Death don't have no mercy: Cell death programs in plant-microbe interactions

Plant Cell

Volumn 8, Issue 10, 1996, Pages 1793-1807

  Dangl, Jeffery L ^a   Dietrich, Robert A ^a   Richberg, Michael H ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0030481542     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.8.10.1793     Document Type: Review

References (131)

1. Alfano, J.R., and Collmer, A. (1996). Bacterial pathogens in plants: Life up against the wall. Plant Cell 8, 1793-1807.
2. 2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol. 107, 1241-1247.
3. Baker, C.J., and Orlandi, E.W. (1995). Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33, 299-322.
4. Bater, C.J., Orlandi, E.W., and Mock, N.M. (1993). Harpin, an elicitor of the hypersensitive response in tobacco caused by Erwinia amylovora, elicits active oxygen production in suspension. Plant Physiol. 102, 1341-1344.
5. Becker, F., Buschfeld, E., Schell, J., and Bachmair, A. (1993). Altered response to viral infection by tobacco plants perturbed in ubiquitin system. Plant J. 3, 875-881.
6. Beffa, R.S., Hofer, R.-M., Thomas, M., and Meins, F., Jr. (1996). Decreased susceptibility to viral disease of β-1,3-glucanase-deficient plants generated by antisense transformation. Plant Cell 8, 1001-1011.
7. Bennetzen, J.L., Qin, M., Ingels, S., and Ellingboe, A.H. (1938). Allele-specific and Mutator-associated instability at the Rp1 disease-resistance locus of maize. Nature 332, 369-370.
8. Bent, A.F. (1996). Plant disease resistance genes: Function meets structure. Plant Cell 8, 1757-1771.
9. Bent, A.F., Innes, R.W., Ecker, J.R., and Staskawicz, B.J. (1992). Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens Mol. Plant-Microbe Interact. 5, 372-378.
10. Bestwick, C.S., Bennett, M.H., and Mansfield, J.W. (1995). Hrp mutant of Pseudomonas syringae pv. phaseolicola induces cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce. Plant Physiol. 108, 503-516.
11. 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, 235-246.
12. 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.
13. Boyes, D.C., McDowell, J.M., and Dangl, J.L. (1996). Many roads lead to resistance. Curr. Biol. 6, 634-637.
14. Bradley, D., Kjellbom, P., and Lamb, C. (1992). Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response. Cell 70, 21-30.
15. Brisson, L.F., Tenhaken, R., and Lamb, C. (1994). Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance Plant Cell 6, 1703-1712.
16. Cao, H., Bowling, S.A., Gordon, A.S., and Dong, X. (1994). Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6, 1583-1592.
17. 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 a fungal pathogen. Proc. Natl. Acad. Sci. USA 92, 6597-6601.
18. Chester, K.S. (1933). The problem of acquired physiological immunity in plants Q. Rev. Biol. 8, 275-324.
19. Cohen, Y., and Kuć, J. (1981). Evaluation of systemic resistance to blue mold induced in tobacco leaves by prior stem inoculation with Peronospora tabacina. Phytopathology 71, 783-787.
20. Collins, R.J., Harmon, B.V., Gobe, G.C., and Kerr, J.F.R. (1992). Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. Int. J. Radiat. Biol. 61, 451-453.
21. Croft, K., Juttner, F., and Slusarenko, A. (1993). Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol. 101, 13-24.
22. Culver, J.N., and Dawson, W.O. (1991). Tobacco mosaic virus elicitor coat protein genes produce a hypersensitive phenotype in transgenic Nicotiana sylvestris plants Mol. Plant-Microbe Interact. 4, 458-463.
23. Dangl, J.L. (1995). Pièce de résistance: Novel classes of plant disease resistance genes. Cell 80, 363-366
24. Delaney, T., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessman, H., Ward, E., and Ryals, J. (1994). A central role of salicylic acid in plant disease resistance. Science 266, 1247-1250.
25. 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.
26. Dietrich, R.A., Delaney, T.P., Uknes, S.J., Ward, E.J., Ryals, J.A., and Dangl, J.L. (1994). Arabidopsis mutants simulating disease resistance response. Cell 77, 565-578.
27. Dixon, M.S., Jones, D.A., Keddie, J.S., Thomas, C.M., Harrison, K., and Jones, J.D.G. (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leuckine-rich repeat proteins. Cell 84, 451-460.
28. Dixon, R.A., Harrison, M.J., and Lamb, C.J. (1994). Early events in the activation of plant defense responses. Annu. Rev. Phytopathol. 32, 479-501.
29. Doke, N. (1983). 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 Pathol. 23, 345-357.
30. - generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophthora infestans. Physiol. Plant Pathol. 27, 311-322.
31. --generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus. Physiol. Mol. Plant Pathol. 32, 163-175.
32. Dwyer, S.C., Legrendre, L., Low, P.S., and Leto, T.L. (1995). Plant and human neutrophil oxidative burst complexes contain immunologically related proteins. Biochem. Biophys. Acta 1289, 231-237.
33. Enyedi, A.J., Yalpani, N., Silverman, P., and Raskin, I. (1992). Signal molecules in systemic plant resistance to pathogens and pests. Cell 70, 879-886.
34. Fett, W.F., and Jones, S.B. (1995). Microscopy of the interaction of hrp mutants of Pseudmonas syringae pv. phaseolicola with a non-host plant. Plant Sci. 107, 27-39.
35. Freialdenhoven, A., Peterhänsel, C., Kurth, J., Kreuzaler, F., and Schulze-Lefert, P. (1996). Identification of genes required for the function of non-race-specific mlo resistance to powdery mildew in barley. Plant Cell 8, 5-14.
36. Freytag, S., Arabatzis, N., Hahlbrock, K., and Schmelzer, E. (1994). Reversible cytoplasmic rearrangements precede cell wall apposition, hypersensitive cell death and defense-related gene activation in potato/Phytophthora infestans interactions. Planta 194, 123-135.
37. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., and Ryals, J. (1993). Requirement for salicylic acid for the induction of systemic acquired resistance. Science 261, 754-756
38. Glazebrook, J., Rogers, E.E., and Ausubel, F.M. (1996). Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143, 973-982.
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.
40. Godiard, L., Grant, M.R., Dietrich, R.A., Kiedrowski, S., and Dangl, J.L. (1994). Perception and response in plant disease resistance. Curr. Opin. Genet. Dev. 4, 662-671.
41. Greenberg, J.T., and Ausubel, F.M. (1993). Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J. 4, 327-342.
42. Greenberg, J.T., and Sussex, I. (1996). Programmed cell death: A way of life for plants. Proc. Natl. Acad. Sci. USA, in press.
43. 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, 551-564.
44. Groom, Q.J., Torres, M.A., Fordham-Skelton, A.P., Hammond-Kosack, K.E., Robinson, N.J., and Jones, J.D.G. (1996). rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J. 10, 515-522.
45. Hahlbrock, K., Scheel, D., Logemann, E., Nurnburger, T., Parniske, M., Reinold, S., Sacks, W.R., and Schmelzer, E. (1995). Oligopeptide elicitor-mediated defense gene activation in cultured parsley cells. Proc. Natl. Acad. Sci. USA 92, 4150-4157.
46. Halliwell, B., and Gutteridge, J.M.C. (1989). Free Radicals in Biology and Medicine. (Oxford, UK: Clarendon Press).
47. Hammond-Kosack, K.E., and Jones, J.D.G. (1996). Resistance gene-dependent plant defense responses. Plant Cell 8, 1773-1791.
48. Hammond-Kosack, K.E., Harrison, K., and Jones, J.D.G. (1994) Developmentally regulated cell death on expression of the fungal avirulence gene Avr9 in tomato seedlings carrying the disease-resitance Cf-9 gene Proc. Natl. Acad. Sci. USA 91, 10445-10449
49. Hammond-Kosack, K.E., Silverman, P., Raskin, I., and Jones, J.D.G. (1996) Race-specific elicitors of Cladosporium fulvum induce changes in cell morphology, and ethylene and salicylic acid synthesis, in tomato cells carrying the corresponding Cf-disease resistance gene. Plant Physiol. 110, 1381-1394.
50. He, S.Y., Huang, H.-C., and Collmer, A. (1993). Pseudomonas syringae pv. syringae harpin Pss: A protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73, 1255-1266.
51. Hengartner, M.O., and Horvitz, H.R. (1994). Programmed cell death in Caenorhabditis elegans. Curr. Opin. Genet. Dev. 4, 581-586.
52. Herbers, K., Meuwly, P., Frommer, W.B., Métraux, J.-P., and Sonnewald, U. (1996). Systemic acquired resistance mediated by the ectopic expression of invertase: Possible hexose sensing in the secretory pathway. Plant Cell 8, 793-803
53. Hooker, A.L., and Russell, W.A. (1962). Inheritance of resistance to Puccinia sorghi in six maize inbred lines. Phytopathology 52, 122-128.
54. 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.
55. Huynh, T.V., Dahlbeck, D., and Staskawicz, B.J. (1989). Bacterial blight of soybean: Regulation of a pathogen gene determining host cuitivar specificity. Science 245, 1374-1377.
56. Inzé, D., and Van Montagu, M. (1995). Oxidative stress in plants. Curr. Opin. Biotechnol. 3, 153-158.
57. 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.
58. 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.
59. Jenns, A., and Kuć, J. (1977). Localized infection with tobacco necrosis virus protects cucumber against Colletotrichum lagenarium. Physiol. Plant Pathol. 11, 207-212.
60. Johal, G.S., Hulbert, S.H., and Briggs, S.P. (1994a). Disease lesion mimics of maize: A model for cell death in plants. Bioessays 17, 685-692.
61. Johal, G.S., Lee, E.A., Close, P.S., Coe, E.H., Neuffer, M.G., and Briggs, S.P. (1994b). A tale of two mimics: Transposon mutagenesis and characterization of two disease lesion mimic mutations in maize. Maydica 39, 69-76.
62. Jones, A.M., and Dangl, J.L. (1996). Logjam at the Styx: Programmed cell death in plants. Trends Plant Sci. 1, 114-119.
63. Jones, J.D.G. (1994). Paranoid plants have their genes examined. Curr. Biol. 4, 749-751.
64. 2. Plant Physiol. 108, 1171-1178.
65. Kauss, H., Theisinger-Hinkel, E., Mindermann, R., and Conrath, U. (1992). Dichloroisonicotinic and salicylic acid, inducers of systemic acquired resistance, enhance fungal elicitor responses in parsley cells. Plant J. 2, 655-660.
66. Kiyosawa, S. (1970). Inheritance of a particular sensitivity of the rice variety Sekiguchi Asahi, to pathogens and chemicals, and linkage relationships with blast resistance genes. Bull. Nat. Inst. Agric. Sci. (Jpn.) Ser. D Physiol. Genet. 21, 61-71.
67. Knogge, W. (1996). Fungal infection of plants. Plant Cell 8, 1711-1722.
68. Korsmeyer, S.J. (1995). Regulators of cell death. Trends Genet. 11, 101-105.
69. Kosslak, R.M., Dieter, J.R., Ruff, R.L., Chamberlin, M.A., Bowen, B.A., and Palmer, R.G. (1996). Tolerance to root-borne infection by Phytophthora sojae in three allelic necrotic-root mutants in soybean. J. Hered., in press.
70. Kuć, J. (1987). Plant immunization and its applicability for disease control. In Innovative Approaches to Plant Disease Control, I. Chet, ed (New York: John Wiley and Sons), pp. 255-275.
71. Langford, A.N. (1948). Autogenous necrosis in tomatoes immune from Cladosporium fulvum Cooke. Can. J. Res. 26, 35-64.
72. Lawton, K.A., Potter, S.L., Uknes, S., and Ryals, J. (1994) Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6, 581-588
73. Lawton, K., Weymann, K., Friedrich, L., Vernooij, B., Uknes, S., and Ryals, J. (1995). Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol. Plant-Microbe Interact. 8, 863-870.
74. Legendre, L., Reuter, S., Heinstein, P.F., and Low, P.S. (1993). Characterization of the oligogalacturonide-induced oxidative burst in cultured soybean (Glycine max) cells. Plant Physiol. 102, 233-240.
75. Lennon, S.V., Martin, S.J., and Cotter, T.G. (1991) Dose-dependent induction of apoptosis in human tumor cell lines by widely diverging stimuli. Cell Prolif. 24, 203-214.
76. Léon, J., Lawton, M.A., and Raskin, I. (1995). Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 108, 1673-1678.
77. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583-593.
78. Levine, A., Pennell, R., Palmer, R., and Lamb, C.J. (1996). Calcium-mediated apoptosis in a plant hypersensitive response. Curr. Biol. 6, 427-437.
79. Low, P.S., and Merida, J.H. (1996). The oxidative burst in plant defense: Function and signal transduction. Physiol. Plant. 96, 533-542.
80. Marchetti, M.A., Bollich, C.N., and Uecker, F.A. (1983). Spontaneous occurence of the Sekiguchi lesion in two American rice lines: Its induction, inheritance, and utilization. Phytopathology 73, 603-606.
81. Martin, G.B., Brommonschenkel, S.H., Chunwongse, J., Frary, A., Ganal, M.W., Spivey, R., Wu, T., Earle, E.D., and Tanksley, S.D. (1993). Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262, 1432-1436.
82. Mauch-Mani, B., and Slusarenko, A.J. (1996). Production of salicylic acid precursors is a major function of phenytalanine-ammonia lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8, 203-212.
83. May, M.J., Hammond-Kosack, K.E., and Jones, J.D.G. (1996). Involvement of reactive oxygen species, glutathione metabolism and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol. 110, 1367-1380.
84. Mehdy, M.C. (1994). Active oxygen species in plant defense against pathogens. Plant Physiol. 105, 467-472.
85. Mittler, R., and Lam, E. (1995). Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death. Plant Cell 7, 1951-1962.
86. Mittler, R., Shulaev, V., and Lam, E. (1995). Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plants expressing a bacterial proton pump. Plant Cell 7, 29-42.
87. Mur, L.A.J., Naylor, G., Warner, S.A.J., Sugars, J.M., White, R.R and Draper, J. (1996). Salicylic acid potentiates defence gene expression in tissue exhibiting acquired resistance to pathogen attack. Plant J. 9, 559-572.
88. Murphy, T.M., and Auh, C.-K. (1996). The superoxide synthases of plasma membrane preparations from cultured rose cells. Plant Physiol. 110, 621-629.
89. Nakashima, T., Sekiguchi, T., Kuraoka, A., Fukushima, K., Shibata, Y., Komiyama, S., and Nishimoto, T. (1993). Molecular cloning of a human cDNA encoding a novel protein, DAD1, whose defect causes apoptotic cell death in Hamster BHK21 cells. Mol. Cell. Biol. 13, 6367-6374.
90. Neuenschwander, U., Vernooij, B., Friedrich, L., Uknes, S., Kessman, H., and Ryals, J. (1995). Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? Plant J. 8, 227-234.
91. Nürnberger, T., Nennstiel, D., Jabs, T., Sacks, W.R., Hahlbrock, K., and Scheel, D. (1994). High-affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78, 449-460.
92. Peng, M., and Kuć, J. (1992). Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks. Phytopathology 82, 696-699.
93. Pryor, A. (1987a). The origin and stucture of fungal disease resistance genes. Trends Genet. 3, 157-161.
94. Pryor, T.P. (1987b). Stability of alleles at Rp (resistance to Puccinia sorghi). Maize Genet. Newsl. 61, 37-38.
95. Pryor, T.P., and Ellis, J. (1993). The genetic complexity of fungal resistance genes in plants. Adv. Plant Pathol. 10, 281-307.
96. Qin, X.-F., Holuigue, L., Horvath, D.M., and Chua, N.-H. (1994). Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element. Plant Cell 6, 863-874.
97. Raff, M. (1992). Social controls on cell survival and cell death. Nature 356, 397-400.
98. Raff, M.C., Barres, B.A., Burne, J.F., Coles, H.S., Ishizaki, Y., and Jacobson, M.D. (1993). Programmed cell death and the control of cell survival: Lessons from the nervous system. Science 262, 695-700.
99. Richter, T.E., Pryor, T.J., Bennetzen, J.B., and Hulbert, S.H. (1995). New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics 141, 373-381.
100. Ryals, J., Uknes, S., and Ward, E. (1994). Systemic acquired resistance. Plant Physiol. 104, 1109-1112.
101. Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H.-Y., and Hunt, M.D. (1996). Systemic acquired resistance. Plant Cell 8, 1809-1819.
102. Ryerson, D.E., and Heath, M.C. (1996). Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 8, 393-402.
103. Sano, H., Seo, S., Orudgev, E., Youssefian, S., Ishizuka, K., and Ohashi, Y. (1994). Expression of the gene for a small GTP binding protein in transgenic tobacco elevates endogenous cytokinin levels, abnormally induces salicylic acid in response to wounding and increases resistance to tobacco mosaic virus infection. Proc Natl. Acad. Sci. USA 91, 10556-10560.
104. Schmelzer, E., Krüger-Lebus, S., and Hahlbrock, K. (1989). Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. Plant Cell 1, 993-1001.
105. 2+ and protein-kinase activities. Planta 187, 136-141.
106. Segal, A.W., and Abo, A. (1993). The biochemical basis of the NADPH oxidase of phagocytes. Trends Biochem. Sci. 18, 48-52.
107. Somssich, I.E., Schmelzer, E., Kawalleck, P., and Hahlbrock, K. (1988) Gene structure and in situ transcript localization of pathogenesis-related protein 1 in parsley. Mol. Gen. Genet. 213, 93-98.
108. Staskawicz, B.J., Ausubel, F.M., Baker, B.J., Ellis, J., and Jones, J.D.G. (1995). Molecular genetics of plant disease resistance. Science 268, 661-667.
109. Stellar, H. (1995). Mechanisms and genes of cellular suicide. Science 267, 1445-1499.
110. Strittmatter, G., Janssens, J., Opsomer, C., and Botterman, J. (1995). Inhibition of fungal disease development in plants by controlled cell death. Bio/Technology 13, 1085-1089.
111. Sudupak, M., Bennetzen, J.L., and Hulbert, S.H. (1993). Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize Genetics 133, 119-125.
112. Sugimoto, A., Hozak, R.R., Makashima, T., Nishimoto, T., and Rothman, J.H. (1995). dad-1, an endogenous programmed cell death suppressor in Caenorhabditis elegans and vertebrates. EMBO J. 14, 4434-4441.
113. Takahashi, H., Goto, N., and Ehara, Y. (1994). Hypersensitive response in cucumber mosaic-virus infected Arabidopsis thaliana. Plant J. 6, 369-378.
114. Tavernier, E., Wendehenne, D., Blein, J.P., and Pugin, A. (1995). Involvement of free calcium in action of cryptogein, a proteinaceous elicitor of hypersensitive response in tobacco cells. Plant Physiol. 109, 1025-1031.
115. Tenhaken, R., Levine, A., Brisson, L.F., Dixon, R.A., and Lamb, C.J. (1995). Function of the oxidative burst in hypersensitive disease resistance Proc. Natl. Acad. Sci. USA 92, 4158-4163.
116. Uknes, S., Dincher, S., Friedrich, L., Negratto, D., Williams, S., Thompson-Taylor, H., Potter, S., Ward, E., and Ryals, J. (1993). Regulation of pathogenesis-related protein 1-a gene expression in tobacco. Plant Cell 5, 159-169.
117. Ullstrup, A.J., and Troyer, A.F. (1967). A lethal leaf spot of maize. Phytopathology 57, 1282-1283.
118. Van den Ackerveken, G.F.J.M., Van Kan, J.A.L., and De Wit, P.J.G.M. (1992). Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. Plant J. 2, 359-366.
119. Van Kan, J.A.L., Van den Ackerveten, G.F.J.M., and De Wit, P.J.G.M. (1991). Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol. Plant-Microbe Interact. 4, 52-59.
120. Vaux, D., Haecker, G., and Strasser, A. (1994). An evolutionary perspective on apoptosis. Cell 76, 777-779.
121. +-ATPase by elicitor-induced enzyme dephosphorylation. Plant Physiol. 104, 209-215.
122. Walbot, V., Hoisington, D.A., and Neuffer, M.G. (1983). Disease lesion mimics in maize. In Genetic Engineering of Plants, T. Kosuge and C. Meredith, eds (New York: Plenum Publishing), pp. 431-442.
123. Wang, H., Jones, C., Ciacci-Zanella, J., Holt, T., Gilchrist, D.G., and Dickman, M.B. (1996a). Fumonisins and AAI toxins: Sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. Proc. Natl. Acad. Sci. USA 93, 3461-3465.
124. Wang, H., Li, J., Bestock, R.M., and Gilchrist, D.G. (1996b). Apoptosis: A functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8, 375-391.
125. Weyman, 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.
126. Wolter, M., Hollricher, K., Salamini, F., and Schulze-Lefert, P. (1993). The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype. Mol. Gen. Genet. 239, 122-128.
127. 2-generating glucose oxidase in transgenic potato plants. Plant Cell 7, 1357-1368.
128. Wyllie, A.H. (1995) The genetic regulation of apoptosis Curr. Opin. Genet. Dev. 5, 97-104.
129. Wyllie, A.H., Kerr, J.F.H., and Curries, A.R. (1980). Cell death: The significance of apoptosis. Int. Rev Cytol 68, 251-306.
130. +-ATPase. Plant Cell 8, 555-564.
131. Zhou, J., Loh, Y., Bressan, R.A., and Martin, G.B. (1995). The tomato gene Pti encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83, 925-935.