Plant Molecular Biology

, Volume 26, Issue 5, pp 1439–1458 | Cite as

The salicylic acid signal in plants

  • Daniel F. Klessig
  • Jocelyn Malamy

Key words

acquired resistance active oxygen species defense response hypersensitive response pathogenesis-related proteins salicylic acid signal transduction 


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  1. 1.
    Åberg B: Plant growth regulators. XLI. monosubstituted benzoic acids. Swedish J Agric Res 11: 93–105 (1981).Google Scholar
  2. 2.
    Ahl P, Gianinazzi S. b-protein as a constitutive component of highly (TMV) resistant interspecific hybrid of Nicotiana glutinosa x Nicotiana debneyi. Plant Sci Lett 26: 173–181 (1982).Google Scholar
  3. 3.
    Albrecht H, van deRhee MD, Bol JF: Analysis of cis-regulatory elements involved in induction of a tobacco PR-5 gene by virus infection. Plant Mol Biol 18: 155–158 (1992).PubMedGoogle Scholar
  4. 4.
    Alexander D, Goodman RM, Gut-Rella M, Glascock C, Weymann K, Friedrich L, Maddox D, AhlGoy P, Luntz T, Ward E, Ryals J: Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proc Natl Acad Sci USA 90: 7327–7331 (1993).PubMedGoogle Scholar
  5. 5.
    Antoniw JF, White RF: The effects of aspirin and poly-acrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. Phytopath Z 98: 331–341 (1980).Google Scholar
  6. 6.
    Apostol I, Heinstein PF, Low PS: Rapid stimulation of an oxidative burst during elicitation of cultured plant cells. Plant Physiol 90: 109–116 (1989).Google Scholar
  7. 7.
    Beilmann A, Albrecht K, Schultze S, Wanner G, Pfitzner UM: Activation of a truncated PR-1 promoter by endogenous enhancers in transgenic plants. Plant Mol Biol 18: 65–78 (1992).PubMedGoogle Scholar
  8. 8.
    Bell JN, Ryder TB, Wingate VPM, Bailey JA, Lamb CJ: Differential accumulation of plant defense gene transcripts in a compatible and an incompatible plantpathogen interaction. Mol Cell Biol 6: 1615–1623 (1986).PubMedGoogle Scholar
  9. 9.
    Ben-Tal Y, Cleland CF: Uptake and metabolism of [14C] salicylic acid in Lemna gibba G3. Plant Physiol 70: 291–296 (1982).Google Scholar
  10. 10.
    Bol JF, Linthorst HJM, Cornelissen BJC: Plant pathogenesis-related proteins induced by virus infection. Annu Rev Phytopath 28: 113–138 (1990).CrossRefGoogle Scholar
  11. 11.
    Bowler C, Alliote T, DeLoose M, VanMontagu M, Inzé D: The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia. EMBO J 8: 31–38 (1989).PubMedGoogle Scholar
  12. 12.
    Bowler C, VanMontagu M, Inzé D: Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43: 83–116 (1992).CrossRefGoogle Scholar
  13. 13.
    Bowles D: Defense-related proteins in higher plants. Annu Rev Biochem 59: 873–907 (1990).CrossRefPubMedGoogle Scholar
  14. 14.
    Bradley DJ, Kjelbom P, Lamb CJ: Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70: 21–30 (1992).CrossRefPubMedGoogle Scholar
  15. 15.
    Broglie K, Chet I, Holliday M, Cressman R, Biddle P, Knowlton S, Mauvais CJ, Broglie R: Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254: 1194–1197 (1991).Google Scholar
  16. 16.
    Campos N, Bako L, Feldwisch J, Schell J, Palme K: A protein from maize labeled with azido-IAA has novel β-glucosidase activity. Plant J 2: 675–684 (1992).Google Scholar
  17. 17.
    Carr JP, Klessig DF: The pathogenesis-related proteins of plants. In: Setlow JK (ed) Genetic Engineering Principles and Methods, vol. 11, pp. 65–109. Plenum Press, New York/London (1989).Google Scholar
  18. 18.
    Chadha KC, Brown SA: Biosynthesis of phenolic acids in tomato plants infected with Agrobacterium tumefaciens. Can J Bot 52: 2041–2046 (1974).Google Scholar
  19. 19.
    Chen Z, Klessig DF: Identification of a soluble salicylic acid-binding protein that may function in signal transduction in the plant disease resistance response. Proc Natl Acad Sci USA 88: 8179–8183 (1991).PubMedGoogle Scholar
  20. 20.
    Chen Z, Ricigliano J, Klessig DF: Purification and characterization of a soluble salicylic acid-binding protein from tobacco. Proc Natl Acad Sci USA 90: 9533–9537 (1993).PubMedGoogle Scholar
  21. 21.
    Chen Z, Silva H, Klessig DF: Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid Science 262: 1883–1886 (1993).PubMedGoogle Scholar
  22. 22.
    Chester KS: The problem of acquired physiological immunity in plants. Quart Rev Biol 8: 275–324 (1933).CrossRefGoogle Scholar
  23. 23.
    Cleland CF: Isolation of flower-inducing and flowerinhibiting factors from aphid honeydew. Plant Physiol 54: 899–903 (1974).Google Scholar
  24. 24.
    Cleland CF, Ajami A: Identification of the flowerinducing factor isolated from aphid honeydew as salicylic acid. Plant Physiol 54: 904–906 (1974).Google Scholar
  25. 25.
    Cohen JD, Bandurski RS: Chemistry and physiology of the bound auxins. Annu Rev Plant Physiol 33: 403–430 (1982).CrossRefGoogle Scholar
  26. 26.
    Conn EE: Compartmentation of secondary compounds. In: Boudet AM, Alibert G, Marigo G, Lea PJ (eds) Annual Proceedings of the Phytochemical Society of Europe: Membranes and Compartmentation in the Regulation of Plant Functions, vol. 24, pp. 1–28. Clarendon Press, Oxford (1984).Google Scholar
  27. 27.
    Cooper-Driver G, Corner-Zamodits JJ, Swain T: The metabolic fate of hydroxybenzoic acids in plants. Z Naturforsch B 27: 943–946 (1972).Google Scholar
  28. 28.
    Crowell DN, John ME, Russell D, Amasino RM: Characterization of a stress-induced developmentally regulated gene family from soybean Plant Mol Biol 18: 459–466 (1992).PubMedGoogle Scholar
  29. 29.
    Cutt JR, Klessig DF: Salicylic acid in plants: a changing perspective. Pharmaceut Technol 16: 26–34 (1992).Google Scholar
  30. 30.
    Cutt JR, Klessig DF: Pathogenesis-related proteins. In: Boller T, MeinsJr F (eds) Plant Gene Research: Genes Involved in Plant Defense, pp. 209–243. Springer-Verlag, Wien/New York (1992).Google Scholar
  31. 31.
    Davis KR, Schott E, Ausubel FM: Virulence of selected phytopathogenic Pseudomonas in Arabidopsis thaliana. Mol Plant-Microbe Interact 4: 477–488 (1991).Google Scholar
  32. 32.
    Debener T, Lehnackers H, Arnold M, Dangl JL: Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant J 1: 289–302 (1991).Google Scholar
  33. 33.
    Dempsey DA, Wobbe KK, Klessig DF: Resistance and susceptible responses of Arabidopsis thaliana to turnip crinkle virus. Phytopathology 83: 1021–1029 (1993).Google Scholar
  34. 34.
    Dixon RA, Harrison MJ: Activation, structure and organization of genes involved in microbial defense in plants. Adv Genet 28: 165–234 (1990).PubMedGoogle Scholar
  35. 34a.
    Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL. Arabidopsis mutants stimulating disease response. Cell 77: 565–577 (1994).CrossRefPubMedGoogle Scholar
  36. 35.
    Doke N: Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity. Physiol Plant Path 23: 359–367 (1983).Google Scholar
  37. 36.
    Doke N: Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Path 23: 345–357 (1983).Google Scholar
  38. 37.
    Doke N, Ohashi Y: Involvement of O2 --generating systems in the induction of necrotic lesions on tobacco leaves infected with TMV. Physiol Mol Plant Path 32: 163–175 (1988).Google Scholar
  39. 38.
    Duchesne M, Fritig B, Hirth L: Phenylalanine ammonia-lyase in tobacco mosaic virus-infected hypersensitive tobacco; density-labelling evidence of de novo synthesis. Biochim Biophys Acta 485: 465–481 (1977).PubMedGoogle Scholar
  40. 39.
    Enyedi AJ, Raskin I: Induction of UDP-glucose: salicylic acid glucosyltransferase activity in tobacco mosaic virus-inoculated tobacco (Nicotiana tabacum) leaves. Plant Physiol 101: 1375–1380 (1993).PubMedGoogle Scholar
  41. 40.
    Enyedi AJ, Yalpani N, Silverman P, Raskin I: Signal molecules in systemic plant resistance to pathogens and pests. Cell 70: 879–886 (1992).PubMedGoogle Scholar
  42. 41.
    Enyedi AJ, Yalpani N, Silverman P, Raskin I: Localization, conjugation and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci USA 89: 2480–2484 (1992).PubMedGoogle Scholar
  43. 42.
    Estruch JJ, Chriqui D, Grossmann K, Schell J, Spena A: The plant oncogene rolC is responsible for the release of cytokinins from glucoside conjugates. EMBO J 10: 2889–2895 (1991).PubMedGoogle Scholar
  44. 43.
    Estruch JJ, Schell J, Spena A: The protein encoded by the rolB plant oncogene hydrolyzes indole glucoside. EMBO J 10: 3125–3128 (1991).PubMedGoogle Scholar
  45. 44.
    Farmer EE, Johnson RR, Ryan CA: Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol 98: 995–1002 (1992).Google Scholar
  46. 45.
    Fleming TM, McCarthy DA, White RF, Antoniw JF, Mikkelsen JD: Induction and characterization of some of the pathogenesis-related proteins in sugar beet. Physiol Mol Plant Path 39: 147–160 (1991).Google Scholar
  47. 46.
    Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J: Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754–756 (1993).Google Scholar
  48. 47.
    Gianinazzi S: Hypersensibilite aux virus, temperatures et proteines solubles chez le Nicotiana tabacum cv. Xanthi-nc. CR Acad Sci Paris D 270: 2382–2386 (1970).Google Scholar
  49. 48.
    Gianinazzi S, Ahl P: The genetic and molecular basis of b-proteins in the genus Nicotiana. Neth J Plant Path 89: 275–281 (1983).Google Scholar
  50. 49.
    Goldsbrough AP, Albrecht H, Stratford R: Salicylic acid-inducible binding of a tobacco nuclear protein to a 10 bp sequence which is highly conserved amongst stress-inducible genes. Plant J 3: 563–571 (1993).PubMedGoogle Scholar
  51. 49a.
    Greenberg JT, Ausubel FM: Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J 4: 327–341 (1994).Google Scholar
  52. 49b.
    Greenberg JT, Guo A, Klessig DF, Ausubel FM: Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77: 551–563 (1994).PubMedGoogle Scholar
  53. 49c.
    Hahlbrook K, Scheel D: Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40: 347–369 (1989).CrossRefGoogle Scholar
  54. 50.
    Hagiwara H, Matsuoka M, Ohshima M, Watanabe M, Hosokawa D, Ohashi Y: Sequence-specific binding of protein factors to two independent promoter regions of the acidic tobacco pathogenesis-related-1 protein gene (PR-1). Mol Gen Genet 240: 197–205 (1993).PubMedGoogle Scholar
  55. 51.
    Harborne JB: Phenolic glycosides and their natural distribution. In: Harborne JB (ed) Biochemistry of Phenolic Compounds, pp. 129–169. Academic Press. London (1964).Google Scholar
  56. 52.
    Hennig J, Dewey RE, Cutt JR, Klessig DF: Pathogen, salicylic acid and developmental dependent expression of a β-1,3-glucanase/GUS gene fusion in transgenic tobacco plants. Plant J 4: 481–493 (1993).PubMedGoogle Scholar
  57. 53.
    Hennig J, Malamy J, Grynkiewicz G, Indulski J, Klessig DI: Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J 4: 593–600 (1993).PubMedGoogle Scholar
  58. 54.
    Hooft van Huijsduijnen RAM, Alblas SW, deRijk RH, Bol JF: Induction by SA of pathogenesis-related proteins and resistance to alfalfa mosaic virus infection in various plant species. J Gen Virol 67: 2143–2153 (1986).Google Scholar
  59. 55.
    Ishige F, Mori H, Yamazaki K, Imaseki H: Cloning of a complementary DNA that encodes an acidic chitinase which is induced by ethylene and expression of the corresponding gene. Plant Cell Physiol 34: 103–111 (1993).PubMedGoogle Scholar
  60. 56.
    Ishikawa M, Obata F, Kumagai T, Ohno T. Isolation of mutants of Arabidopsis thaliana in which accumulation of tobacco mosaic virus coat protein is reduced to low levels. Mol Gen Genet 230: 33–38 (1991).PubMedGoogle Scholar
  61. 57.
    Kassanis B: Some effects of high temperature on the susceptibility of plants to infection with viruses. Ann Appl Biol 39: 358–369 (1952).Google Scholar
  62. 58.
    Kauss H, Franke R, Krause K, Conrath U, Jeblick W, Grimmig B, Matern U: Conditioning of parsley (Petroselinum crispum L.) suspension cells increases elicitor-induced incorporation of cell wall phenolics. Plant Physiol 102: 459–466 (1933).Google Scholar
  63. 59.
    Keen NT: Pathogenic strategies for fungi. In: Lugtenberg B (ed) Recognition in Microbe-Plant Symbiotic and Pathogenic Interactions. NATO-ASI Series H, vol. 4, pp. 171–188. Springer-Verlag, Berlin/New York (1986).Google Scholar
  64. 60.
    Keppler LD, Baker CJ: O2 --initiated lipid peroxidation in a bacteria-induced hypersensitive reaction in tobacco cell suspensions. Phytopathology 79: 555–562 (1989).Google Scholar
  65. 61.
    Keppler LD, Novacky A: Involvement of membrane lipid peroxidation in the development of a bacterially induced hypersensitive reaction. Phytopathology 76: 104–108 (1986).Google Scholar
  66. 62.
    Kim SR, Kim Y, An G: Identification of methyl jasmonate and salicylic acid response elements from the nopaline synthase (nos) promoter. Plant Physiol 103: 97–103 (1993).PubMedGoogle Scholar
  67. 63.
    Koch E, Slusarenko A: Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2: 437–445 (1990).CrossRefPubMedGoogle Scholar
  68. 64.
    Kunkel BN, Bent AF, Dahlbeck D, Innes RW, Staskawicz B: RPS2, an Arabidopsis disease resistant locus specifying recognition of Pseudomonas syringae expressing the avirulence gene avrRpt2. Plant Cell 5: 865–875 (1993).CrossRefPubMedGoogle Scholar
  69. 64a.
    Lawton KA, Potter SL, Uknes S, Ryals J: Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6: 581–588 (1994).PubMedGoogle Scholar
  70. 64b.
    Lawton KA, Uknes S, Friedrich L, Gaffney T, Alexander D, Goodman R, Métraux JP, Kessman H, Ahl-Goy P, Gut-Rella M, Ward D, Ryals J: The molecular biology of systemic acquired resistance. In: B.Fritig, M.Legrande (eds) Developments in Plant Biology, Mechanisms of Plant Defense Responses, pp. 422–432. Kluwer Academic Publishers, Dordrecht/Boston/London (1993).Google Scholar
  71. 65.
    Lee TT, Skoog F: Effects of substituted phenols on bud formation and growth of tobacco tissue culture. Physiol Plant 18: 386–402 (1965).Google Scholar
  72. 66.
    Legendre L, Rueter S, Heinstein PF, Low PS: Characterization of the oligogalacturonide-induced oxidative burst in cultured soybean (Glycine max) cells. Plant Physiol 102: 233–240 (1993).PubMedGoogle Scholar
  73. 67.
    Leisner SM, Howell SH: Symptom variation in different Arabidopsis thaliana ecotypes produced by cauliflower mosaic virus. Phytopathology 82: 1042–1046 (1992).Google Scholar
  74. 68.
    León J, Yalpani N, Raskin I, Lawton MA: Induction of benzoic acid 2-hydroxylase in virus-inoculated tobacco. Plant Physiol 103: 323–328 (1993).PubMedGoogle Scholar
  75. 69.
    Leslie CA, Romani RJ: Inhibition of ethylene biosynthesis by salicylic acid. Plant Physiol 88: 833–837 (1988).Google Scholar
  76. 70.
    Letham DS, Palni LMS: The biosynthesis and metabolism of cytokinins. Annu Rev Plant Physiol 34: 163–197 (1983).CrossRefGoogle Scholar
  77. 71a.
    Liu D, Raghothama KG, Hasegawa PM, Bressan RA: Osmotin overexpression in potato delays development of disease symptoms. Proc Natl Acad Sci USA 91: 1888–1892 (1994).PubMedGoogle Scholar
  78. 71.
    Linthorst HJM: Pathogenesis-related proteins of plants. Crit Rev Plant Sci 10: 123–150 (1991).Google Scholar
  79. 72.
    Madamanchi NR, Kuć J: Induced systemic resistance in plants. In: Cole GT, Hoch HC (eds) The Fungal Spore and Disease Initiation in Plants and Animals, pp. 347–362. Plenum Press, New York (1991).Google Scholar
  80. 73.
    Malamy J, Klessig DF: Salicylic acid and plant disease resistance. Plant J 2: 643–654 (1992).Google Scholar
  81. 74.
    Malamy J, Carr JP, Klessig DF, Raskin I: Salicylic acid — a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1001–1004 (1990).Google Scholar
  82. 75.
    Malamy J, Hennig J, Klessig DF: Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 4: 359–366 (1992).CrossRefPubMedGoogle Scholar
  83. 76.
    Malamy J, Sánchez-Casas P, Hennig J, Guo A, Klessig DF: Dissection of the salicylic acid signalling pathway for defense responses in tobacco. Plant Physiol, submitted (1994).Google Scholar
  84. 77.
    Matsuta C, van denBulcke M, Bauw G, vanMontagu M, Caplan AG: Differential effects of elicitors on the viability of rice suspension cells. Plant Physiol 97: 619–629 (1991).Google Scholar
  85. 78.
    Matthews REF: Plant Virology, 3rd ed. Harcourt Brace Jovanovich, San Diego, CA (1991).Google Scholar
  86. 79.
    Mauch F, Mauch-Mani B, Boller T: Antifungal hydrolases in pea tissue. II. Inhibition of fungal growth by combinations of β-1,3-glucanase and chitinase. Plant Physiol 88: 936–942 (1988).Google Scholar
  87. 79a.
    Mauch-Mani B, Slusarenko A: Systematic acquired resistance in Arabidopsis thaliana induced by a predisposing infection with a pathogenic isolate of Fusarium oxysporum. Mol Plant-Microbe Interact 7: 378–383 (1994).Google Scholar
  88. 80.
    McGurl B, Pearce G, Orizco-Cardensa M, Ryan C: Structure, expression and antisense inhibition of the systemin precursor gene. Science 255: 1570–1573 (1992).PubMedGoogle Scholar
  89. 81.
    Meeuse BJD: Thermogenic respiration in aroids. Annu Rev Plant Physiol 26: 117–126 (1975).CrossRefGoogle Scholar
  90. 82.
    Melcher U: Symptoms of cauliflower mosaic virus infection in Arabidopsis thaliana and turnip. Bot Gaz 150: 139–147 (1989).CrossRefGoogle Scholar
  91. 83.
    Métraux JP, Ahl-Goy P, Staub T, Speich J, Steinemann A, Ryals J, Ward E: Induced resistance in cucumber in response to 2,6-dichloroisonicotinic acid and pathogens. In: Hennecke H, Verma DPS (eds) Advances in Molecular Genetics of Plant-Microbe Interactions, vol. 1, pp. 432–439. Kluwer Academic Publishers, Dordrecht (1991).Google Scholar
  92. 84.
    Métraux JP, Burkhart W, Moyer M, Dincher S, Middlesteadt W, Williams S, Payne G, Carnes M, Ryals J: Isolation of a complementary DNA encoding a chitinase with structural homology to a bifunctional lysozyme/chitinase. Proc Natl Acad Sci USA 86: 896–900 (1989).PubMedGoogle Scholar
  93. 85.
    Métraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B: Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250: 1004–1006 (1990).Google Scholar
  94. 86.
    Meuwly Ph, Mölders W, Summermatter K, Sticher L, Métraux JP: Salicylic acid and chitinase in infected cucumber plants. Acta Hort, in press (1994).Google Scholar
  95. 87.
    Meyerowitz EM: Arabidopsis, a useful weed. Cell 56: 263–269 (1989).PubMedGoogle Scholar
  96. 88.
    Mills PR, Wood RKS: The effects of polyacrylic acid, aspirin and salicylic acid on resistance of cucumber to Colletotrichum lagenarium. Phytopath Z 111: 209–216 (1984).Google Scholar
  97. 89.
    Ohashi Y, Ohshima M, Itoh H, Matsuoka M, Watanabe S, Murakami T, Hosokawa D: Constitutive expression of stress-inducible genes, including pathogenesis-related 1 protein gene in a transgenic interspecific hybrid of Nicotiana glutinosa x Nicotiana debneyi. Plant Cell Physiol 33: 177–187 (1992).Google Scholar
  98. 90.
    Ohshima M, Itoh H, Matsuoka M, Murakami T, Ohashi Y: Analysis of stress-induced or salicylic acid-induced expression of the pathogenesis-related 1a protein gene in transgenic tobacco. Plant Cell 2: 95–106 (1990).CrossRefPubMedGoogle Scholar
  99. 90a.
    Palva TK, Hurtig M, Saindrenan P, Palva ET: Salicylic acid-induced resistance to Erwinia carotovora subsp. carotovora in tobacco. Mol Plant-Microbe Interact 7: 356–363 (1994).Google Scholar
  100. 91.
    Pegg GF: The involvement of ethylene in plant pathogenesis. In: Heitefuss R, Williams PH (eds) Encyclopedia of Plant Physiology, New Series, vol. 4, pp. 582–591. Springer-Verlag, Heidelberg (1976).Google Scholar
  101. 91a.
    Peña-Cortés H, Albrecht T, Prat S, Water EW, Willmitzer L: Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191: 123–128 (1993).Google Scholar
  102. 92.
    Ponstein AS, Bres-Vloemans SA, Sela-Buurlage MB, van denElzen PJM, Melchers LS, Cornelissen BJC: A novel pathogen- and wound-inducible tobacco (Nicotiana tabacum) protein with antifungal activity. Plant Physiol 104: 109–118 (1994).CrossRefPubMedGoogle Scholar
  103. 93.
    Pucacka S: Role of phenolic compounds in the resistance of poplars to the fungus Dothichiza populae. Arbor Kornickie 25: 257–268 (1980).Google Scholar
  104. 93a.
    Qin XF, Holuigue L, Horvath DM, Chua N-H: Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element. Submitted (1994).Google Scholar
  105. 94.
    Rainsford KD: Aspirin and the Salicylates. Butterworth, London (1984).Google Scholar
  106. 95.
    Raskin I: Role of salicylic acid in plants. Annu Rev Plant Physiol Plant Mol Biol 43: 439–463 (1992).CrossRefGoogle Scholar
  107. 96.
    Raskin I: Salicylate, a new plant hormone. Plant Physiol 99: 799–803 (1992).Google Scholar
  108. 97.
    Raskin I, Ehmann A, Melander WR, Meeuse BJD: Salicylic acid—a natural inducer of heat production in Arum lilies. Science 237: 1601–1602 (1987).Google Scholar
  109. 98.
    Raskin I, Skubatz H, Tang W, Meeuse BJD: Salicylic acid levels in thermogenic and non-thermogenic plants. Ann Bot 66: 369–373 (1990).Google Scholar
  110. 99.
    Raskin I, Turner IM, Melander WR: Regulation of heat production in the inflorescences of an arum lily by endogenous salicylic acid. Proc Natl Acad Sci USA 86: 2214–2218 (1989).Google Scholar
  111. 100.
    Rasmussen JB, Hammerschmidt R, Zook M: Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiol 97: 1342–1347 (1991).Google Scholar
  112. 101.
    Raz V, Fluhr R: Calcium requirement for ethylene-dependent responses. Plant Cell 4: 1123–1130 (1992).CrossRefPubMedGoogle Scholar
  113. 102.
    Reinecke DM, Bandurski RS: Auxin biosynthesis and metabolism. In: Davis PJ (ed) Plant Hormones and their Role in Plant Growth and Development, pp. 24–42. Martinus Nijhoff, Dordrecht (1988).Google Scholar
  114. 103.
    Rhoads DM, McIntosh L: Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. Plant Cell 4: 1131–1139 (1992).CrossRefPubMedGoogle Scholar
  115. 104.
    Rhoads DM, McIntosh L: The salicylic acid-inducible alternative oxidase gene aox1 and genes encoding pathogenesis-related proteins share regions of sequence similarity in their promoters. Plant Mol Biol 21: 615–624 (1993).PubMedGoogle Scholar
  116. 105.
    Rhoads DM, McIntosh L: Cytochrome and alternative pathway respiration in tobacco; effects of salicylic acid. Plant Physiol 103: 877–883 (1993).PubMedGoogle Scholar
  117. 106.
    Roggero P, Pennazio S: Effects of salicylate on systemic invasion of tobacco plants by various viruses. J Phytopath 123: 207–216 (1988).Google Scholar
  118. 107.
    Roggero P, Pennazio S: Salicylate does not induce resistance to plant viruses, or stimulate pathogenesis-related protein production in soybean. Microbiologica 14: 65–69 (1991).Google Scholar
  119. 108.
    Romani RJ, Hess BM, Leslie CA: Salicylic acid inhibition of ethylene production by apple discs and other plant tissues. J Plant Growth Regul 8: 63–70 (1989).Google Scholar
  120. 109.
    Ross AF: Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14: 329–339 (1961).CrossRefPubMedGoogle Scholar
  121. 110.
    Ross AF: Systemic acquired resistance induced by localized virus infections in plants. Virology 14: 340–358 (1961).CrossRefPubMedGoogle Scholar
  122. 111.
    Roustan JP, Latche A, Fallot J: Inhibition of ethylene production and stimulation of carrot somatic embryogenesis by salicylic acid. Biol Plant 32: 273–276 (1990).Google Scholar
  123. 112.
    Ryals J, Ward E, Ahl-Goy P, Métraux JP: Systemic acquired resistance: an inducible defence mechanism in plants. In: Wray JL (ed) Inducible Plant Proteins, pp. 205–229, Society for Experimental Biology Seminar series 49 (1992).Google Scholar
  124. 113.
    Ryan CA: Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopath 28: 425–449 (1990).CrossRefGoogle Scholar
  125. 114.
    Saint-Pierre B, Miville L, Dion P: The effects of salicylates on phenomena related to crown gall. Can J Bot 62: 729–734 (1984).Google Scholar
  126. 115.
    Samac DA, Shah DM: Developmental and pathogen-induced activation of the Arabidopsis acidic chitinase promoter. Plant Cell 3: 1063–1072 (1991).CrossRefPubMedGoogle Scholar
  127. 116.
    Schneider G, Jensen E, Spray C, Phinney BO: Hydrolysis and reconjugation of gibberelin A20 glucosyl ester by seedlings of Zea mays L. Proc Natl Acad Sci USA 89: 8045–8048 (1992).PubMedGoogle Scholar
  128. 117.
    Schreck R, Baeuerle PA: A role for oxygen radicals as second messengers. Trends Cell Biol 1: 39–42 (1991).CrossRefPubMedGoogle Scholar
  129. 118.
    Schultz M, Schnabl H, Manthe B, Schweihofen B, Casser I: Uptake and detoxification of salicylic acid by Vicia faba and Fagopyrum esculentum. Phytochemistry 33: 291–294 (1993).CrossRefGoogle Scholar
  130. 119.
    Sijmons PC, Grundler FMW, vonMende N, Burrows PR, Wyss U: Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant J 1: 245–254 (1991).CrossRefGoogle Scholar
  131. 120.
    Silverman P, Nuckles E, Ye XS, Kuć J, Raskin I: Salicylic acid, ethylene, and pathogen resistance in tobacco. Mol Plant-Microbe Interact 6: 775–781 (1993).Google Scholar
  132. 121.
    Simmons CR, Litts JC, Huang N, Rodriguez RL: Structure of a rice β-glucanase gene regulated by ethylene, cytokinin, wounding, salicylic acid and fungal elicitors. Plant Mol Biol 18: 33–45 (1992).PubMedGoogle Scholar
  133. 122.
    Simon AE, Li XH, Lew JE, Stange R, Zhang C, Polacco M, Carpenter CD: Susceptibility and resistance of Arabidopsis thaliana to turnip crinkle virus. Mol Plant-Microbe Interact 5: 496–503 (1992).Google Scholar
  134. 123.
    Simpson RB, Johnson LJ: Arabidopsis thaliana as a host for Xanthomonas campestris pv. campestris. Mol Plant-Microbe Interact 3: 233–237 (1990).Google Scholar
  135. 124.
    Singh L: In vitro screening of some chemicals against three phytopathogenic fungi. J Indian Bot Soc 57: 191–195 (1978).Google Scholar
  136. 124a.
    Smith JA, Hammerschmidt R, Fulbright DW: Rapid induction of systemic induction of systemic resistance in cucumber by Pseudomonas syringae pv. syringae. Physiol Mol Plant Pathol 38: 223–235 (1991).Google Scholar
  137. 125.
    Sutherland MW: The generation of oxygen radicals during host plant responses to infection. Physiol Mol Plant Path 39: 79–93 (1991).Google Scholar
  138. 126.
    Summermatter K, Meuwly Ph, Mölders W, Métraux JP: Salicylic acid levels in Arabidopsis thaliana after treatments with Pseudomonas syringae or synthetic inducers. Acta Hort, in press (1994).Google Scholar
  139. 126a.
    Takahashi H, Goto N, Ehara Y: Hypersensitive response in cucumber mosaic virus-inoculated Arabidopsis thaliana. Plant J, in press (1994).Google Scholar
  140. 127.
    Tanaka S, Hayakawa K, Umetani Y, Tabata M: Glucosylation of isomeric hydroxybenzoic acids by cell suspension cultures of Mallotus japonicus. Phytochemistry 29: 1555–1558 (1990).CrossRefGoogle Scholar
  141. 128.
    Towers GHN: Metabolism of phenolics in higher plants and microorganisms. In: Harborne JB (ed) Biochemistry of Phenolic Compounds, pp. 249–294. Academic Press, London (1964).Google Scholar
  142. 129.
    Tsuji J, Somerville SC, Hammerschmidt R: Identification of a gene in Arabidopsis thaliana that controls resistance to Xanthomonas campestris pv. campestris. Physiol Mol Plant Path 38: 57–65 (1991).Google Scholar
  143. 130.
    Uknes S, Dincher S, Friedrich L, Negrotto D, Williams S, Thompson-Taylor H, Potter S, Ward E, Ryals J: Regulation of pathogenesis-related protein-1a gene expression in tobacco. Plant Cell 5: 159–169 (1993).CrossRefPubMedGoogle Scholar
  144. 131.
    Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J: Acquired resistance in Arabidopsis. Plant Cell 4: 645–655 (1992).CrossRefPubMedGoogle Scholar
  145. 132.
    Uknes S, Winter AM, Delaney T, Vernooij B, Morse A, Friedrich L, Nye G, Potter S, Ward E, Ryals J: Biological induction of systemic acquired resistance in Arabidopsis. Mol Plant-Microbe Interact 6: 692–698 (1993).Google Scholar
  146. 133.
    Umetani Y, Kodakari E, Yamamura T, Tanaka S, Tabata M: Glucosylation of salicylic acid by cell suspension cultures of Mallotus japonicus. Plant Cell Rep 9: 325–327 (1990).CrossRefGoogle Scholar
  147. 134.
    vanDamme EJM, Willems P, Torrekens S, vanLeuven F, Peumans WJ: Garlic (Allium sativum) chitinases: characterization and molecular cloning. Physiol Plant 87: 177–186 (1993).CrossRefGoogle Scholar
  148. 135.
    vanLoon LC: The induction of pathogenesis-related proteins by pathogens and specific chemicals. Neth J Plant Path 89: 265–273 (1983).Google Scholar
  149. 136.
    vanLoon LC, Antoniw JF: Comparison of the effects of salicylic acid and ethephon with virus-induced hypersensitivity and acquired resistance in tobacco. Neth J Plant Path 88: 237–256 (1982).Google Scholar
  150. 137.
    van deRhee MD, Bol JF: Induction of the tobacco PR-1a gene by virus infection and salicylate treatment involves an interaction between multiple regulatory elements. Plant J 3: 71–82 (1993).Google Scholar
  151. 138.
    van deRhee MD, Lemmers R, Bol JF: Analysis of regulatory elements involved in stress-induced and organ-specific expression of tobacco acidic and basic β-1,3-glucanase genes. Plant Mol Biol 21: 451–461 (1993).PubMedGoogle Scholar
  152. 139.
    van deRhee MD, vanKan JAL, Gonzalez-Jaen MT, Bol JF: Analysis of regulatory elements involved in the induction of two tobacco genes by salicylate treatment and virus infection. Plant Cell 2: 357–366 (1990).CrossRefPubMedGoogle Scholar
  153. 140.
    Vane JR: Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nature-New Biol 231: 232–235 (1971).PubMedGoogle Scholar
  154. 141.
    Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jawhar R, Ward E, Uknes S, Kessmann H, Ryals J: Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6: 959–968 (1994).CrossRefPubMedGoogle Scholar
  155. 142.
    Vigers AJ, Roberts WK, Selitrennikoff CP: A new family of plant antifungal proteins. Mol Plant-Microbe Interact 4: 315–323 (1991).PubMedGoogle Scholar
  156. 143.
    Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhol DL, Alexander DC, Ahl-Goy P, Métraux JP, Ryals J: Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3: 1085–1094 (1991).CrossRefPubMedGoogle Scholar
  157. 144.
    Weete JD: Induced systemic resistance to Alternaria cassiae in sicklepod. Physiol Mol Plant Path 40: 437–445 (1992).Google Scholar
  158. 145.
    Weissman G: Aspirin. Sci Am 264: 84–90 (1991).Google Scholar
  159. 146.
    Whalen MC, Innes RW, Bent AF, Staskawicz BJ: Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3: 49–59 (1991).CrossRefPubMedGoogle Scholar
  160. 147.
    White RF: Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99: 410–412 (1979).CrossRefGoogle Scholar
  161. 148.
    White RF: Serological detection of pathogenesis-related proteins. Neth J Plant Path 89: 311–317 (1983).Google Scholar
  162. 149.
    White RF, Antoniw JF: Virus-induced resistance responses in plants. Crit Rev Plant Sci 9: 443–455 (1991).Google Scholar
  163. 150.
    White RF, Rybicki EP, vonWechmar MB, Dekker JL, Antoniw JF: Detection of PR-1 type proteins in Amaranthaceae, Chemopodiaceae, Graminae and Solanaceae by immunoelectroblotting. J Gen Virol 68: 2043–2048 (1987).Google Scholar
  164. 151.
    Wilson DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Doherty HM, O'Donnell PJ, Bowles DJ: Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360: 62–65 (1992).CrossRefGoogle Scholar
  165. 152.
    Woloshuk CP, Meulenhoff JS, Sela-Buurlage M, van denElzen PJM, Cornelissen BJC: Pathogen-induced proteins with inhibitory activity toward Phytophthora infestans. Plant Cell 3: 619–628 (1991).CrossRefPubMedGoogle Scholar
  166. 153.
    Yalpani N, León J, Lawton MA, Raskin I: Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol 103: 315–321 (1993).PubMedGoogle Scholar
  167. 154.
    Yalpani N, Schulz M, Davis MP, Balke NE: Partial purification and properties of an inducible uridine 5′-diphosphate-glucose: salicylic acid glucosyltransferase from oat roots. Plant Physiol 100: 457–463 (1992).Google Scholar
  168. 155.
    Yalpani N, Shulaev V, Raskin I: Endogenous salicylic acid levels correlate with accumulation of pathogenesis-related proteins and virus resistance in tobacco. Phytopathology 83: 702 (1993).Google Scholar
  169. 156.
    Yalpani N, Silverman P, Wilson TMA, Kleier DA, Raskin I: Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3: 809–818 (1991).CrossRefPubMedGoogle Scholar
  170. 157.
    Yang SF, Pratt HK: The physiology of ethylene in wounded plant tissue. In: Wahl G (ed) Biochemistry of Wounded Plant Tissues, pp. 595–622. Walter de Gruyter, Berlin (1978).Google Scholar
  171. 158.
    Ye XS, Pan SQ, Kuć J: Pathogenesis-related proteins and systemic resistance to blue mould and tobacco mosaic virus induced by tobacco mosaic virus, Peronspora tabacina and aspirin. Physiol Mol Plant Path 35: 161–175 (1989).Google Scholar
  172. 159.
    Ye XS, Pan SQ, Kuć J: Specificity of induced systemic resistance as elicited by ethephon and tobacco mosaic virus in tobacco. Plant Sci 84: 1–9 (1992).CrossRefGoogle Scholar
  173. 160.
    Yoshikawa M, Tsuda M, Takeuchi Y: Resistance to fungal diseases in transgenic tobacco plants expressing the phytoalexin elicitor-releasing factor, β-1,3-endoglucanase from soybean. Naturwissenschaften 80: 417–420 (1993).Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Daniel F. Klessig
    • 1
    • 2
  • Jocelyn Malamy
    • 1
    • 2
  1. 1.Waksman InstituteRutgers-The State University of New JerseyPiscatawayUSA
  2. 2.Department of Molecular Biology and BiochemistryRutgers-The State University of New JerseyPiscatawayUSA

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