Systemic Acquired Resistance

In the spectrum of plant-microbe interactions disease is a rare outcome. In many interactions complex, integrated defense mechanisms prevent infection and disease. These defensive systems include preformed physical and chemical barriers as well as inducible defenses such as the strengthening of cell walls or synthesis of antimicrobial compounds (i.e., phytoalexins) and proteins.1,2 In certain cases plants react to pathogen attack by developing long-lasting, broad-spectrum systemic resistance to later attacks by pathogens. This phenomenon, termed systemic acquired resistance (SAR), has been observed in many species and may be ubiquitous among higher plants. In the last five years progress has been made toward understanding the molecular basis of SAR. In this review we first provide a brief history of SAR research, then describe our present knowledge of the manifestation and induction of SAR. We discuss recent findings that indicate a central role for the SAR pathway in plant health and finally present our current working model of SAR induction.

[1]  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.

[2]  E. Ward,et al.  Salicylic acid as a signal molecule in plant-pathogen interactions. , 1994, Current opinion in cell biology.

[3]  A. Ross,et al.  Localized acquired resistance to plant virus infection in hypersensitive hosts. , 1961, Virology.

[4]  J. Beynon,et al.  Phenotypic and genotypic characterization of interactions between isolates of Peronospora parasitica and accessions of Arabidopsis thaliana , 1994 .

[5]  J. Kuc,et al.  Movement of a factor in tobacco infected with Peronospora tabacina Adam which systemically protects against blue mold , 1985 .

[6]  J. Ryals,et al.  Suppression and Restoration of Lesion Formation in Arabidopsis lsd Mutants. , 1995, The Plant cell.

[7]  N. Hoffman,et al.  Ethylene biosynthesis and its regulation in higher plants , 1984 .

[8]  J. Wessels,et al.  Fungal Cell Walls: A Survey , 1981 .

[9]  T. Boller,et al.  Antifungal Hydrolases in Pea Tissue : II. Inhibition of Fungal Growth by Combinations of Chitinase and beta-1,3-Glucanase. , 1988, Plant physiology.

[10]  Leslie Friedrich,et al.  Biological induction of systemic acquired resistance in Arabidopsis , 1993 .

[11]  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.

[12]  A. Simon,et al.  Symptom intensification on cruciferous hosts by the virulent satellite RNA of turnip crinkle virus. , 1990 .

[13]  R. Creelman,et al.  Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[14]  T. K. Kirk,et al.  Lignification as a Mechanism of Disease Resistance , 1980 .

[15]  D. Klessig,et al.  Resistance and susceptible responses of Arabidopsis thaliana to turnip crinkle virus , 1993 .

[16]  T. Boller,et al.  Vacuolar localization of ethylene-induced chitinase in bean leaves. , 1984, Plant physiology.

[17]  S. Volrath,et al.  Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. , 1996, The Plant cell.

[18]  I. Raskin,et al.  Induction of UDP-Glucose:Salicylic Acid Glucosyltransferase Activity in Tobacco Mosaic Virus-Inoculated Tobacco (Nicotiana tabacum) Leaves , 1993, Plant physiology.

[19]  E. Ward,et al.  Systemic Acquired Resistance in Tobacco: Use of Transgenic Expression to Study the Functions of Pathogenesis-Related Proteins , 1993 .

[20]  N. Yalpani,et al.  Partial purification and properties of an inducible uridine 5'-diphosphate-glucose-salicylic Acid glucosyltransferase from oat roots. , 1992, Plant physiology.

[21]  N. Raikhel,et al.  Structure and Function of Chitin-Binding Proteins , 1993 .

[22]  J. Draper,et al.  Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. , 1995, The Plant journal : for cell and molecular biology.

[23]  E. Ward,et al.  The Molecular Biology of Systemic Acquired Resistance , 1993 .

[24]  R. Dixon,et al.  Biologically induced systemic acquired resistance in Arabidopsis thaliana , 1994 .

[25]  J. Dangl,et al.  Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. , 1996, The Plant cell.

[26]  D F Klessig,et al.  Disease response to tobacco mosaic virus in transgenic tobacco plants that constitutively express the pathogenesis-related PR1b gene. , 1989, Virology.

[27]  J. Kuc Induced Immunity to Plant Disease , 1982 .

[28]  R. Dixon,et al.  Molecular Communication in Interactions Between Plants and Microbial Pathogens , 1990 .

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

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

[31]  J. Ryals,et al.  2,6-Dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid , 1995 .

[32]  T. Boller,et al.  Local and systemic induction of chitinase in cucumber plants in response to viral, bacterial and fungal infections , 1986 .

[33]  D. Shah,et al.  Developmental and Pathogen-Induced Activation of the Arabidopsis Acidic Chitinase Promoter. , 1991, The Plant cell.

[34]  I. Raskin,et al.  Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Beynon,et al.  Map positions of three loci in Arabidopsis thaliana associated with isolate-specific recognition of Peronospora parasitica (Downy mildew) , 1994 .

[36]  U. Pfitzner,et al.  Pathogenesis-related proteins in plants , 1999 .

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

[38]  G. Felix,et al.  Resistance to disease in the hybrid Nicotiana glutinosa x Nicotiana debneyi is associated with high constitutive levels of β-1,3-glucanase, chitinase, peroxidase and polyphenoloxidase , 1992 .

[39]  R. Dixon,et al.  Signal transduction in plant immunity. , 1996, Current opinion in immunology.

[40]  J. Kuc,et al.  Induced resistance of cucumber to anthracnose and angular leaf spot by Pseudomonas lachrymans and Colletotrichum lagenarium , 1979 .

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

[42]  N. Madamanchi,et al.  Induced Systemic Resistance in Plants , 1991 .

[43]  R. Dean,et al.  Rapid lignification in response to wounding and infection as a mechanism for induced systemic protection in cucumber , 1987 .

[44]  Ecker The ethylene signal transduction pathway in plants , 1995, Science.

[45]  R. Cressman,et al.  Transgenic Plants with Enhanced Resistance to the Fungal Pathogen Rhizoctonia solani , 1991, Science.

[46]  F. Caruso Protection of Watermelon and Muskmelon Against Colletotrichum lagenarium by Colletotrichum lagenarium , 1977 .

[47]  H. Silva,et al.  Induction, modification, and transduction of the salicylic acid signal in plant defense responses. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[48]  R. Dixon,et al.  Enhanced Protection Against Fungal Attack by Constitutive Co–expression of Chitinase and Glucanase Genes in Transgenic Tobacco , 1994, Bio/Technology.

[49]  H. Kauss,et al.  Pretreatment of Parsley Suspension Cultures with Salicylic Acid Enhances Spontaneous and Elicited Production of H2O2 , 1995, Plant physiology.

[50]  J. Ryals,et al.  Isolation of a complementary DNA encoding a chitinase with structural homology to a bifunctional lysozyme/chitinase. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[51]  E. Farmer,et al.  Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[52]  H. Kauss Some Aspects of Calcium-Dependent Regulation in Plant Metabolism , 1987 .

[53]  F. Katagiri,et al.  Tissue-Specific Expression of as-1 in Transgenic Tobacco. , 1994, The Plant cell.

[54]  J. Metraux,et al.  Systemic Responses in Arabidopsis thaliana Infected and Challenged with Pseudomonas syringae pv syringae , 1995, Plant physiology.

[55]  D. Klessig,et al.  Interconversion of the salicylic acid signal and its glucoside in tobacco. , 1993, The Plant journal : for cell and molecular biology.

[56]  G. Martin,et al.  Map-based cloning of a protein kinase gene conferring disease resistance in tomato. , 1993, Science.

[57]  S. Pan,et al.  Induction of chitinases in tobacco plants systemically protected against blue mold by Peronospora tabacina or tobacco mosaic virus. , 1992 .

[58]  D. Scheel,et al.  Physiology and Molecular Biology of Phenylpropanoid Metabolism , 1989 .

[59]  C. Gessler Induction of Resistance to Fusarium Wilt in Cucumber by Root and Foliar Pathogens , 1982 .

[60]  J. Ellis,et al.  In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants , 1993 .

[61]  P. Hasegawa,et al.  Osmotin overexpression in potato delays development of disease symptoms. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[62]  F. Grundler,et al.  Arabidopsis thaliana as a new model host for plant‐parasitic nematodes , 1991 .

[63]  E. Ward,et al.  Inducible Plant Proteins: Systemic acquired resistance: an inducible defence mechanism in plants , 1992 .

[64]  M. N. Rao,et al.  Induced systemic resistance to blue mold: early induction and accumulation of β-1,3-glucanases, chitinases, and other pathogenesis-related proteins (b-proteins) in immunized tobacco , 1989 .

[65]  P. Low,et al.  The oxidative burst in plant defense: Function and signal transduction , 1996 .

[66]  F. Ausubel,et al.  Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions , 1994, Cell.

[67]  S. Kay,et al.  A novel circadian phenotype based on firefly luciferase expression in transgenic plants. , 1992, The Plant cell.

[68]  D. Klessig,et al.  Temperature-Dependent Induction of Salicylic Acid and Its Conjugates during the Resistance Response to Tobacco Mosaic Virus Infection. , 1992, The Plant cell.

[69]  J. Kuc,et al.  Localized infection with tobacco necrosis virus protects cucumber against Colletotrichum lagenarium , 1977 .

[70]  K TSUGITA,et al.  Tobacco Mosaic Virus , 2008 .

[71]  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.

[72]  P. Staswick Jasmonate, genes, and fragrant signals. , 1992, Plant physiology.

[73]  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.

[74]  F. Ausubel,et al.  An Arabidopsis thaliana Lipoxygenase Gene Can Be Induced by Pathogens, Abscisic Acid, and Methyl Jasmonate , 1993, Plant physiology.

[75]  A. N. Langford Autogenous necrosis in tomatoes immune from Cladosporium fulvum Cooke. , 1948, Canadian journal of research.

[76]  R. Hammerschmidt,et al.  Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium , 1982 .

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

[78]  F. Ausubel,et al.  Virulence of selected phytopathogenic pseudomonads in Arabidopsis thaliana , 1991 .

[79]  T. Boller,et al.  Plant chitinases are potent inhibitors of fungal growth , 1986, Nature.

[80]  R. Dixon THE PHYTOALEXIN RESPONSE: ELICITATION, SIGNALLING AND CONTROL OF HOST GENE EXPRESSION , 1986 .

[81]  D. Bowles,et al.  Defense-related proteins in higher plants. , 1990, Annual review of biochemistry.

[82]  R. Hughes,et al.  The effect of ethylene on phenylalanine ammonia lyase (PAL) induction by a fungal elicitor in Phaseolus vulgaris , 1989 .

[83]  S. Potter,et al.  Regulation of pathogenesis-related protein-1a gene expression in tobacco. , 1993, The Plant cell.

[84]  J. Ryals,et al.  Systemic acquired resistance signal transduction , 1996 .

[85]  J. A. Ryals,et al.  Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. , 1991, The Plant cell.

[86]  Y. Cohen,et al.  Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic methyl ester , 1993 .

[87]  H. H. Flor The Complementary Genic Systems in Flax and Flax Rust , 1956 .

[88]  Jennifer A. Smith,et al.  Pseudomonas syringae pv. syringae induces systemic resistance to Pyricularia oryzae in rice , 1991 .

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

[90]  J. Kuc,et al.  Systemic protection of cucumber plants against disease caused by Cladosporium cucumerinum and Colletotrichum lagenarium by prior infection with either fungus , 1980 .

[91]  W. Nasser,et al.  Maize pathogenesis-related proteins: characterization and cellular distribution of 1,3-β-glucanases and chitinases induced by brome mosaic virus infection or mercuric chloride treatment. , 1990 .

[92]  N. Yalpani,et al.  Induction of UDP-Glucose:Salicylic Acid Glucosyltransferase in Oat Roots. , 1992, Plant physiology.

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

[94]  Z. Kiraly,et al.  Hypersensitivity as a Consequence, Not the Cause, of Plant Resistance to Infection , 1972, Nature.

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

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

[97]  E. Ward,et al.  Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[98]  J. Stougaard Substrate‐dependent negative selection in plants using a bacterial cytosine deaminase gene , 1993 .

[99]  J. Metraux,et al.  A pathogenesis-related protein in cucumber is a chitinase , 1988 .

[100]  F. Caruso Field Protection of Cucumber, Watermelon, and Muskmelon Against Colletotrichum lagenarium by Colletotrichum lagenarium , 1977 .

[101]  B. Mauch-Mani,et al.  Systemic acquired resistance in Arabidopsis thaliana induced by a predisposing infection with a pathogenic isolate of Fusarium oxysporum , 1994 .

[102]  I. Raskin,et al.  Pathway of Salicylic Acid Biosynthesis in Healthy and Virus-Inoculated Tobacco , 1993, Plant physiology.

[103]  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.

[104]  R. Fluhr,et al.  Calcium Requirement for Ethylene-Dependent Responses. , 1992, The Plant cell.

[105]  G. Brimhall The genesis of ores , 1991 .

[106]  M. Sela-Buurlage,et al.  A Novel Pathogen- and Wound-Inducible Tobacco (Nicotiana tabacum) Protein with Antifungal Activity , 1994, Plant physiology.

[107]  E. Ward,et al.  Induction of systemic acquired disease resistance in plants by chemicals. , 1994, Annual review of phytopathology.

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

[109]  N. Keen Gene-for-gene complementarity in plant-pathogen interactions. , 1990, Annual review of genetics.

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

[111]  R. Meuwissen,et al.  Constitutive expression of pathogenesis-related proteins PR-1, GRP, and PR-S in tobacco has no effect on virus infection. , 1989, The Plant cell.

[112]  J. Dangl Applications of Arabidopsis thaliana to outstanding issues in plant-pathogen interactions , 1993 .

[113]  F. Mauch,et al.  Differential Induction of Distinct Glutathione-S-Transferases of Wheat by Xenobiotics and by Pathogen Attack , 1993, Plant physiology.

[114]  J. Bol,et al.  Plant Pathogenesis-Related Proteins Induced by Virus Infection , 1990 .

[115]  S. He,et al.  Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. , 1992, Science.

[116]  L. Heide,et al.  Formation of p-hydroxybenzoic acid from p-coumaric acid by cell free extract of Lithospermum erythrorhizon cell cultures , 1991 .

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

[118]  J. Kuc,et al.  Induced systemic resistance to anthracnose in cucumber as influenced by the location of the inducer inoculation with Colletotrichum lagenarium and the onset of flowering and fruiting , 1980 .

[119]  R. Hammerschmidt,et al.  Histochemistry and Ultrastructure of the Induced Resistance Response of Cucumber Plants to Colletotrichum lagenarium , 1993 .

[120]  Jennifer A. Smith,et al.  Comparative study of acidic peroxidases associated with induced resistance in cucumber, muskmelon and watermelon , 1988 .

[121]  J. Antoniw,et al.  Detection of PR 1-type Proteins in Amaranthaceae, Chenopodiaceae, Graminae and Solanaceae by Immunoelectroblotting , 1987 .

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

[123]  C. Reimmann,et al.  cDNA Cloning and Sequence Analysis of a Pathogen-Induced Thaumatin-Like Protein from Rice (Oryza sativa) , 1993, Plant physiology.

[124]  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.

[125]  R. Hampton,et al.  Resistance to Erysiphe polygoni of Red Clover Infected with Bean Yellow Mosaic Virus , 1964, Science.

[126]  J. H. Elgin,et al.  Characterization of induced resistance to anthracnose in alfalfa by races, isolates, and species of Colletotrichum , 1989 .

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

[128]  F. García-García,et al.  Expression Patterns of Defense-Related Genes in Infected and Uninfected Plants , 1993 .

[129]  R. W. Davis,et al.  Plant defense genes are regulated by ethylene. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[130]  M. Flaishman,et al.  Timing of fungal invasion using host's ripening hormone as a signal. , 1994 .

[131]  A. E. Jenns Graft Transmission of Systemic Resistance of Cucumber to Anthracnose Induced byColletotrichum lagenariumand Tobacco Necrosis Virus , 1979 .

[132]  J. Kuc Aspects of the Protection of Cucumber Against Colletotrichum lagenarium by Colletotrichum lagenarium , 1977 .

[133]  S. Pan,et al.  Association of pathogenesis-related proteins and activities of peroxidase, β-1,3-glucanase and chitinase with systemic induced resistance to blue mould of tobacco but not to systemic tobacco mosaic virus , 1990 .

[134]  J. Kuc,et al.  Characteristics of anthracnose resistance induced by localized infection of cucumber with tobacco necrosis virus , 1980 .

[135]  B. Kunkel,et al.  A useful weed put to work: genetic analysis of disease resistance in Arabidopsis thaliana. , 1996, Trends in genetics : TIG.

[136]  S. Potter,et al.  Regulation of cucumber class III chitinase gene expression. , 1994, Molecular plant-microbe interactions : MPMI.

[137]  I. Raskin,et al.  Endogenous salicylic acid levels correlate with accumulation of pathogenesis-related proteins and virus resistance in tobacco , 1993 .

[138]  H. S. Shetty,et al.  Induced systemic resistance protects pearl millet plants against downy mildew disease due to Sclerospora graminicola , 1993 .

[139]  I. Raskin,et al.  Induction of Benzoic Acid 2-Hydroxylase in Virus-Inoculated Tobacco , 1993, Plant physiology.

[140]  E. Ward,et al.  Induced Systemic Resistance in Cucumber in Response to 2,6-Dichloro-Isonicotinic Acid and Pathogens , 1991 .

[141]  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.

[142]  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.

[143]  K. Century,et al.  NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[144]  S. Potter,et al.  Acquired Resistance Signal Transduction in Arabidopsis Is Ethylene Independent. , 1994, The Plant cell.

[145]  W. K. Roberts,et al.  A new family of plant antifungal proteins. , 1991, Molecular plant-microbe interactions : MPMI.

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

[147]  C. Gessler,et al.  Induced Systemic Resistance in Tomato Plants against Phytophthora infestans , 1986 .

[148]  B. Mauch-Mani,et al.  Production of Salicylic Acid Precursors Is a Major Function of Phenylalanine Ammonia-Lyase in the Resistance of Arabidopsis to Peronospora parasitica. , 1996, The Plant cell.

[149]  N. Chua,et al.  The role of salicylic acid in systemic acquired resistance , 1994 .

[150]  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.

[151]  T. Boller,et al.  Ethylene: Symptom, Not Signal for the Induction of Chitinase and beta-1,3-Glucanase in Pea Pods by Pathogens and Elicitors. , 1984, Plant physiology.

[152]  C. Lamb Plant disease resistance genes in signal perception and transduction , 1994, Cell.

[153]  E. Meyerowitz,et al.  Introduction to the Arabidopsis genome. , 1992 .

[154]  I. Raskin,et al.  Hydrogen Peroxide Stimulates Salicylic Acid Biosynthesis in Tobacco , 1995, Plant physiology.

[155]  A. Slusarenko,et al.  Arabidopsis is susceptible to infection by a downy mildew fungus. , 1990, The Plant cell.

[156]  I. Raskin,et al.  Signal molecules in systemic plant resistance to pathogens and pests , 1992, Cell.

[157]  A. Asselin,et al.  Light-influenced extracellular accumulation of b (pathogenesis-related) proteins in Nicotiana green tissue induced by various chemicals or prolonged floating on water , 1985 .

[158]  C. Woloshuk,et al.  Pathogen-induced proteins with inhibitory activity toward Phytophthora infestans. , 1991, The Plant cell.

[159]  J. Antoniw,et al.  The effects of aspirin and polyacrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. , 1980 .

[160]  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.

[161]  T. J. Morris,et al.  Turnip crinkle virus defective interfering RNAs intensify viral symptoms and are generated de novo. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[162]  J. B. Heale,et al.  Cell death, 6-methoxymellein accumulation, and induced resistance to Botrytis cinerea in carrot root slices , 1987 .

[163]  F. Ausubel,et al.  Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. , 1991, The Plant cell.

[164]  M. Hahn,et al.  Competence for Elicitation of H2O2 in Hypocotyls of Cucumber Is Induced by Breaching the Cuticle and Is Enhanced by Salicylic Acid , 1996, Plant physiology.

[165]  J. Dangl,et al.  Arabidopsis mutants simulating disease resistance response , 1994, Cell.

[166]  G. Hahne,et al.  Sunflower (Helianthus annuus L.) Pathogenesis-Related Proteins (Induction by Aspirin (Acetylsalicylic Acid) and Characterization) , 1993, Plant physiology.

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

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

[169]  J. Kuc,et al.  Relationship of Phytoalexin Accumulation to Local and Systemic Protection of Bean against Anthracnose1) , 1977 .

[170]  B. Steipe,et al.  Evidence against specific binding of salicylic acid to plant catalase , 1995, FEBS letters.

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

[172]  R. Hammerschmidt,et al.  Lignification as a mechanism for induced systemic resistance in cucumber , 1982 .

[173]  M. Mehdy Active Oxygen Species in Plant Defense against Pathogens , 1994, Plant physiology.

[174]  J. Mikkelsen,et al.  Induction, purification and characterization of barley leaf chitinase , 1990 .

[175]  B. Cornelissen,et al.  A tobacco mosaic virus-induced tobacco protein is homologous to the sweet-tasting protein thaumatin , 1986, Nature.

[176]  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.

[177]  R. Blaese,et al.  Transfer of the bacterial gene for cytosine deaminase to mammalian cells confers lethal sensitivity to 5-fluorocytosine: a negative selection system. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

[179]  R. Leah,et al.  Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. , 1995, The Plant journal : for cell and molecular biology.