defense Priming via Salicylic Acid-Dependent and -Independent Pathways , 2015, Plant Cell.

[32]  K. Shirasu,et al.  Plant cells under siege: plant immune system versus pathogen effectors. , 2015, Current opinion in plant biology.

[33]  Chung-Mo Park,et al.  Systemic Immunity Requires SnRK2.8-Mediated Nuclear Import of NPR1 in Arabidopsis , 2015, Plant Cell.

[34]  S. Snyder,et al.  Human GAPDH Is a Target of Aspirin’s Primary Metabolite Salicylic Acid and Its Derivatives , 2015, PloS one.

[35]  Mika Nomoto,et al.  Posttranslational Modifications of the Master Transcriptional Regulator NPR1 Enable Dynamic but Tight Control of Plant Immune Responses. , 2015, Cell host & microbe.

[36]  U. Conrath,et al.  Priming for enhanced defense. , 2015, Annual review of phytopathology.

[37]  G. Ahammed,et al.  Crosstalk among Jasmonate, Salicylate and Ethylene Signaling Pathways in Plant Disease and Immune Responses. , 2015, Current protein & peptide science.

[38]  J. Greenberg,et al.  Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming , 2015, Nature Communications.

[39]  Steve A. Kay,et al.  Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid , 2015, Proceedings of the National Academy of Sciences.

[40]  N. Anjum,et al.  Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants , 2015, Front. Plant Sci..

[41]  G. Montelione,et al.  Aspirin’s Active Metabolite Salicylic Acid Targets High Mobility Group Box 1 to Modulate Inflammatory Responses , 2015, Molecular medicine.

[42]  P. Kachroo,et al.  Signal regulators of systemic acquired resistance , 2015, Front. Plant Sci..

[43]  C. Després,et al.  Integrating data on the Arabidopsis NPR1/NPR3/NPR4 salicylic acid receptors; a differentiating argument , 2015, Front. Plant Sci..

[44]  B. Kuai,et al.  TCP transcription factors are critical for the coordinated regulation of isochorismate synthase 1 expression in Arabidopsis thaliana. , 2015, The Plant journal : for cell and molecular biology.

[45]  M. S. Mukhtar,et al.  TCP three-way handshake: linking developmental processes with plant immunity. , 2015, Trends in plant science.

[46]  G. Friso,et al.  Salicylic Acid Inhibits the Replication of Tomato bushy stunt virus by Directly Targeting a Host Component in the Replication Complex. , 2015, Molecular plant-microbe interactions : MPMI.

[47]  T. Tschaplinski,et al.  ALD1 Regulates Basal Immune Components and Early Inducible Defense Responses in Arabidopsis. , 2015, Molecular plant-microbe interactions : MPMI.

[48]  C. Pieterse,et al.  How salicylic acid takes transcriptional control over jasmonic acid signaling , 2015, Front. Plant Sci..

[49]  L. Holuigue,et al.  Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression , 2015, Front. Plant Sci..

[50]  W. Moeder,et al.  Crossroads of stress responses, development and flowering regulation—the multiple roles of Cyclic Nucleotide Gated Ion Channel 2 , 2015, Plant signaling & behavior.

[51]  G. Friso,et al.  Identification of multiple salicylic acid-binding proteins using two high throughput screens , 2014, Front. Plant Sci..

[52]  B. Snel,et al.  DOWNY MILDEW RESISTANT 6 and DMR6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis. , 2015, The Plant journal : for cell and molecular biology.

[53]  P. Willems,et al.  Plant innate immunity--sunny side up? , 2015, Trends in plant science.

[54]  Keshun Yu,et al.  Mono- and digalactosyldiacylglycerol lipids function nonredundantly to regulate systemic acquired resistance in plants. , 2014, Cell reports.

[55]  Carolin Seyfferth,et al.  Salicylic acid signal transduction: the initiation of biosynthesis, perception and transcriptional reprogramming , 2014, Front. Plant Sci..

[56]  H. Takatsuji,et al.  Development of disease-resistant rice using regulatory components of induced disease resistance , 2014, Front. Plant Sci..

[57]  Monica Höfte,et al.  Making sense of hormone-mediated defense networking: from rice to Arabidopsis , 2014, Front. Plant Sci..

[58]  Dhirendra Kumar,et al.  Salicylic acid signaling in disease resistance. , 2014, Plant science : an international journal of experimental plant biology.

[59]  Robby A. Petros,et al.  Signaling by small metabolites in systemic acquired resistance. , 2014, The Plant journal : for cell and molecular biology.

[60]  D. Wendehenne,et al.  Free radical-mediated systemic immunity in plants. , 2014, Current opinion in plant biology.

[61]  Xinnian Dong,et al.  Perception of the plant immune signal salicylic acid. , 2014, Current opinion in plant biology.

[62]  K. Nordström,et al.  Elevated salicylic acid levels conferred by increased expression of ISOCHORISMATE SYNTHASE 1 contribute to hyperaccumulation of SUMO1 conjugates in the Arabidopsis mutant early in short days 4. , 2014, The Plant journal : for cell and molecular biology.

[63]  Keshun Yu,et al.  Free radicals mediate systemic acquired resistance. , 2014, Cell reports.

[64]  B. Hwang,et al.  An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens , 2014, Journal of experimental botany.

[65]  N. Suzuki,et al.  ROS as key players in plant stress signalling. , 2014, Journal of experimental botany.

[66]  Jessika Adrian,et al.  Elevated Levels of MYB30 in the Phloem Accelerate Flowering in Arabidopsis through the Regulation of FLOWERING LOCUS T , 2014, PloS one.

[67]  K. Miura,et al.  Regulation of water, salinity, and cold stress responses by salicylic acid , 2014, Front. Plant Sci..

[68]  C. Myers,et al.  Mechanisms underlying robustness and tunability in a plant immune signaling network. , 2014, Cell host & microbe.

[69]  F. Faoro,et al.  Systemic acquired resistance (50 years after discovery): moving from the lab to the field. , 2013, Journal of agricultural and food chemistry.

[70]  R. Guérois,et al.  Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. , 2013, Cell host & microbe.

[71]  J. Glazebrook,et al.  Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana , 2013, PLoS genetics.

[72]  Sorina C. Popescu,et al.  The Arabidopsis oligopeptidases TOP1 and TOP2 are salicylic acid targets that modulate SA-mediated signaling and the immune response. , 2013, The Plant journal : for cell and molecular biology.

[73]  S. Gan,et al.  Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism , 2013, Proceedings of the National Academy of Sciences.

[74]  M. S. Mukhtar,et al.  Tell me more: roles of NPRs in plant immunity. , 2013, Trends in plant science.

[75]  P. Palukaitis,et al.  Regulation of RNA-Dependent RNA Polymerase 1 and Isochorismate Synthase Gene Expression in Arabidopsis , 2013, PloS one.

[76]  F. Mauch,et al.  Export of Salicylic Acid from the Chloroplast Requires the Multidrug and Toxin Extrusion-Like Transporter EDS51[W][OPEN] , 2013, Plant Physiology.

[77]  A. Molina,et al.  Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs , 2013, Front. Plant Sci..

[78]  Xinnian Dong,et al.  Systemic acquired resistance: turning local infection into global defense. , 2013, Annual review of plant biology.

[79]  J. Fowler,et al.  A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. , 2013, Cell reports.

[80]  Sofia Hirth,et al.  The Arabidopsis NIMIN proteins affect NPR1 differentially , 2013, Front. Plant Sci..

[81]  G. Glauser,et al.  Induced resistance in maize is based on organ-specific defence responses. , 2013, The Plant journal : for cell and molecular biology.

[82]  N. Havis,et al.  Controlling crop diseases using induced resistance: challenges for the future. , 2013, Journal of experimental botany.

[83]  B. Mauch-Mani,et al.  On the move: induced resistance in monocots. , 2013, Journal of experimental botany.

[84]  J. Shah,et al.  Long-distance communication and signal amplification in systemic acquired resistance , 2013, Front. Plant Sci..

[85]  T. Shiina,et al.  Chloroplast envelope localization of EDS5, an essential factor for salicylic acid biosynthesis in Arabidopsis thaliana , 2013, Plant signaling & behavior.

[86]  Giulia Friso,et al.  The combined use of photoaffinity labeling and surface plasmon resonance-based technology identifies multiple salicylic acid-binding proteins. , 2012, The Plant journal : for cell and molecular biology.

[87]  J. Zeier,et al.  Pipecolic Acid, an Endogenous Mediator of Defense Amplification and Priming, Is a Critical Regulator of Inducible Plant Immunity[W] , 2012, Plant Cell.

[88]  C. Pieterse,et al.  Hormonal modulation of plant immunity. , 2012, Annual review of cell and developmental biology.

[89]  D. Klessig,et al.  SOS - too many signals for systemic acquired resistance? , 2012, Trends in plant science.

[90]  Robby A. Petros,et al.  An abietane diterpenoid is a potent activator of systemic acquired resistance. , 2012, The Plant journal : for cell and molecular biology.

[91]  Patrick J. Boyle,et al.  The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. , 2012, Cell reports.

[92]  Zheng Qing Fu,et al.  NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants , 2012, Nature.

[93]  Jian-Min Zhou,et al.  The U-Box/ARM E3 Ligase PUB13 Regulates Cell Death, Defense, and Flowering Time in Arabidopsis1[C][W][OA] , 2012, Plant Physiology.

[94]  S. Spoel,et al.  How do plants achieve immunity? Defence without specialized immune cells , 2012, Nature Reviews Immunology.

[95]  S. Sano,et al.  Chloroplast-mediated activation of plant immune signalling in Arabidopsis , 2012, Nature Communications.

[96]  D. Klessig,et al.  Salicylic Acid Biosynthesis and Metabolism , 2011, The arabidopsis book.

[97]  S. H. Kim,et al.  Pathogen Effectors Target Arabidopsis EDS1 and Alter Its Interactions with Immune Regulators , 2011, Science.

[98]  R. Jeong,et al.  SAG101 Forms a Ternary Complex with EDS1 and PAD4 and Is Required for Resistance Signaling against Turnip Crinkle Virus , 2011, PLoS pathogens.

[99]  D. Klessig,et al.  The Extent to Which Methyl Salicylate Is Required for Signaling Systemic Acquired Resistance Is Dependent on Exposure to Light after Infection1[OA] , 2011, Plant Physiology.

[100]  J. Glazebrook,et al.  CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. , 2011, The Plant journal : for cell and molecular biology.

[101]  Murray Grant,et al.  Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. , 2011, Annual review of phytopathology.

[102]  Elizabeth A. Savory,et al.  The role of NDR1 in pathogen perception and plant defense signaling , 2011, Plant signaling & behavior.

[103]  Mariana Rivas-San Vicente,et al.  Salicylic acid beyond defence: its role in plant growth and development. , 2011, Journal of experimental botany.

[104]  Hua Lu,et al.  Multiple Roles of WIN3 in Regulating Disease Resistance, Cell Death, and Flowering Time in Arabidopsis1[C][W][OA] , 2011, Plant Physiology.

[105]  A. Stromberg,et al.  Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants , 2011, Nature Genetics.

[106]  B. Thomma,et al.  Of PAMPs and Effectors: The Blurred PTI-ETI Dichotomy[OA] , 2011, Plant Cell.

[107]  Minghui Gao,et al.  Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors , 2010, Proceedings of the National Academy of Sciences.

[108]  L. Tong,et al.  Methyl esterase 1 (StMES1) is required for systemic acquired resistance in potato. , 2010, Molecular plant-microbe interactions : MPMI.

[109]  D. Leister,et al.  Redox Regulation of the NPR1-TGA1 System of Arabidopsis thaliana by Nitric Oxide[W][OA] , 2010, Plant Cell.

[110]  R. Huibers,et al.  Balanced Nuclear and Cytoplasmic Activities of EDS1 Are Required for a Complete Plant Innate Immune Response , 2010, PLoS pathogens.

[111]  B. Fan,et al.  Functional Analysis of the Arabidopsis PAL Gene Family in Plant Growth, Development, and Response to Environmental Stress1[W][OA] , 2010, Plant Physiology.

[112]  C. Foyer,et al.  Accumulation of Isochorismate-derived 2,3-Dihydroxybenzoic 3-O-β-d-Xyloside in Arabidopsis Resistance to Pathogens and Ageing of Leaves* , 2010, The Journal of Biological Chemistry.

[113]  A. Vojnov,et al.  Salicylic acid is involved in the Nb-mediated defense responses to Potato virus X in Solanum tuberosum. , 2010, Molecular plant-microbe interactions : MPMI.

[114]  S. Hayat,et al.  EFFECT OF EXOGENOUS SALICYLIC ACID UNDER CHANGING ENVIRONMENT: A REVIEW , 2010 .

[115]  E. Pichersky,et al.  Altering expression of benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMP-triggered immunity in arabidopsis. , 2010, Molecular plant-microbe interactions : MPMI.

[116]  J. Glazebrook,et al.  Network Properties of Robust Immunity in Plants , 2009, PLoS genetics.

[117]  D. Klessig,et al.  Salicylic Acid, a multifaceted hormone to combat disease. , 2009, Annual review of phytopathology.

[118]  Pradeep Kachroo,et al.  Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. , 2009, PLoS genetics.

[119]  P. Genschik,et al.  Proteasome-Mediated Turnover of the Transcription Coactivator NPR1 Plays Dual Roles in Regulating Plant Immunity , 2009, Cell.

[120]  C. Pieterse,et al.  Networking by small-molecule hormones in plant immunity. , 2009, Nature chemical biology.

[121]  R. Okrent,et al.  Arabidopsis GH3.12 (PBS3) Conjugates Amino Acids to 4-Substituted Benzoates and Is Inhibited by Salicylate*S⃞ , 2009, Journal of Biological Chemistry.

[122]  Jane Glazebrook,et al.  Priming in Systemic Plant Immunity , 2009, Science.

[123]  N. Dudareva,et al.  An important role of a BAHD acyl transferase-like protein in plant innate immunity. , 2009, The Plant journal : for cell and molecular biology.

[124]  P. Taylor,et al.  S-Nitrosylation of AtSABP3 Antagonizes the Expression of Plant Immunity* , 2009, Journal of Biological Chemistry.

[125]  E. Pichersky,et al.  Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. , 2008, The Plant journal : for cell and molecular biology.

[126]  Karolina M. Pajerowska-Mukhtar,et al.  Plant Immunity Requires Conformational Charges of NPR1 via S-Nitrosylation and Thioredoxins , 2008, Science.

[127]  D. E. Somers,et al.  The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure , 2007, The Plant journal : for cell and molecular biology.

[128]  Dhirendra Kumar,et al.  Methyl Salicylate Is a Critical Mobile Signal for Plant Systemic Acquired Resistance , 2007, Science.

[129]  P. Staswick,et al.  Dual Regulation Role of GH3.5 in Salicylic Acid and Auxin Signaling during Arabidopsis-Pseudomonas syringae Interaction1[W][OA] , 2007, Plant Physiology.

[130]  J. Zeier,et al.  Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. , 2007, The Plant journal : for cell and molecular biology.

[131]  Youn-sung Kim,et al.  GH3-mediated Auxin Homeostasis Links Growth Regulation with Stress Adaptation Response in Arabidopsis* , 2007, Journal of Biological Chemistry.

[132]  Van Loon Virus Resistance Induced in Plants by Polyacrylic Acid , 2007 .

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

[134]  B. Poinssot,et al.  Priming: getting ready for battle. , 2006, Molecular plant-microbe interactions : MPMI.

[135]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[136]  G. Martin,et al.  Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase. , 2005, Molecular plant-microbe interactions : MPMI.

[137]  J. Glazebrook Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. , 2005, Annual review of phytopathology.

[138]  J. Parker,et al.  Plant immunity: the EDS1 regulatory node. , 2005, Current opinion in plant biology.

[139]  A. Cabral,et al.  Arabidopsis SENESCENCE-ASSOCIATED GENE101 Stabilizes and Signals within an ENHANCED DISEASE SUSCEPTIBILITY1 Complex in Plant Innate Immunityw⃞ , 2005, The Plant Cell Online.

[140]  A. Harvey Millar,et al.  Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana , 2005, Plant Molecular Biology.

[141]  V. Lipka,et al.  Non-host resistance in plants: new insights into an old phenomenon. , 2005, Molecular plant pathology.

[142]  D. Navarre,et al.  Differential characteristics of salicylic acid-mediated signaling in potato , 2004 .

[143]  K. Mysore,et al.  Nonhost resistance: how much do we know? , 2004, Trends in plant science.

[144]  A. Millar,et al.  Salicylic Acid Is an Uncoupler and Inhibitor of Mitochondrial Electron Transport1 , 2004, Plant Physiology.

[145]  D. Klessig,et al.  The salicylic acid signal in plants , 1994, Plant Molecular Biology.

[146]  Cristina Martinez,et al.  Salicylic acid regulates flowering time and links defence responses and reproductive development. , 2004, The Plant journal : for cell and molecular biology.

[147]  Dhirendra Kumar,et al.  High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[148]  Xinnian Dong,et al.  Inducers of Plant Systemic Acquired Resistance Regulate NPR1 Function through Redox Changes , 2003, Cell.

[149]  Martin J. Mueller,et al.  NPR1 Modulates Cross-Talk between Salicylate- and Jasmonate-Dependent Defense Pathways through a Novel Function in the Cytosol Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009159. , 2003, The Plant Cell Online.

[150]  G. Martin,et al.  The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[151]  I. Baldwin,et al.  Fitness costs of induced resistance: emerging experimental support for a slippery concept. , 2002, Trends in plant science.

[152]  Jean-Pierre Métraux,et al.  EDS5, an Essential Component of Salicylic Acid–Dependent Signaling for Disease Resistance in Arabidopsis, Is a Member of the MATE Transporter Family Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010376. , 2002, The Plant Cell Online.

[153]  K. Chapman,et al.  Biochemical and Molecular Inhibition of Plastidial Carbonic Anhydrase Reduces the Incorporation of Acetate into Lipids in Cotton Embryos and Tobacco Cell Suspensions and Leaves 1 , 2002 .

[154]  Frederick M. Ausubel,et al.  Isochorismate synthase is required to synthesize salicylic acid for plant defence , 2001, Nature.

[155]  F. Ausubel,et al.  Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. , 2000, The Plant journal : for cell and molecular biology.

[156]  Jean-Pierre Métraux,et al.  Salicylic Acid Induction–Deficient Mutants of Arabidopsis Express PR-2 and PR-5 and Accumulate High Levels of Camalexin after Pathogen Inoculation , 1999, Plant Cell.

[157]  D. Klessig,et al.  Benzothiadiazole, an inducer of plant defenses, inhibits catalase and ascorbate peroxidase , 1998 .

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

[159]  D. Klessig,et al.  Identification of a Soluble, High-Affinity Salicylic Acid-Binding Protein in Tobacco , 1997, Plant physiology.

[160]  W. Pierpoint The natural history of salicylic acid Plant product and mammalian medicine , 1997 .

[161]  J. Ryals,et al.  The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. , 1997, The Plant cell.

[162]  D. Klessig,et al.  Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. , 1997, Molecular plant-microbe interactions : MPMI.

[163]  D. Klessig,et al.  Salicylic Acid Is a Modulator of Tobacco and Mammalian Catalases* , 1996, The Journal of Biological Chemistry.

[164]  J. Metraux,et al.  Transport of Salicylic Acid in Tobacco Necrosis Virus-Infected Cucumber Plants , 1996, Plant physiology.

[165]  R. Dixon,et al.  Tobacco plants epigenetically suppressed in phenylalanine ammonia‐lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus , 1996 .

[166]  F. Ausubel,et al.  Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. , 1996, Genetics.

[167]  D. Klessig,et al.  Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[168]  J. Ryals,et al.  Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. , 1995, Molecular plant-microbe interactions : MPMI.

[169]  I. Raskin,et al.  Is Salicylic Acid a Translocated Signal of Systemic Acquired Resistance in Tobacco? , 1995, The Plant cell.

[170]  D. Klessig,et al.  Two inducers of plant defense responses, 2,6-dichloroisonicotinec acid and salicylic acid, inhibit catalase activity in tobacco. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[171]  J. Ryals,et al.  Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[174]  E. Farmer,et al.  Two Classes of Plant Antibiotics: Phytoalexins versus "Phytoanticipins" , 1994, The Plant cell.

[175]  E. Ward,et al.  Salicylic Acid Is Not the Translocated Signal Responsible for Inducing Systemic Acquired Resistance but Is Required in Signal Transduction. , 1994, The Plant cell.

[176]  D. Klessig,et al.  Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. , 1993, Science.

[177]  D. Klessig,et al.  Purification and characterization of a soluble salicylic acid-binding protein from tobacco. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

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

[179]  D. Klessig,et al.  Salicylic acid and plant disease resistance , 1992 .

[180]  L. Mcintosh,et al.  Salicylic Acid Regulation of Respiration in Higher Plants: Alternative Oxidase Expression. , 1992, The Plant cell.

[181]  I. Raskin Role of Salicylic Acid in Plants , 1992 .

[182]  R. Hammerschmidt,et al.  Systemic Induction of Salicylic Acid Accumulation in Cucumber after Inoculation with Pseudomonas syringae pv syringae. , 1991, Plant physiology.

[183]  D. Klessig,et al.  Identification of a soluble salicylic acid-binding protein that may function in signal transduction in the plant disease-resistance response. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[184]  I. Raskin,et al.  Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. , 1991, The Plant cell.

[185]  Jennifer A. Smith,et al.  Rapid induction of systemic resistance in cucumber by Pseudomonas syringae pv. syringae , 1991 .

[186]  D F Klessig,et al.  Salicylic Acid: A Likely Endogenous Signal in the Resistance Response of Tobacco to Viral Infection , 1990, Science.

[187]  H. Signer,et al.  Increase in Salicylic Acid at the Onset of Systemic Acquired Resistance in Cucumber , 1990, Science.

[188]  I. Raskin,et al.  Regulation of heat production in the inflorescences of an Arum lily by endogenous salicylic acid. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[189]  R. F. White Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. , 1979, Virology.

[190]  C. F. Cleland Isolation of Flower-inducing and Flower-inhibitory Factors from Aphid Honeydew. , 1974, Plant physiology.

[191]  A. Ajami,et al.  Identification of the Flower-inducing Factor Isolated from Aphid Honeydew as being Salicylic Acid. , 1974, Plant physiology.

[192]  A. van Kammen,et al.  Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. "Samsun" and "Samsun NN". II. Changes in protein constitution after infection with tobacco mosaic virus. , 1970, Virology.

[193]  A. Ross Systemic acquired resistance induced by localized virus infections in plants. , 1961, Virology.

[194]  K. S. Chester The Problem of Acquired Physiological Immunity in Plants , 1933, The Quarterly Review of Biology.