Skip to main content

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

  • Chapter
Programmed Cell Death in Higher Plants

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 S A 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. The term ‘necrotic’ alludes to either apoptotic or necrotic cell death.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Abbreviations

AA:

arachidonic acid; avr gene, pathogen avirulence gene

BA:

benzoic acid

BA2H:

benzoic acid 2-hydroxylase

COX:

cyclooxygenase

HR:

hypersensitive response

H202 :

hydrogen peroxide

IKK:

IKB kinase complex

INA:

2,6-dichloroisonicotinic acid

MAP kinase:

mitogen-activated protein kinase

NO:

nitric oxide

03 :

ozone

02- :

superoxide anion

PAL:

phenylalanine ammonia-lyase

PR:

protein, pathogenesis-related protein

R gene:

plant resistance gene

ROI:

reactive oxygen intermediates

SA:

salicylic acid

SAG:

SA 2-0-ß-D-glucoside

SAR:

systemic acquired resistance

tCA:

trans-cinnamic acid

TMV:

tobacco mosaic virus

References

  • Adam, 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.

    PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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.

    Article  CAS  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.

    Article  PubMed  CAS  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.

    PubMed  CAS  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.

    PubMed  CAS  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.

    Article  PubMed  CAS  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. Sei. USA 92: 6597–6601.

    Article  CAS  Google Scholar 

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

    Article  CAS  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.

    Article  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.

    PubMed  CAS  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.

    PubMed  CAS  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.

    Article  CAS  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.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

  • Delaney, T.R, 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.

    Article  PubMed  CAS  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. Sei. USA 92: 6602–6606.

    Article  CAS  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.

    Article  PubMed  CAS  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.

    Article  Google Scholar 

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

    Article  CAS  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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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.

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  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. Sei. USA 92: 11312–11316.

    Article  CAS  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. Sei. USA 95: 10328–10333.

    Article  CAS  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. Sei. USA 89: 2480–2484.

    Article  CAS  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.

    PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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 Lisi gene of maize. Cell 89: 25–31.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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. Sei. USA 29: 4800–4805.

    Article  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.

    Article  Google Scholar 

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

    PubMed  CAS  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.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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., Leon, J. and Raskin, I. 1995. Biosynthesis and metabolism of salicylic acid. Proc. Natl. Acad. Sei. USA 92: 4076–4079.

    Article  CAS  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.

    PubMed  CAS  Google Scholar 

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

    PubMed  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.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Malamy, J., Carr, J.R, 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.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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.

    PubMed  CAS  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.

    Article  PubMed  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.

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  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.

    Article  PubMed  CAS  Google Scholar 

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

    Article  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.

    Article  CAS  Google Scholar 

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

    Article  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.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 integrin-dependent neutrophil adhesion. Proc. Natl. Acad. Sei. USA 95: 14540–14545.

    Article  CAS  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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  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.

    Article  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.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 of MAP kinases in tobacco cell cultures and leaves: convergence of resistance genes, elicitor, wound and salicylate responses. Plant Cell 11: 273–287.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 NIM I protein shows homology to the mammalian transcription factor inhibitor 1/κB. Plant Cell 9: 425–439.

    PubMed  CAS  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.

    PubMed  CAS  Google Scholar 

  • Scofield, S.R., Tobias, CM., 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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  CAS  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.

    PubMed  CAS  Google Scholar 

  • Simmons, C, Hantke, S., Grant, S., Johal, G.S. and Briggs, S.R 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.

    Article  CAS  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.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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.

    Article  Google Scholar 

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

    PubMed  CAS  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.

    PubMed  CAS  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.

    Article  PubMed  CAS  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.

    PubMed  CAS  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.

    PubMed  CAS  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.

    Article  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.

    Article  PubMed  Google Scholar 

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

    Article  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.

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  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.

    PubMed  CAS  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.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  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. Sei. USA 95:7433–7438.

    Article  CAS  Google Scholar 

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

    PubMed  CAS  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.

    PubMed  CAS  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. Sei. USA 96: 6523–6528.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media New York

About this chapter

Cite this chapter

Alvarez, M.E. (2000). Salicylic acid in the machinery of hypersensitive cell death and disease resistance. In: Lam, E., Fukuda, H., Greenberg, J. (eds) Programmed Cell Death in Higher Plants. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0934-8_14

Download citation

  • DOI: https://doi.org/10.1007/978-94-010-0934-8_14

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-3797-6

  • Online ISBN: 978-94-010-0934-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics