Plant Molecular Biology

, Volume 44, Issue 3, pp 321–334 | Cite as

Hypersensitive response-related death

  • Michèle C. Heath


The hypersensitive response (HR) of plants resistant to microbial pathogens involves a complex form of programmed cell death (PCD) that differs from developmental PCD in its consistent association with the induction of local and systemic defence responses. Hypersensitive cell death is commonly controlled by direct or indirect interactions between pathogen avirulence gene products and those of plant resistance genes and it can be the result of multiple signalling pathways. Ion fluxes and the generation of reactive oxygen species commonly precede cell death, but a direct involvement of the latter seems to vary with the plant-pathogen combination. Protein synthesis, an intact actin cytoskeleton and salicylic acid also seem necessary for cell death induction. Cytological studies suggest that the actual mode and sequence of dismantling the cell contents varies among plant-parasite systems although there may be a universal involvement of cysteine proteases. It seems likely that cell death within the HR acts more as a signal to the rest of the plant rather than as a direct defence mechanism.

hypersensitive response pathogens plants programmed cell death proteases reactive oxygen species resistance genes 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aist, J.R. and Bushnell, W.R. 1991. Invasion of plants by powdery mildew fungi, and cellular mechanisms of resistance. In: G.T. Cole and H.C. Hoch (Eds.) The Fungal Spore and Disease Initiation in Plants and Animals, Plenum Press, New York/London, pp. 321–345.Google Scholar
  2. Alfano, J.R. and Collmer, A. 1996. Bacterial pathogens in plants: life up against the wall. Plant Cell 8: 1683–1698.Google Scholar
  3. Allen, L.J., MacGregor, K.B., Koop, R.S., Bruce, D.H., Karner, J. and Bown, A.W. 1999. The relationship between photosynthesis and a mastoparan-induced hypersensitive response in isolated mesophyll cells. Plant Phyiol 119: 1233–1241.Google Scholar
  4. 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: 773–784.Google Scholar
  5. Atkinson, M.M. and Baker, C.J. 1989. Role of the plasmalemma H+-ATPase in Pseudomonas syringae-induced K+/H+ exchange in suspension-cultured tobacco cells. Plant Physiol 91: 298–303.Google Scholar
  6. Baker, J.C. and Orlandi, E.W. 1995. Active oxygen in plant pathogenesis. Annu. Rev. Phytopath. 33: 299–321.Google Scholar
  7. Baudouin, E., Charpenteau, M., Ranjeva, R. and Ranty, B. 1999. Involvement of active oxygen species in the regulation of a tobacco defence gene by phorbol ester. Plant Sci. 142: 67–72.Google Scholar
  8. Bestwick, C.S., Bennett, M.H. and Mansfield, J.W. 1995. Hrp mutant of pseudomonas syringae pv. phaseolicola induced cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce. Plant Physiol. 108: 503–516.Google Scholar
  9. Bestwick, C.S., Brown, I.R. and Mansfield, J.W. 1998. Localized changes in peroxidase activity accompany hydrogen peroxide generation during the development of a nonhost hypersensitive reaction in lettuce. Plant Physiol. 118: 1067–1078.Google Scholar
  10. Birch, P.R.J., Avrova, A.O., Duncan, J.M., Lyon, G.D. and Toth, R.L. 1999. Isolation of potato genes that are induced during an early stage of the hypersensitive response to Phytophthora infestans. Mol. Plant-Microbe Interact. 12: 356–361.Google Scholar
  11. Blumwald, E., Aharon, G.S. and Lam, B.C.-H. 1998. Early signal transduction pathways in plant-pathogen interactions. Trends Plant Sci. 3: 342–346.Google Scholar
  12. Bolwell, G.P. and Wojtaszek, P. 1997. Mechanisms for the generation of reactive oxygen species in plant defence: a broad perspective. Physiol. Mol. Plant Path. 51: 347–366.Google Scholar
  13. Boyes, D.C., Nam, J. and Dangl, J.L. 1998. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc. Natl. Acad. Sci. USA 95: 15849–15854.Google Scholar
  14. Buchanan-Wollaston, V. 1997. The molecular biology of leaf senescence. J. Exp. Bot. 48: 181–199.Google Scholar
  15. Chandra, S., Heinstein, P.F. and Low, P.S. 1996a. Activation of phospholipase A by plant defense elicitors. Plant Physiol. 110: 979–986.Google Scholar
  16. Chandra, S., Martin, G.B. and Low, P.S. 1996b. The Pto kinase mediates a signalling pathway leading to the oxidative burst in tomato. Proc. Natl. Acad. Sci. USA 93: 13393–13397.Google Scholar
  17. Chen, C.-Y. and Heath, M.C. 1992. Effect of stage of development of the cowpea rust fungus on the release of a cultivar-specific elicitor of necrosis. Physiol. Mol. Plant Path. 40: 23–30.Google Scholar
  18. Chen, C.-Y. and Heath, M.C. 1994. Elicitors of necrosis in rust diseases. In: K. Kohmoto and O.C. Yoder (Eds.) Host-Specific Toxin: Biosynthesis, Receptor and Molecular Biology, Tottori University, Japan, pp. 73–82.Google Scholar
  19. Chivasa, S. and Carr, J.P. 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
  20. Collmer, A. 1998. Determinants of pathogenicity and avirulence in plant pathogenic bacteria. Curr. Opin. Plant Biol. 1: 329–335.Google Scholar
  21. 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.Google Scholar
  22. Dawson, W.O. 1999. Tobacco mosaic virus virulence and avirulence. Phil. Trans. R. Soc. Lond. B 354: 645–651.Google Scholar
  23. Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffne, T., Gut-Rella, M., Kessmann, H., Ward, E. and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266: 1247–1250Google Scholar
  24. 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
  25. del Pozo, O. and Lam, E. 1998. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol. 8: 1129–1132.Google Scholar
  26. Dion, M., Chamberland, H., St-Michel, C., Plante, M., Darveau, A., Lafontaine, J.G. and Brisson, L.F. 1997. Detection of a homologue of bcl-2 in plant cells. Biochem. Cell Biol. 75: 457–461.Google Scholar
  27. Doke, N. 1983. Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissue to infection with an incompatible race of Phytophthora infestans and to the hypha wall components. Physiol. Plant Path. 23: 345–357.Google Scholar
  28. Doke, N., Sanchez, L.M., Yoshioka, H., Kawakita, K., Miura, Y. and Park, H.-J. 1998. In: K. Kohmoto and O.C. Yoder (Eds.) Molecular Genetics of Host-Specific Toxins in Plant Disease, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 331–341.Google Scholar
  29. Dong, Y.-H., Zhan, X.-C., Kvarnheden, A., Atkinson, R.G., Morris, B.A. and Gardner, R.C. 1998. Expression of a cDNA from apple encoding a homologue of DAD1, an inhibitor of programmed cell death. Plant Sci. 139: 165–174.Google Scholar
  30. Dorey, S., Baillieul, F., Pierrel, M.-A., Saindrenan, P., Fritig, B. and Kauffmann, S. 1997. Spatial and temporal induction of cell death, defense genes, and accumulation of salicylic acid in tobacco leaves reacting hypersensitively to a fungal glycoprotein elicitor. Mol. Plant-Microbe Interact. 10: 646–655.Google Scholar
  31. D'Silva, I. and Heath, M.C. 1997. Purification and characterization of two novel hypersensitive response-inducing specific elicitors produced by the cowpea rust fungus. J. Biol. Chem. 272: 3924–3927.Google Scholar
  32. D'Silva, I., Poirier, G.G. and Heath, M.C. 1998. Activation of cysteine proteases in cowpea plants during the hypersensitive response - a form of programmed cell death. Exp. Cell Res. 245: 389–399.Google Scholar
  33. Durner, J., Wendehenne, D. and Klessig, D.F. 1998. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 95: 10328–10333.Google Scholar
  34. Ebel, J. and Scheel, D. 1997. Signals in host-parasite interactions. In: G.C. Carroll and P. Tudzynski (Eds.) The Mycota Vol. V. Plant Relationships Part A, Springer-Verlag, Berlin/Heidelberg, pp. 85–105.Google Scholar
  35. Falk, A., F eys, B.J., Frost, L.N., Jones, J.D.G., Daniels, M.J. and Parker, J.E. 1999. EDS1, an essential component of R genemediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. USA 96: 3292–3297.Google Scholar
  36. Freytag, S., Arabatzis, N., Hahlbrock, K. and Schmelzer, E. 1994. Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell death and defense-related gene activation in potato/Phytophthora infestans interactions. Planta 194: 123–135.Google Scholar
  37. Gabriel, D.W. 1999. Why do pathogens carry avirulence genes? Physiol. Mol. Plant Path. 55: 205–214.Google Scholar
  38. Gilchrist, D.G. 1998. Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu. Rev. Phytopath. 36: 393–414.Google Scholar
  39. Glazener, J.A., Orlandi, E.W. and Baker, C.J. 1996. The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause hypersensitive cell death. Plant Physiol. 110: 759–763.Google Scholar
  40. Goodman, R.N. and Novacky, A.J. 1994. The Hypersensitive Reaction in Plants to Pathogens. APS Press, St. Paul, MN.Google Scholar
  41. Gopalan, S., Wei, W. and He, S.Y. 1996. hrp gene-dependent induction of hin 1: a plant gene activated rapidly by both harpins and the avrPto gene-mediated signal. Plant J. 10: 591–600.Google Scholar
  42. Graham, T.L. and Graham, M.Y. 1999. Role of hypersensitive cell death in conditioning elicitation competency and defense potentiation. Physiol. Mol. Plant Path. 55: 13–20.Google Scholar
  43. Green, D.R. and Reed, J.C. 1998. Mitochondria and apoptosis. Science 281: 1309–1312.Google Scholar
  44. Groover, A. and Jones, A.M. 1999. Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary wall synthesis. Plant Physiol. 119: 375–384.Google Scholar
  45. Groover A., Dewitt, N., Heidel, A. and Jones, A. 1997. Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma 196: 197–211.Google Scholar
  46. Gross, P., Julius, C., Schmelzer, E. and Hahlbrock, K. 1993. Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerisation of microtubules and defence gene activation in infected cultured parsley cells. EMBO J. 12: 1735–1744.Google Scholar
  47. Gus-Mayer, S., Naton, B., Hahlbrock, K. and Schmelzer, E. 1998. Local mechanical stimulation induces components of the pathogen defense response in parsley. Proc. Natl. Acad. Sci. USA 95: 8398–8403.Google Scholar
  48. Hammond-Kosack, K.E. and Jones, J.D.G. 1997. Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 575–607.Google Scholar
  49. Hammond-Kosack, K.E., Tang, S., Harrison, K. and Jones, J.D.G. 1998. The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product Avr9. Plant Cell 10: 1251–1266.Google Scholar
  50. He, S.Y. 1998. Type III protein secretion systems in plant and animal pathogenic bacteria. Annu. Rev. Phytopath. 36: 363–392.Google Scholar
  51. Heath, M.C. 1982. The absence of active defense mechanisms in compatible host-pathogen interactions. In: R.K.S. Wood (Ed.) Active Defense Mechanisms in Plants, Plenum Press, New York, pp. 143–156.Google Scholar
  52. Heath, M.C. 1991. The role of gene-for-gene interactions in the determination of host species specificity. Phytopathology 81: 127–130.Google Scholar
  53. Heath, M.C. 1996. Plant resistance to fungi. Can. J. Plant Path. 18: 469–475.Google Scholar
  54. Heath, M.C. 1997. Evolution of plant resistance and susceptibility to fungal parasites. In: G.C. Carroll and P. Tudzynski (Eds.) The Mycota Vol. V. Plant Relationships Part B, Springer-Verlag, Berlin/Heidelberg, pp. 257–276.Google Scholar
  55. Heath, M.C. 1998a. Apoptosis, programmed cell death and the hypersensitive response. Eur. J. Plant Path. 104: 117–124.Google Scholar
  56. Heath, M.C. 1998b. Involvement of reactive oxygen species in the response of resistant (hypersensitive) or susceptible cowpeas to the cowpea rust fungus. New Phytol. 138: 251–263.Google Scholar
  57. Heath, M.C., Nimchuk, Z.L. and Xu, H. 1997. Plant nuclear migrations as indicators of critical interactions between resistant or susceptible cowpea epidermal cells and invasion hyphae of the cowpea rust fungus. New Phytol. 135: 689–700.Google Scholar
  58. Higgins, V.J., Lu, H., Xing, T., Gellie, A. and Blumwald, E. 1998. The gene-for-gene concept and beyond: interactions and signals. Can. J. Plant Path. 20: 150–157.Google Scholar
  59. Hu, G., Richter, T.E., Hulbert, S.H. and Pryor, T. 1996. Disease lesion mimicry caused by mutations in the rust resistance gene rp1. Plant Cell 8: 1367–1376.Google Scholar
  60. Hu, G., Yalpani, N., Briggs, S.P. and Johal, G.S. 1998. A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10: 1095–1105.Google Scholar
  61. Hückelhoven, R. and Kogel, K.-H. 1998. Tissue-specific superoxide generation at interaction sites in resistant and susceptible nearisogenic barley lines attacked by the powdery mildew fungus (Erysiphe graminis f. sp. hordei). Mol. Plant-Microbe Interact. 11: 292–300.Google Scholar
  62. Jabs, T. 1999. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem. Pharmacol. 57: 231–245.Google Scholar
  63. Jakobek, J.L. and Lindgren, P.B. 1993. Generalized induction of defense responses in bean is not correlated with the induction of the hypersensitive reaction. Plant Cell 5: 49–56.Google Scholar
  64. Ji, C., Boyd, C., Slaymaker, D., Okinaka, Y., Takeuchi, Y., Midland, S.L., Sims, J.J., Herman, E. and Keen, N. 1998. Characterization of a 34-kDa soybean binding protein for the syringolide elicitors. Proc. Natl. Acad. Sci. USA 95: 3306–3311.Google Scholar
  65. Johal, G.S. Briggs, S.P. 1992. Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258: 985–987.Google Scholar
  66. Kamoun, S., van West, P., Vleeshouwers, V.G.A.A., de Groot, K.E. and Govers, F. 1998. Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10: 1413–1425.Google Scholar
  67. Kato, S. and Misawa, T. 1976. Lipid peroxidation during the appearance of hypersensitive reaction in cowpea leaves infected with cucumber mosaic virus. Ann. Phytopath. Soc. Japan 42: 472–480.Google Scholar
  68. Kawakita, K. and Doke, N. 1994. Involvement of a GTP-binding protein in signal transduction in potato tubers treated with the fungal elicitor from Phytophthora infestans. Plant Sci. 96: 81–86.Google Scholar
  69. Kazan, K., Murray, F.R., Goulter, K.C., Llewellyn, D.J. and Manners, J.M. 1998. Induction of cell death in transgenic plants expressing a fungal glucose oxidase. Mol. Plant-Microbe Interact. 11: 555–562.Google Scholar
  70. Keller, H., Pamboukdjian, N., Ponchet, M., Poupet, A., Delon, R., Verrier, J.-L., Roby, D. and Ricci, P. 1999. Pathogen-induced elicitin production in transgenic tobacco generates a hypersensitive response in nonspecific disease resistance. Plant Cell 11: 223–235.Google Scholar
  71. Keppler, L.D. and Novacky, A. 1987. The initiation of membrane lipid peroxidation during bacteria-induced hypersensitive reaction. Physiol. Mol. Plant Path. 30: 233–245.Google Scholar
  72. Lamb, C. and Dixon, R.A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 251–275.Google Scholar
  73. Laugé, R. and de Wit, P.J.G.M. 1998. Fungal avirulence genes: structure and possible functions. Fungal Genet. Biol. 24: 285–297.Google Scholar
  74. Levine, A., Pennell, R.I., Alvarez, M.E., Palmer, R. and Lamb, C. 1996. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6: 427–437.Google Scholar
  75. Ligterink, W., Kroj, T., zur Nieden, U., Hirt, H. and Scheel, D. 1997. Receptor-mediated activation of aMAP kinase in pathogen defense of plants. Science 276: 2054–2057.Google Scholar
  76. Lu, H. and Higgins, V.J. 1998. Measurement of active oxygen species generated in planta in response to elicitor AVR9 of Cladosporium fulvum. Physiol. Mol. Plant Path. 52: 35–51.Google Scholar
  77. Lu, H. and Higgins, V.J. 1999. The effect of hydrogen peroxide on the viability of tomato cells and of the fungal pathogen Cladosporium fulvum. Physiol. Mol. Plant Path. 54: 131–143.Google Scholar
  78. Malhó , R., Moutinho, A., van der Luit, A. and Trewavas, A.J. 1998. Spatial characteristics of calcium signalling: the calcium wave as a basic unit in plant cell calcium signalling. Phil. Trans. R. Soc. Lond. B 353: 1463–1473.Google Scholar
  79. Mansfield, J., Bennett, M., Bestwick, C. and Woods-Tör, A. 1997. Phenotypic expression of gene-for-gene interactions involving fungal and bacterial pathogens: variation from recognition to response. In: I.R. Crute, E.B. Holub and J.J. Burdon (Eds.) The Gene-for-Gene Relationship in Plant-Parasite Interactions, CAB International, Wallingford, UK/ New York, pp. 265–291.Google Scholar
  80. Meyer, S.L.F. and Heath, M.C. 1988a. A comparison of the death induced by fungal invasion or toxic chemicals in cowpea epidermal cells. I. Cell death induced by heavy metal salts. Can. J. Bot. 66: 613–623.Google Scholar
  81. Meyer, S.L.F. and Heath, M.C. 1988b. A comparison of the death induced by fungal invasion or toxic chemicals in cowpea epidermal cells. II. Responses induced by Erysiphe cichoracearum. Can. J. Bot. 66: 624–634.Google Scholar
  82. Michelmore, R.W. and Meyers, B.C. 1998. Clusters of resistance genes in plants evolve by divergent selection and a birth-anddeath process. Genome Res. 8: 1113–1130.Google Scholar
  83. Mittler, R., Simon, L. and Lam, E. 1997a. Pathogen-induced programmed cell death in tobacco. J. Cell Sci. 110: 1333–1344.Google Scholar
  84. Mittler, R., del Pozo, O., Meisel, L. and Lam, E. 1997b. Pathogeninduced programmed cell death in plants, a possible defense mechanism. Dev. Genet. 21: 279–289.Google Scholar
  85. Molina, A., Volrath, S., Guyer, D., Maleck, K., Ryals, J. and Ward, E. 1999. Inhibition of protoporphyrinogen oxidase expression in Arabidopsis causes a lesion mimic phenotype that induced systemic acquired resistance. Plant J. 17: 667–678.Google Scholar
  86. Morel, J.-B. and Dangl, J.L. 1997. The hypersensitive response and the induction of cell death in plants. Cell Death Different. 4: 671–683.Google Scholar
  87. Morel, J.-B. and Dangl, J.L. 1999. Suppressors of the Arabidopsis lsd5 cell death mutation identify genes involved in regulating disease resistance responses. Genetics 151: 305–319.Google Scholar
  88. Mould, M.J.R. and Heath, M.C. 1999. Ultrastructural evidence of differential changes in transcription, translation, and cortical microtubules during in planta penetration of cells resistant or susceptible to rust infection. Physiol. Mol. Plant Path. 55: 225–236.Google Scholar
  89. Naton, B., Hahlbrock, K. and Schmelzer, E. 1996. Correlation of rapid cell death with metabolic changes in fungus-infected, cultured parsley cells. Plant Physiol. 112: 433–444.Google Scholar
  90. Nicholson, R.L. and Hammerschmidt, R. 1992. Phenolic compounds and their role in disease resistance. Annu. Rev. Phytopath. 30: 369–386.Google Scholar
  91. Person, C. and Mayo, G.M.E. 1973. Genetic limitations on models of specific interactions between a host and its parasite. Can. J. Bot. 52: 1339–1347.Google Scholar
  92. Peterhänsel, C., Freialdenhoven, A., Kurth, J., Kolsch, R. and Schulze-Lefert, P. 1997. Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. Plant Cell 9: 1397–1409.Google Scholar
  93. Pike, S.M., Ádám, A.L., Pu, X.-A., Hoyos, M.E., Laby, R., Beer, S.V. and Novacky, A. 1998. Effects of Erwinia amylovora harpin on tobacco leaf cell membranes are related to leaf necrosis and electrolyte leakage and distinct from perturbations caused by inoculated E. amylovora. Physiol. Mol. Plant Path. 53: 39–60.Google Scholar
  94. Pontier, D., Tronchet, M., Rogowsky, P., Lam, E. and Roby, D. 1998. Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Mol. Plant-Microbe Interact. 11: 544–554.Google Scholar
  95. Pontier, D., Gan, S., Amasino, R.M., Roby, D. and Lam, E. 1999. Markers for hypersensitive response and senescence show distinct patterns of expression. Plant Mol. Biol. 39: 1243–1255.Google Scholar
  96. Rahe, J.E. and Arnold, R.M. 1975. Injury-related phaseolin accumulation in Phaseolus vulgaris and its implications with regard to specificity of host-parasite interaction. Can. J. Bot. 53: 921–928.Google Scholar
  97. Rathjen, J.P., Chang, J.H., Staskawicz, B.J. and Michelmore, R.W. 1999. Constitutively active Pto induced a Prf-dependent hypersensitive response in the absence of avrPto. EMBO J. 18: 3232–3240.Google Scholar
  98. 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
  99. Reichheld, J.-P., Vernoux, T., Lardon, F., Van Montagu, M. and Inzé, D. 1999. Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J. 17: 647–656.Google Scholar
  100. Richael, C. and Gilchrist, D. 1999. The hypersensitive response: a case of hold or fold? Physiol. Mol. Plant Path. 55: 5–12.Google Scholar
  101. Romeis, T., Peidras, P. Zhang, S., Klessig, D.F., Hirt, H. and Jones, J.D.G. 1999. Rapid Avr9-and Cf-9-dependent activation ofMAP kinases in tobaccco cell cultures and leaves: convergence of resistance gene, elicitor, wound and salicylate responses. Plant Cell 11: 273–287.Google Scholar
  102. Ryerson, D.E. and Heath, M.C. 1996. Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or be abiotic treatments. Plant Cell 8: 393–402.Google Scholar
  103. Schaller, A. and Oecking, C. 1999. Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11: 263–272.Google Scholar
  104. Seehaus, K. and Tenhaken, R. 1998. Cloning of genes by mRNA differential display induced during the hypersensitive reaction of soybean after inoculation with Pseudomonas syringae pv. glycinea. Plant Mol. Biol. 38: 1225–1234.Google Scholar
  105. Shiraishi, T., Yamada, K., Toyoda, K., Kato, T., Kin, H.M., Ishinose, Y. and Oku, H. 1994. Regulation of ATPase and signal transduction for pea defense responses by the suppressor and elicitor from Mycosphaerella pinodes. In: K. Kohmoto and O.C. Yoder (Eds.) Host-Specific Toxin: Biosynthesis, Receptor and Molecular Biology, Tottori University, Japan, pp. 169–182.Google Scholar
  106. Shirasu, K., Nakajima, H., Rajasekhar, V.K., 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: 1–10.Google Scholar
  107. Škalamera, D. and Heath, M.C. 1998. Changes in the cytoskeleton accompanying infection-induced nuclear movements and the hypersensitive response in plant cells invaded by rust fungi. Plant J. 16: 191–200.Google Scholar
  108. Stakman, E.C. 1915. Relation between Puccinia graminis and plants highly resistant to its attack. J. Agric. Res. 4: 193–200.Google Scholar
  109. Suzuki, K., Yano, A. and Shinshi, H. 1999. Slow and prolonged activation of the p47 protein kinase during hypersensitive cell death in a culture of tobacco cells. Plant Physiol. 119: 1465–1472.Google Scholar
  110. Thordal-Christensen, H., Zhang, Z., Wei, Y. and Collinge, D.B. 1997. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11: 1187–1194.Google Scholar
  111. Tomiyama, K., Sato, K., and Doke, N. 1982. Effect of cytochalasin B and colchicine on hypersensitive death of potato cells infected by incompatible race of Phytophthora infestans. Ann. Phytopath. Soc. Japan 48: 228–230.Google Scholar
  112. van der Biezen, E.A. and Jones, J.D.G. 1998. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8: R226–R227.Google Scholar
  113. Warren, R.F., Henk, A., Mowery, P., Holub, E. and Innes, R.W. 1998. A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10: 1439–1452.Google Scholar
  114. Xie, Z. and Chen, Z. 1999. Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells. Plant Physiol. 120: 217–225.Google Scholar
  115. Xu, H. and Heath, M.C. 1998. Role of calcium in signal transduction during the hypersensitive response caused by basidiosporederived infection of the cowpea rust fungus. Plant Cell 10: 585–597.Google Scholar
  116. Yano, A., Suzuki, K. and Shinshi, H. 1999. A signalling pathway, independent of the oxidative burst, that leads to hypersensitive cell death in cultured tobacco cells includes a serine protease. Plant J. 18: 105–109.Google Scholar
  117. Yu, I.-c., Parker, J. and Bent, A.F. 1998. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc. Natl. Acad. Sci. USA 95: 7819–7824.Google Scholar
  118. Zeyen, R.J., Bushnell, W.R., Carver, T.L.W., Robbins, M.P., Clark, T.A., Boyles, D.A. and Vance, C.P. 1995. Inhibiting phenylalanine ammonia lyase and cinnamyl-alcohol dehydrogenase suppresses Mla1 (HR) but not mlo5 (non-HR) barley powdery mildew resistances. Physiol. Mol. Plant Path. 47: 119–140.Google Scholar
  119. Zhao, Y., Jiang, Z.-F., Sun, Y.-L. and Zhai, Z.-H. 1999. Apoptosis of mouse liver nuclei in the cytosol of carrot cells. FEBS Lett. 448: 197–200.Google Scholar
  120. Zhou, J., Tang, X., Frederick, R. and Martin, G. 1998. Pathogen recognition and signal transduction by the Pto kinase. J. Plant Res. 111: 353–356.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Michèle C. Heath
    • 1
  1. 1.Botany DepartmentUniversity of TorontoTorontoCanada

Personalised recommendations