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Salicylic acid in the machinery of hypersensitive cell death and disease resistance

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Abstract

Although extensive data has described the key role of salicylic acid (SA) in signaling pathogen-induced disease resistance, its function in physiological processes related to cell death is still poorly understood. Recent studies have explored the requirement of SA for mounting the hypersensitive response (HR) against an invading pathogen, where a particular cell death process is activated at the site of attempted infection causing a confined lesion. Biochemical data suggest that SA potentiates the signal pathway for HR by affecting an early phosphorylation-sensitive step preceding the generation of pro-death signals, including those derived from the oxidative burst. Accordingly, the epistatic relationship between cell death and SA accumulation, analyzed in crosses between lesion-mimic mutants (spontaneous lesion formation) and the transgenic nahG line (depleted in SA) places the SA activity in a feedback loop downstream and upstream of cell death. Exciting advances have been made in the identification of cellular protective functions and cell death suppressors that might operate in HR. Moreover, the spatio-temporal patterns of the SA accumulation (non-homogeneous distribution, biphasic kinetics) described in some HR lesions, may also reveal important clues for unraveling the complex cellular network that tightly balances pro- and anti-death functions in the hypersensitive cell death.

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References

  • Adám, A.L., Pike, S., Hoyos, M.E., Stone, J.M., Walker, J.C. and Novacky, A. 1997. Rapid and transient activation of myelin basic protein kinase in tobacco leaves treated with hairpin from Erwinia amylovora. Plant Physiol. 115: 853–861.

    Google Scholar 

  • Alvarez, M.E., Pennell, R.I., Meijer, P-J., Ishikawa, A., Dixon, R.A. and Lamb, C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92: 773–783.

    Google Scholar 

  • Baker, B., Zambryski, P., Staskswicz, B. and Dinesh-Kumar, S.P. 1997. Signaling in plant-microbe interactions. Science 276: 726–733.

    Google Scholar 

  • Beg, A.A. and Baltimore, D. 1996. An essential role for NF-k_B in preventing TNF-a_-induced cell death. Science 274: 782–784.

    Google Scholar 

  • Bennetzen, J.L., Blevins, W.E. and Ellingboe, A.H. 1988. Cellautonomous recognition of the rust pathogen determines Rp1-specified resistance in maize. Science 241: 208–210.

    Google Scholar 

  • Beligni, M.V and Lamattina, L. 1999. Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta 208: 337–344.

    Google Scholar 

  • Bi, Y.-M., Kenton, P., Mur, L., Darby, R. and Draper, J. 1995. Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J. 8: 235–245.

    Google Scholar 

  • Bowling, S.A., Guo, A., Cao, H., Gordon, A.S., Klessig, D.F. and Dong, X. 1994. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6: 1845–1857.

    Google Scholar 

  • Bowling, S.A., Clarke, J.D., Liu, Y., Klessig, D.F. and Dong, X. 1997. The cpr 5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9: 1573–1584.

    Google Scholar 

  • Cao, H., Glazebrook, J., Clarke, J.D., Volko, S. and Dong, X. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57–63.

    Google Scholar 

  • Century, K.S., Holub, E.B. and Staskawicz, B.J. 1995. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and fungal pathogen. Proc. Natl. Acad. Sci. USA 92: 6597–6601.

    Google Scholar 

  • Chamnongpol, S., Willekens, H., Moeder, W., Langebartels, C., Sandermann, H., Van Montagu, M., Inzé, D. and Van Camp, W. 1998. Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc. Natl. Acad. Sci. USA 95: 5818–5823.

    Google Scholar 

  • Chen, Z., Silva, H. and Klessig, D.F. 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 263: 1883–1886.

    Google Scholar 

  • Chivasa, S. and Carr, J. 1998. Cyanide restores N-gene mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase. Plant Cell 10: 1489–1498.

    Google Scholar 

  • Chivasa, S., Murphy, A.M., Naylor, M. and Carr, J.P. 1997. Salicylic acid interferes with tobacco mosaic virus via a novel salicylhydroxamic acid sensitive mechanism. Plant Cell 9: 547–557.

    Google Scholar 

  • Coquoz, J.L., Buchala, A., Meuwly, P. and Métraux, J.P. 1995. Arachidonic acid induces local but not systemic synthesis of salicylic acid and confers systemic resistance in potato plants to Phytophthora infestans and Alternaria solani. Phytopathology 85: 1219–1224.

    Google Scholar 

  • Coquoz, J.L., Buchala, A. and Métraux, J.P. 1998. The biosynthesis of salicylic acid in potato plants. Plant Physiol. 117: 1095–1101.

    Google Scholar 

  • Dangl, J.L., Dietrich, R.A. and Richberg, M.H. 1996. Death dont't have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8: 1793–1807.

    Google Scholar 

  • Dat, J.F., Lopez-Delgado, H., Foyer, C.H. and Scott, I.M. 1998a. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol. 116: 1351–1357.

    Google Scholar 

  • Dat, J.F., Foyer, C.H. and Scott, I.M. 1998b. Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol. 118: 1455–1461.

    Google Scholar 

  • Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negroto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E. and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266: 1247–1250.

    Google Scholar 

  • Delaney, T.P., Friedrich, L. and Ryals, J.A. 1995. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. USA 92: 6602–6606.

    Google Scholar 

  • Delledonne, M., Xia, Y., Dixon, R.A. and Lamb, C. 1998. Nitric oxide functions as a signal in plant disease resistance. Nature 394: 585–588.

    Google Scholar 

  • de Wit, P.J.G.M. 1997. Pathogen avirulence and plant resistance: a key role for recognition. Trends Plant Sci. 2: 452–458.

    Google Scholar 

  • DiDonatto, J.A., Hayakawa, M., Rothwarf, D.M., Zandi, E. and Karin, M.A. 1997. Cytokine responsive-B kinase that activates transcription factor NF-_B. Nature 388: 548–554.

    Google Scholar 

  • Dietrich, R.A., Delaney, T.P., Uknes, S.K., Ward, E.R., Ryals, J.A. and Dangl, J.L. 1994. Arabidopsis mutants simulating disease resistance response. Cell 77: 565–577.

    Google Scholar 

  • Dietrich, R.A., Richberg, M.H., Schmidt, R., Dean, C. and Dangl, J.L. 1997. A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88: 685–694.

    Google Scholar 

  • Dixon, R. and Paiva, N.L. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7: 1085–1097.

    Google Scholar 

  • Doke, N. 1983. 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 the hypersensitive response. Physiol. Plant Path. 23: 359–367.

    Google Scholar 

  • Dong, X. 1998. SA, JA, ethylene and disease resistance in plants. Curr. Biol. 1: 316–323.

    Google Scholar 

  • Dong, Z. 1997. Inhibition of ultraviolet B-induced activator protein-1 (AP-1) activity by aspirin in AP-1-luciferase transgenic mice. J. Biol. Chem. 272: 26325–26329.

    Google Scholar 

  • Draper, J. 1997. Salicylate, superoxide synthesis and cell suicide in plant defense. Trends Plant Sci. 2: 162–165.

    Google Scholar 

  • Durner, J. and Klessig, D.F. 1995. Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense. Proc. Natl. Acad. Sci. USA 92: 11312–11316.

    Google Scholar 

  • Durner, J., Wendehenne, D. and Klessig, D.F. 1998. Defense gene induction in tobacco by nitric oxide, cylic GMP, and cylic ADP ribose. Proc. Natl. Acad. Sci. USA 95: 10328–10333.

    Google Scholar 

  • Enyedi, A.J., Yalpani, N., Silverman, P. and Raskin, I. 1992. 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.

    Google Scholar 

  • Fauth, M., Merten, A., Hang, M.G. Jeblick, W and Kauss, H. 1996. Competence for elicitation of H2O2 in hypocotyls of cucumber is induced by breaching the cuticule and is enhanced by salicylic acid. Plant Physiol. 110: 347–354.

    Google Scholar 

  • Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754–756.

    Google Scholar 

  • Gallois, P., Makishima, T., Hecht, V., Despres, B., Laudié, M., Nishimoto, T. and Cooke, R. 1997. An Arabidopsis thaliana cDNA complementing a hamster apoptosis suppressor mutant. Plant J. 11: 1325–1331.

    Google Scholar 

  • Glazebrook, J., Rogers, E.E. and Ausubel, F.M. 1997. Use of Arabidopsis for genetic dissection of plant defense responses. Annu. Rev. Genet. 31: 547–569.

    Google Scholar 

  • Gray, J., Close, P.S., Briggs, S.P. and Johal, G.S. 1997. A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89: 25–31.

    Google Scholar 

  • Green, D.R. and Reed, J.C. 1998. Mitochondria and apoptosis. Sicience 281: 1309–1312.

    Google Scholar 

  • Greenberg, J.T. 1997. Programmed cell death in plant-pathogen interactions. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 525–545.

    Google Scholar 

  • Greenberg, J.T., Guo, A. Klessig, D.F. and Ausubel, F.M. 1994. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77: 551–563.

    Google Scholar 

  • Hammond-Kosack, K.E. and Jones, J.D.G. 1996. Resistance genedependent plant defense responses. Plant Cell 8: 1773–1791.

    Google Scholar 

  • Horvath, D.M., Huang, D.J. and Chua, N-H. 1998. Four classes of salicylate induced tobacco genes. Mol. Plant-Microbe Interact. 11: 895–905.

    Google Scholar 

  • Hunt, M., Delaney T.P., Dietrich, R.A., Weymann, K.B., Dangl, J.L. and Ryals, J.A. 1997. Salicylate-independent lesion formation in Arabidopsis lsd mutants. Mol. Plant-Microbe Interact. 10: 531–536.

    Google Scholar 

  • Jabs, T., Dietrich, R.A. and Dangl, J.L. 1996. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273: 1853–1856.

    Google Scholar 

  • Jabs, T., Tschöpe, M., Colling, C., Hahlbrock, K. and Scheel, D. 1997. Elicitor-stimulated ion fluxes and O2 from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. USA 29: 4800–4805.

    Google Scholar 

  • Johal, G.S., Hulbert, S.H. and Briggs, S.P. 1995. Disease lesion mimic in maize: a model for cell death in plants. BioEssays 17: 685–692.

    Google Scholar 

  • Jupin, I. and Chua, N-H. 1996. Activation of the CaMV as-1 ciselement by salicylic acid: differential DNA-binding of a factor related to TGA1a. EMBO J. 15: 5679–5689.

    Google Scholar 

  • Kauss, H. and Jeblick, W. 1995. Pretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2. Plant Physiol. 108: 1171–1178.

    Google Scholar 

  • Klessig, D.F. and Malamy, J. 1994. The salicylic acid signal in plants. Plant Mol. Biol. 26: 1439–1458.

    Google Scholar 

  • Kopp, E and Ghosh, S. 1994. Inhibition of NF-κB by sodium salicylate and aspirin. Science 265: 956–959.

    Google Scholar 

  • Kvaratskhelia, M., George, S.J. and Thorneley, R.N. 1997. Salicylic acid is a reducing substrate and not an effective inhibitor of ascorbate peroxidase. J. Biol. Chem. 272: 20998–21001.

    Google Scholar 

  • Lamb, C.J. and Dixon, R.A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 76: 419–422.

    Google Scholar 

  • Lee, H-I., Leó n, J. and Raskin, I. 1995. Biosynthesis and metabolism of salicylic acid. Proc. Natl. Acad. Sci. USA 92: 4076–4079.

    Google Scholar 

  • Lennon, A.M., Neuenschwander, U.H., Ribas-Carbo, M., Giles, L., Ryals, J.A. and Siedow, J.N. 1997. The effects of salicylic acid and tobacco mosaic virus infection on the alternative oxidase of tobacco. Plant Physiol. 115: 783–791.

    Google Scholar 

  • Leó n, J., Lawton, M.A. and Raskin, I. 1995. Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 108: 1673–1678.

    Google Scholar 

  • Levine, A., Tenhaken, R., Dixon, R. and Lamb, C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583–593.

    Google Scholar 

  • Levine, A., Penell, R.I., Alvarez, M.E., Palmer, R. and Lamb, C. 1996. Calcium-mediated apoptosis in plant hypersensitive disease resistance response. Curr. Biol. 6: 427–437.

    Google Scholar 

  • Ligterink, W., Kroj, T., zur Nieden, U., Hirt, H. and Scheel, D. 1997. Receptor-mediated activation of aMAP kinase in pathogen defense in plants. Science 276: 2054–2057.

    Google Scholar 

  • Malamy, J., Carr, J.P., Klessig, D.F. and Raskin, I. 1990. Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002–1004.

    Google Scholar 

  • Malamy, J., Henning, J. and Klessig, D.F. 1992. Temperaturedependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 4: 359–366.

    Google Scholar 

  • Mauch-Mani, B. and Slusarenko, A. 1996. Production of salicylic acid precursors is a mayor function of phenylalanine ammonialyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8: 203–212.

    Google Scholar 

  • Métraux, J.P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W. and Inverardi, B. 1990. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250: 1004–1006.

    Google Scholar 

  • Meuwly, P., Mölders, W., Buchala, A. and Métraux, J.-P. 1995. Local and systemic biosynthesis of salicylic acid in infected cucumber plants. Plant Physiol. 109: 1107–1114.

    Google Scholar 

  • Mitchell, J.A. Akarasereenont, P., Thiemermann, C. Flower, R.J. and Vane, R. 1994. Selectivity of non-steroideal antiinflammatory drugs as inhibitors of constitutive and inducible cyclooxygenase. Proc. Natl. Acad. Sci. USA 90: 11693–11697.

    Google Scholar 

  • Mittler, R. and Rizhsky, L. 2000. Trangenic-induced lesion mimic. Plant Mol. Biol., this issue.

  • Mur, L.A.J., Naylor, G., Warner, S.A.J., Sugars, J.M., White, R.F. and Draper, J. 1996. Salicylic acid potentiates defence gene expression in tissues exhibiting acquired resistance to pathogen attack. Plant J. 9: 559–571.

    Google Scholar 

  • Mur, L.A.J., Bi, Y.-M., Darby, R.M., Firek, S. and Draper, J. 1997. Compromising early salicylic acid accumulation delays the hypersensitive response and increases viral dispersal during lesion establishment in TMV infected tobacco. Plant J. 12: 1113–1126.

    Google Scholar 

  • Murphy, A.M., Chivasa, S., Singh, D.P. and Carr, J.P. 1999. Salicylic acid-induced resistance to viruses and other pathogens: a parting of the ways? Trends Plant Sci. 4: 155–160.

    Google Scholar 

  • Neuenschwander, U., Vernooij, B., Friedrich, L., Uknes, S., Kessmann, H. and Ryals, J. 1995. Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? Plant J. 8: 227–233.

    Google Scholar 

  • O'Brien, I.E.W., Baguley, B.C., Murray, B.G., Morris, B.A.M. and Ferguson, I.B. 1998. Early stages of the apoptotic pathway in plant cells are reversible. Plant J. 13: 803–814.

    Google Scholar 

  • Pancheva, T.V., Popova, L.P. and Uzunova, A.N. 1996. Effects of salicylic acid on growth and photosynthesis in barely plants. Plant Physiol. 149: 57–63.

    Google Scholar 

  • Pennell, R.I. and Lamb, C.J. 1997. Programmed cell death in plants. Plant Cell 9: 1157–1168.

    Google Scholar 

  • Pillinger, M.H., Capodici, C., Risenthal, P., Kheterpal, N., Hanft, S., Philips, M.R. and Weissmann G. 1998. Modes of action of aspirin-like drugs: salicylates inhibit Erk activation and integrindependent neutrophil adhesion. Proc. Natl. Acad. Sci. USA 95: 14540–14545.

    Google Scholar 

  • Rao, M.V. and Davis, K.R. 1999. Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J. 17: 603–614.

    Google Scholar 

  • Raskin, I., Ehman, A., Melander, W.R. and Meusse, B.D.J. 1987. Salicylic acid: a natural inducer of heat production in Arum lilies. Science 237: 1601–1602.

    Google Scholar 

  • Raskin, I. 1992. Role of salicylic acid in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 439–463.

    Google Scholar 

  • Rasmussen, J.B., Hammerschmidt, R. and Zook, M.N. 1991. Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiol. 97: 1324–1347.

    Google Scholar 

  • Rate, D.N., Cuenca, J.V., Bowman, G.R., Guttman, D.S. and Greenberg, J.T. 1999. The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses and cell growth. Plant Cell 11: 1695–1708.

    Google Scholar 

  • Rhoads, D.M. and McIntosh, L. 1993. The salicylic acid-inducible alternative oxidase gene aox1 and genes encoding pathogenesisrelated proteins share regions of sequence similarity in their promoters. Plant Mol. Biol. 21: 615–624.

    Google Scholar 

  • Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H. and Jones, J.D.G. 1999. Rapid Avr-9 and Cf-9-dependent activation ofMAP kinases in tobacco cell cultures and leaves: convergence of resistance genes, elicitor, wound and salicylate responses. Plant Cell 11: 273–287.

    Google Scholar 

  • Ross, A.F. 1961. Systemic Acquired Resistance induced by localized virus infections in plants. Virology 14: 340–358.

    Google Scholar 

  • Ryals, J., Weymann, K., Lawton, K., Friedrich, L., Ellis, D., Steiner, H.-Y., Johnson, J., Delaney, T.P., Jesse, T., Vos, P. and Uknes, S. 1997. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB. Plant Cell 9: 425–439.

    Google Scholar 

  • Ryals, J. Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H.-Y and Hunt, M. 1996. Systemic acquired resistance. Plant Cell 8: 1809–1819.

    Google Scholar 

  • Scofield, S.R., Tobias, C.M., Rathgen, J.P., Chang, J.H. Lavelle, D.T., Michelmore, R.W and Staskawicz, B.J. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274: 2063–2065.

    Google Scholar 

  • Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H. and Ohashi, Y. 1995. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270: 1988–1992.

    Google Scholar 

  • Shah, J. Tsui, F. and Klessig, D. 1997. Characterization of salicylic acid insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol. Plant-Microbe Interact. 10: 69–78.

    Google Scholar 

  • Shirasu, K., Nakajima, H., Krishnamachari Rajasekhar, V., Dixon, R.A. and Lamb, C. 1997. Salicylic acid potentiates an agonistdependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9: 261–270.

    Google Scholar 

  • Shulaev, V., Silverman P. and Raskin I. 1997. Airborne signaling by methyl salicylate in plant pathogen resistance. Nature 385: 718–721.

    Google Scholar 

  • Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Métraux, J-P. and Raskin, I. 1995. Salicylic acid in rice. Plant Physiol. 108: 633–639.

    Google Scholar 

  • Simmons, C., Hantke, S., Grant, S., Johal, G.S. and Briggs, S.P. 1998. The maize lethal leaf spot 1 mutant has elevated resistance to fungal infection at the leaf epidermis. Mol. Plant-Microbe Interact. 11: 1110–1118.

    Google Scholar 

  • Simons, B.H., Millenaar, F.F. Mulder. L. van Loon, L.C. and Lambers H. 1999. Enhanced expression and activation of the alternative oxidase during the infection of Arabidopsis with Pseudomonas syringae pv. tomato. Plant Physiol. 120: 529–538.

    Google Scholar 

  • Stange, C., Ramirez, I., Gó mez, I., Jordana, X. and Holuigue, L. 1997. Phosphorylation of nuclear proteins directs binding to salicylic acid-responsive elements. Plant J. 11: 1315–1324.

    Google Scholar 

  • Stone, E. 1763. An account of the success of the bark of the willow in the cure of agues. Phil. Trans. R. Soc. 53: 195–200.

    Google Scholar 

  • Summermatter, K., Sticher, L. and Métraux, J.P. 1995. Systemic responses in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv. syringae. Plant Physiol. 108: 1379–1385.

    Google Scholar 

  • Suzuki, K and Shinshi, H. 1995. Transient activation and tyrosine phosphorylation of a protein kinase in tobacco cells treated with fungal elicitors. Plant Cell 7: 639–647.

    Google Scholar 

  • Tanaka, Y., Makishima, T., Ichinose, Y., Shiraishi, T., Nishimoto, T. and Yamada, T. 1997. dad-1, a putative programmed cell death suppressor gene in rice. Plant Cell Physiol. 38: 379–383.

    Google Scholar 

  • Tang, X., Xie, M., Kim, Y.J., Zhou, J.; Klessig, D.F. and Martin, G.B. 1999. Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11: 15–29.

    Google Scholar 

  • Tenhaken, R. and Rubel, C. 1997. Salicylic acid is needed in hypersensitive cell death in soybean but does not act as a catalase inhibitor. Plant Physiol. 115: 291–298.

    Google Scholar 

  • Thukle, O. and Conrath, U. 1998. Salicylic acid has a dual role in the activation of defense-related genes in parsley. Plant J. 14: 35–42.

    Google Scholar 

  • Uknes, S., Winter, A.M., Delaney, T., Vernooij, B., Morse, A., Friedrich, L., Potter, S., Slusarenko A., Ward, E. and Ryals, J. 1993. Biological induction of systemic acquired resistance in Arabidopsis. Mol. Plant-Microbe Interact. 6: 680–685.

    Google Scholar 

  • Van Antwerp, D.J., Martin, S.J., Kafri, T., Green, D.R. and Verma,I.M. 1996. Suppression of TNF_-induced apoptosis by NF-_B. Science 274: 784–787.

    Google Scholar 

  • Vane, J.R. 1971. Inhibition of prostaglandin synthesis as a mechanisms of action of the aspirin-like drugs. Nature New Biol. 231: 232–235.

    Google Scholar 

  • Vane, J.R. and Botting, R.M. 1998. Anti-inflammatory drugs and their mechanism of action. Inflamm. Res. 47: 78–87.

    Google Scholar 

  • Vanlerberghe, G.C. and McIntosh, L. 1997. Alternative oxidase: from gene to function. Annu. Rev. Plant Physiol. PlantMol. Biol. 48: 703–734.

    Google Scholar 

  • Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, R., Ward, E., Uknes, S., Kessmann, H. and Ryals, J. 1994. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6: 959–965.

    Google Scholar 

  • Walbot, V. 1991. Maize mutants for the 21st century. Plant Cell 3: 857–866.

    Google Scholar 

  • Weymann, K., Hunt, M., Uknes, S., Neuenschwander, U., Lawton, K., Steiner, H.Y. and Ryals, J. 1995. Suppression and restoration of lesion formation in Arabidopsis Lsd mutants. Plant Cell 7: 2013–2022.

    Google Scholar 

  • White, R.F. 1979. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99: 410–412.

    Google Scholar 

  • Xie, Z. and Chen, Z. 1999. Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells. Plant Physiol. 120: 217–226.

    Google Scholar 

  • Yalpani, N., Silverman, P., Wilson, T.M.A., Kleier, D.A. and Raskin, I. 1991. Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3: 809–818.

    Google Scholar 

  • Yalpani, N., Leó n, J., Lawton, M. and Raskin, I. 1993. Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol. 103: 315–321.

    Google Scholar 

  • Yin, M.-J., Yamamoto, Y. and Gaynor, B. 1998. The anti-inflammatory agents aspirin and salicylates inhibit the activity of I kB kinase-_. Nature 396: 77–80.

    Google Scholar 

  • Yu, D., Liu, Y., Fan, B., Klessig, D. and Chen, Z. 1997. Is the high basal level of salicylic acid important for disease resistance in potato? Plant Physiol. 11: 343–349.

    Google Scholar 

  • Yu, I.-C., Parker, J. and Bent, A. 1998. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc. Natl. Acad. Sci. USA 95: 7819–7824.

    Google Scholar 

  • Zandi, E., Rothwarf, D.M., Delhase, M., Hayakawa, M. and Karin, M. 1997. The IkB kinase complex (IKK) contains two kinase subunits IKKκ and IKKκ necessary for I_B phosphorylation and NF-κB activation. Cell 91: 243–252.

    Google Scholar 

  • Zhang, S. and Klessig, D.F. 1998. Resistance gene N-mediated the novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc. Natl. Acad. Sci. USA 95: 7433–7438.

    Google Scholar 

  • Zhang, S. and Klessig, D.F. 1997. Salicylic acid activates a 48-KD MAP kinase in tobacco. Plant Cell 9: 809–824.

    Google Scholar 

  • Zhang, S., Du, H. and Klessig, D.F. 1998. Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. Plant Cell 10: 435–449.

    Google Scholar 

  • Zhang, Y., Fan, W., Kinkema, M., Li, X. and Dong, X. 1999. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc. Natl. Acad. Sci. USA 96: 6523–6528.

    Google Scholar 

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  1. Departamento de Química Biológica, CIQUIBIC-CONICET, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Ciudad Universitaria, 5000, Córdoba, Argentina

    María Elena Alvarez

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  1. María Elena Alvarez
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Alvarez, M.E. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol Biol 44, 429–442 (2000). https://doi.org/10.1023/A:1026561029533

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