The hypersensitive response. A programmed cell death associated with plant resistance

Comptes Rendus de l'Academie des Sciences - Serie III

Volumn 321, Issue 9, 1998, Pages 721-734

  Pontier, Dominique ^a,b   Balagué, Claudine ^a   Roby, Dominique ^a  

^a CEMAGREF   (France)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Hypersensitive response; Plant pathogen interactions; Programmed cell death; Resistance

Indexed keywords

REACTIVE OXYGEN METABOLITE; VEGETABLE PROTEIN;

APOPTOSIS; HOST RESISTANCE; HYPERSENSITIVITY; ION CURRENT; NONHUMAN; PATHOGENESIS; PLANT; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0032172055     PISSN: 07644469     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0764-4469(98)80013-9     Document Type: Article

References (173)

1. [1] Bowles D.J., Defense-related proteins in higher plants, Annu. Rev. Biochem. 59 (1990) 873-907.
2. [2] Kombrink E., Somssich I.E., Defense responses of plants to pathogens, Adv. Bot. Res. 21 (1995) 1-34.
3. [3] Ryals J., Uknes S., Ward E., Systemic acquired resistance, Plant Physiol. 104 (1994) 1109-1112.
4. [4] Delaney T.P., Genetic dissection of acquired resistance to disease, Plant Physiol. 113 (1997) 5-12.
5. [5] Brown I., Mansfield J., Irlam I., Conrads-Srauch J., Bonas U., Ultrastructure of interactions between Xanthomonas campestris pv vesicatoria and pepper, including immuno-cytochemical localization of extracellular polyssacharides and the avrBS3 protein, Mol. Plant-Microbe Interact. 6 (1993) 376-386.
6. [6] Wang H., Li J., Bostock R.M., Gilchrist D.G., Apoptosis: A functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development, Plant Cell 8 (1996) 375-391.
7. [7] Mittler S.L.F., Lam E., In situ detection of nDNA fragmentation during the differentiation of tracheary elements in higher plants, Plant Physiol. 108 (1995) 489-493.
8. [8] Ryerson D.E., Heath M.C., Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatment, Plant Cell 8 (1996) 393-402.
9. [9] Dangl J.L., Dietrich R.A., Richberg M.H., Death don't have no mercy: cell death programs in plant-microbe interactions, Plant Cell 8 (1996) 1793-1807.
10. [10] Greenberg J.T., Programmed cell death in plant pathogen interactions, Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 (1997) 525-545.
11. [11] Keen N.T., Ersek T., Long M., Bruegger B., Holliday M., Inhibition of the hypersensitive response of soybean leaves to incompatible Pseudomonas spp. by blastocidin S, streptomycin or elevated temperature, Physiol. Plant Pathol. 18 (1981) 325-337.
12. Pss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants, Cell 73 (1993) 1255-1266.
13. [14] Beffa R., Szell M., Meuwly P., Pay A., Vogeli-Lange C., Metraux J.P., Neuhaus G., Meins F., Nagy F., Cholera toxin elevates pathogen resistance and induces pathogenesis-related gene expression in tobacco, EMBO J. 14 (1995) 5753-5761.
14. [15] Hammond-Kosack K.E., Harrison K., Jones J.D.G., Developmentally regulated cell death on expression of the fungal avirulence gene avr9 in tomato seedlings carrying the disease-resistance CT-9 gene, Proc. Natl. Acad. Sci. USA 91 (1994) 10445-10449.
15. [16] Culver J.N., Dawson W.O., Tobacco mosaic virus elicitor coat protein genes produce a hypersensitive phenotype in transgenic Nicotiana sylvestris plants, Mol. Plant-Microbe Interact. 5 (1991) 458-463.
16. [17] Becker F., Bushfield E., Schell J., Bachmair A., Altered response to viral infection by tobacco plants perturbed in ubiquitin system, Plant J. 3 (1993) 875-881.
17. [18] Herbers K., Meuwly P., Frommer W.B., Métraux J.P., Sonnewald U., Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway, Plant Cell 8 (1996) 793-803.
18. [19] Mittler R., Shulaev V., Lam E., Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plant expressing a bacterial proton pump, Plant Cell 7 (1995) 29-42.
19. [20] Mittler R., Lam E., Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death, Plant Cell 7 (1995) 1951-1962.
20. [21] Flor H.H., Host-parasite interaction in flax rust: Its genetics and other implications, Phytopathology 45 (1955) 680-685.
21. [22] Dangl J.L., The enigmatic avirulence genes of phytopathogenic bacteria, Curr. Opin. Microbiol. Immunol. 192 (1994) 99-118.
22. [23] Kobayashi D.Y., Tamaki S.J., Keen N.T., Cloned avirulence gene from the tomato pathogen Pseudomonas syringae pv. tomato cultivar specificity on soybean, Proc. Natl. Acad. Sci. USA 86 (1989) 157-161.
23. [24] Whalen M.C., Stall R.E., Staskawicz B.J., Characterization of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean, Proc. Natl. Acad. Sci. USA 85 (1988) 6743-6747.
24. [25] Whalen M.C., Wang J.F., Carland F.M., Heiskell M.F., Dahlbeck D., Minisavage G., Jones J.B., Scott J.V.V., Stall R.E., Staskawicz B.J., Avirulence gene avrXxv from Xanthomonas campestris pv vesicatoria specifies resistance on tomato line Hawaii 7998, Mol. Plant-Microbe Interact. 5 (1993) 616-627.
25. [26] Yucel I., Midland S.L., Sims J.J., Keen N.T., Class I and II avrD alleles direct the production of different products in Gram negative bacteria, Mol. Plant-Microbe Interact. 7 (1994) 148-150.
26. [27] Kobayashi D.A., Tamaki S.J., Keen N.T., Molecular characterization of avirulence gene D from Pseudomonas syringae pv. tomato, Mol. Plant-Microbe Interact. 3 (1990) 94-102.
27. [28] Kearney B., Staskawicz B.J., Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2, Nature 346 (1990) 385-386.
28. [29] Swarup S., De Feyter R., Brlansky R.H., Gabriel D.W., A pathogenicity locus from Xanthomonas citri enables strains from several pathovars of X. campestris to elicit canker-like lesions on citrus, Phytopathol. (1991) 802-809.
29. [30] De Feyter R., Yang Y., Gabriel G., Gene-for-gene interactions between cotton R genes and Xanthomonas campestris pv malvacearum, Mol. Plant-Microbe Interact. 6 (1993) 225-237.
30. [31] Lorang J.M., Shen H., Kobayashi D., Cooksey D., Keen N.T., AvrA and AvrE in Pseudomonas syringae pv. tomato PT23 play a role in virulence on tomato plants, Mol. Plant-Microbe Interact. 7 (1994) 508-515.
31. [32] Ritter C., Dangl J.L., The AvrRpm1 Gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis, Mol. Plant-Microbe Interact. 8 (1995) 444-453.
32. [33] Bonas U., Van den Ackerveken G., Recognition of bacterial avirulence proteins occurs inside the plant cell: a general phenomenon in resistance to bacterial diseases?, Plant J. 12 (1997) 1-7.
33. [34] Van Gijsegem F., Genin S., Boucher C., Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria, Trends Microbiol. 1 (1993) 175-180.
34. [35] Wei Z.M., Laby R.J., Zumoff C.H., Bauer D.W., He S.Y., Collmer A., Beer S.V., Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora, Science 257 (1992) 85-88.
35. [36] Arlat M., Van Gijsegem F., Huet J.C., Pernollet J.C., Boucher C., Pop A1, a protein which induces a hypersensitivity-like response on specific Petunia genotypes is secreted via the Hrp pathway of Pseudomonas solanacearum, EMBO J. 13 (1994) 543-553.
36. [37] Roine E., Wei W., Yuan J., Nurmiaho-Lassila E.L., Kalkkinen N., Romantschuk M., He S.Y., Hrp pilus: a hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000, Proc. Natl. Acad. Sci. USA 94 (1997) 3459-3464.
37. [38] Hammond-Kosack K. E., Jones J. D. G., Plant disease resistance genes, Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 (1997) 575-607.
38. [39] Boyes D. C., McDowell J. M., Dangl J. L., Many roads lead to resistance, Curr. Biol. 6 (1996) 634-637.
39. [40] Geghardt C., Plant genes for pathogen resistance-variation on a theme, Trends Plant Sci. 2 (1997) 243-244.
40. [41] Parker J.E., Coleman M.J., Molecular intimacy between proteins specifying plant-pathogen recognition, Trends Biochem. Sci. 22 (1997) 291-296.
41. [42] Baker B., Zambryski P., Staskawicz B., Dinesh-Kumar S.P., Signaling in plant-microbe interactions, Science 276 (1997) 726-732.
42. [43] De Wit P.J.G.M., Pathogen avirulence and plant resistance: a key role for recognition, Trends Plant Sci. 2 (1997) 452-458.
43. [44] Martin G.B., Brommonschenkel S.H., Chunwongse J., Frary A., Ganal M.W., Spivey R., Wu T., Earle E.D., Tanksley S.D., Map-based cloning of a protein kinase gene conferring disease resistance in tomato, Science 262 (1993) 1432-1436.
44. [45] Salmeron J.M., Barker S.J., Carland F.M., Mehta A.Y., Staskawicz B.J., Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition, Plant Cell 6 (1994) 511-520.
45. [46] Salmeron J.M., Oldroyd G.E.D., Rommens C.M.T., Scofield S.R., Kim H.S., Staskawicz B.J., Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster, Cell 86 (1996) 123-133.
46. [47] Kobe B., Deisenhofer J., The leucine-rich repeat: a versatile binding motif, Trends Biochem. Sci. 19 (1994) 415-421.
47. [48] Scofield S.R., Tobias C.M., Rathjen J.P., Chang J.H., Lavell D.T., Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato, Science 274 (1996) 2063-2065.
48. [49] Tang X., Frederick R.D., Zhou J., Halterman D.A., Martin G.B., Initiation of plant disease resistance by physical interaction of avrPto and Pto kinase, Science 274 (1996) 2060-2063.
49. [50] Century K.S., Holub E.B., Staskawicz B.J., 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 (1995) 6597-6601.
50. [51] Penninckx J.A.M.A., Eggermont K., Terras E.R.G., Thomma B.P.H.J., De Samblanx G.W., Buchala A., Métraux J.-P., Manners J.M., Broekaert W.F., Pathogen-induced sytemic activation of a plant defensin gene in Arabidopsis follows a salicilic acid-independent pathway, Plant Cell 8 (1996) 2309-2323.
51. [52] Peterhänsel C., Freiadenhoven A., Kurth J., Kolsch R., Schulze-Lefert P., Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death, Plant Cell 9 (1997) 1397-1409.
52. [53] Yang Y., Shah J., Klessig D.F, Signal perception and transduction in plant defense responses, Genes Dev. 11 (1997) 1621-1639.
53. 13Phosphate, Proc. Natl. Acad. Sci. USA 91 (1994) 952-956.
54. [55] Viard M.P., Martin F., Pugin A., Ricci P., Blein J.-P., Protein phosphorylation is induced in tobacco cells by the elicitor cryptogein, Plant Physiol. 104 (1994) 1245-1249.
55. [56] Chandra S., Low P.S., Role of phosphorylation in elicitation of the oxidative burst in cultured soybean cells, Proc. Natl. Acad. Sci. USA 92 (1995) 4120-4123.
56. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response, Cell 79 (1994) 583-593.
57. [58] Mackintosh C., Lyon G.D., Mackintosh R.W., Protein phosphatase inhibitors activate anti-fungal defense responses of soybean cotyledons and cell cultures, Plant J. 5 (1994) 137-147.
58. [59] Chandra S., Martin G., Low P.S., The Pto kinase mediates a signaling pathway leading to the oxidative burst in tomato, Proc. Natl. Acad. Sci. USA 93 (1996) 13393-13397.
59. [60] Loh Y.-T., Martin G.B., The Pto bacterial resistance gene and the Fen insecticide sensitivity gene encode functional protein kinases with serine/threonine specificity, Plant Physiol. 108 (1995) 1735-1739.
60. [61] Zhou J., Loh Y.-T., Bressan R.A., Martin G.B., The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response, Cell 83 (1995) 925-935.
61. [62] Zhou J., Tang X., Martin J.B., The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes, EMBO J. 16 (1997) 3207-3218.
62. [63] Doke N., Generation of superoxyde anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity, Physiol. Plant Pathol. 23 (1983) 359-367.
63. [64] Baker C.J., Orlandi E.W., Active oxygen in plant pathogenesis, Annu. Rev. Phytopathol. 33 (1995) 299-321.
64. [65] Lamb C., Dixon R.A., The oxidative burst in plant disease resistance, Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 (1997) 251-275.
65. [66] Alvarez M.E., Pennell R.I., Meijer P.-J., Ishikawa A., Dixon R.A., C.L., Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity, Cell 92 (1998) 773-784.
66. [67] Lummerzheim M., Molecular and genetic dissection of the hypersensitive response in Arabidopsis thaliana, Ph.D., Gand, 1996.
67. [68] Mittler R., Shulaev V., Seskar M., Lam E., Inhibition of programmed cell death in tobacco plants during a pathogen-induced hypersensitive response at low oxygen pressure, Plant Cell 8 (1996) 1991-2001.
68. [69] Gray J., Close P. S., Briggs S. P., Johal G. S., A novel suppressor of cell death in plants encoded by the Lls1 gene of maize, Cell 89 (1997) 25-31.
69. [70] Levine A., Pennell R.I., Alvarez M.E., Palmer R., Lamb C., Calcium-mediated apoptosis in a plant hypersensitive disease resistance response, Curr. Biol. 6 (1996) 427-437.
70. [71] Jabs T., Dietrich R.A., Dangl J.L., Initiation of runaway cell death in an Arabidopsis mutant by extracellular superperoxide, Science 273 (1996) 1853-1856.
71. [72] Nürnberger T., Nennstiel D., Jabs T., Sacks W.R., High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses, Cell 78 (1994) 449-460.
72. [73] Allan A. C., Fluhr R., Two distint sources of elicited reactive oxygen species in tobacco epidermal cells, Plant Cell 9 (1997) 1559-1572.
73. [74] Xing T., Higgins J., Blumwald E., Race-specific elicitors of Cladosporium fulvum promote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells., Plant Cell 9 (1997) 249-259.
74. [75] Jones O.T.G., The regulation of superoxide production by the NADPH oxidase of neutrophils and other mammalian cells, BioEssays 16 (1994) 919-923.
75. phox respiratory burst oxidase gene, Plant J. 10 (1996) 515-522.
76. 2+ binding motifs, Plant Cell 10 (1998) 255-266.
77. [78] Bestwick C.S., Brown I.R., Bennett M.H.R., Mansfield J.W., Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola, Plant Cell 9 (1997) 209-221.
78. [79] Peng M.J.K., Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks, Phytopathology 82 (1992) 696-699.
79. [80] Bradley D.J., Kjellbom P., Lamb C.J., Elicitor- and wound-incluced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response, Cell 70 (1992) 21-30.
80. [81] Brisson L.F., Tenhaken R., Lamb C., Function of oxydative cross-linking of cell-wall structural proteins in plant disease resistance, Plant Cell 6 (1994) 1703-1712.
81. [82] Leon J., Lawton M.A., Raskin I., Hydrogen peroxide stimulates salicilic acid biosynthesis in tobacco, Plant Physiol. 108 (1995) 1673-1678.
82. [83] Atkinson M.M., Keppler L.D., Orlandi E.W., Baker C.J., Mischke C.F., Involvement of plasma membrane calcium influx in bacterial induction of the K+/H+ and hypersensitive responses in tobacco, Plant Physiol. (1990) 215-221.
83. [84] Tavernier E., Wendehenne D., Blein J.-P., Pugin A., Involvement of free calcium in action of cryptogein, a proteinaceous elicitor of hypersensitive reaction in tobacco cells, Plant Physiol. 109 (1995) 1025-1031.
84. [85] Abad M.S., Hakimi S.M., Kaniewski W.J., Rommens C.M., Shulaev V., Lam E., Shah D.M., Characterization of acquired resistance in lesion-mimic transgenic potato expressing bacterio-opsin, Mol. Plant-Microbe Interact. 10 (1997) 635-645.
85. [86] Mittler R., del Pozo O., Meisel L., Lam E., Pathogen-induced programmed cell death in plants, a possible defense mechanism, Dev. Genet. 21 (1997) 279289.
86. - from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley, Proc. Natl. Acad. Sci. USA 94 (1997) 4800-4805.
87. [88] Glazener J.A., Orlandi E.W., Baker C.J., The active oxygen response of cell suspensions to imcompatible bacteria is not sufficient to cause hypersensitive cell death, Plant Physiol. 110 (1996) 759-763.
88. [89] Hammond-Kosack K.E., Jones J.D.G., Incomplete dominance of tomato Cf genes for resistance to Cladosporium fulvum, Mol. Plant-Microbe Interact. 7 (1994) 58-70.
89. l2-specified race-specific resistance to powdery mildew in barley, Plant Cell 6 (1994) 983-994.
90. [91] Freialdenhoven A., Peterhänsel C., Kurth J., Kreuzaler F., Schulze-Lefert P., Identification of genes required for the function of non-race-specific mL o resistance to powdery mildew in barley, Plant Cell 8 (1996) 5-14.
91. [92] Aviv D.H., Dietrich B.A., Parker J.E., Dangl J.L., Dissecting disease resistance pathways in Arabidopsis: Phenotypic analysis of lsd1/eds and lsd1/nim1 plants, in: 9th International Conference on Arabidopsis Research, Madison, Wisconsin, 1998, p. 494.
92. [93] Parker J.E., Holub E.B., Frost L.N., Falk A., Gunn N.D., Daniels M.J., Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes, Plant Cell 8 (1996) 2033-2046.
93. [94] Century K.S., Shapiro A.D., Repetti P.P., Dahlbeck D., Holub E., Staskawicz B.J., NDR1, a pathogen-induced component required for Arabidopsis disease resistance, Science 278 (1997) 1963-1965.
94. [95] Repetti P.P., Staskawicz B., Enhanced bacterial resistance due to overexpression of NDR1, a disease signaling component in Arabidopsis, in: 9th International Conference on Arabidopsis Research, Madison, Wisconsin, 1998, p 537.
95. [96] Dietrich R.A., Delaney T.P., Uknes S.J., Ward E.R., Ryals J.A., Dangl J.L., Arabidopsis mutants simulating disease resistance response, Cell 77 (1994) 565-577.
96. [97] Johal G.M., Hulbert S.H., Briggs P., Disease lesion mimics of maize: a model for cell death in plants, BioEssays 17 (1995) 685-692.
97. [98] Büschges R., Hollricher K., Panstruga R., Simons G., Wolter M., Frijters A., van Daelen R., van der Lee T., Diergaarde P., Groenendijk J., Töpsch S., Vos P., Salamini F., Schulze-Lefert P., The barley Mlo gene: a novel control element of plant pathogen resistance, Cell 88 (1997) 695-705.
98. [99] Dietrich R.A., Richberg M.H., Shmidt R., Dean C., Dangl J.L., A novel zing finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death, Cell 88 (1997) 685-694.
99. [100] Naton B., Hahlbrock K., Schmelzer E., Correlation of rapid cell death with metabolic changes in fungus-infected, cultured parsley cells, Plant Physiol. 112 (1996) 433-444.
100. [101] May M.J., Hammond-Kosack K.E., Jones J.D.J., 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 (1996) 1367-1379.
101. 2, Plant Physiol. 115 (1997) 137-149.
102. [103] White E., Life, death and the pursuit of apoptosis, Genes Dev. 10 (1996) 1-15.
103. [104] Villa P., Kaufmann S.H., Earnshaw W.C., Caspases and caspases inhibitors, Trends Biochem. Sci. 22 (1997) 388-392.
104. [105] del Pozo O., Lam E., Caspases and programmed cell death in the hypersensitive reaction of plants to pathogens, submitted (1998).
105. [106] Clem R.J., Hardwick M.J., Miller L.K., Active oxygen species in the induction of plant systemic acquired resistance by salicilic acid, Science 262 (1996) 1883-1886.
106. [107] Tenhaken R., Rübel C., Salicilic acid is needed in hypersensitive cell death in soybean but does not act as a catalase inhibitor, Plant Physiol. 115 (1997) 291-298.
107. [108] Weymann K., Hunt M., Uknes S., Neuenschwander U., Lawton K., Steiner H.Y., Ryals J., Suppression and restauration of lesion formation in Arabidopsis lsd mutants, Plant Cell 7 (1995) 2013-2022.
108. [109] Mur L.A.J., Bi Y.M., Darby R.M., Firek S., Draper J., Compromising early salicilic acid accumulation delays the hypersensitive response and increases viral dispersion during lesion establishment in TMV-infected tobacco, Plant J. 12 (1997) 1113-1126.
109. [110] Neuenschwander U., Vernooj B., Uknes S., Kessmann H., Ryals J., Is hydrogen peroxide a second messenger of salicilic acid in systemic acquired resistance?, Plant J. 8 (1995) 227-233.
110. [111] Summermatter K., Sticher L., Métraux J.-P., Systemic responses in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv syringae, Plant Physiol. 108 (1995)
111. [112] Shirasu K., Nakajima H., Rajasekhar V.K., Dixon R.A., Lamb C., Salicilic-acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms, Plant Cell 9 (1997) 261-270.
112. [113] Chen Z., Silva H., Klessig D., Active oxygen species in the induction of plant systemic acquired resistance by salicilic acid, Science 262 (1993) 1883-1886.
113. [114] Kiedrowski S., Kawalleck P., Hahlbrock K., Somssich I., Dangl J.L., Rapid activation of a novel plant defense gene is strictly dependent on the Arabidopsis RPM1 disease resistance locus, EMBO J. 11 (1992) 4667-4684.
114. [115] Pontier D., Godiard L., Marco Y., Roby D., Hsr2031, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant-pathogen interactions, Plant J. 5 (1994) 507-521.
115. [116] Pontier D., Tronchet M., Rogowsky P., Lam E., Roby D., Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death, Mol. Plant-Microbe Interact. 11 (1998) 544-554.
116. [117] Gopalan S., Wei W., He S.Y., hrp gene-dependent induction of hin1: a plant gene activated rapidly by both harpins and the avrPto gene-mediated signal, Plant J. 10 (1996) 591-600.
117. [118] Baudouin E., Charpenteau M., Roby D., Marco Y., Ranjeva R., Ranty B., Functional expression of a tobacco gene related to the serine hydrolase family. Esterase activity towards short chain dinitrophenyl acylesters, Eur. J. Biochem. 248 (1997) 700-706.
118. [119] Reuber T.L., Ausubel F.M., Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes, Plant Cell 8 (1996) 241-249.
119. [120] Ritter C., Dangl J.L., Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes, Plant Cell 8 (1996) 251-257.
120. [121] Daniel X., Lacomme C., Balagué C., Roby D., A novel MYB oncogen homolog in Arabidopsis thaliana related to the hypersensitive programmed cell death, in: 9th International Conference on Arabidopsis Research, Madison, WI, 1998, pp. 506.
121. [122] Freytag S., Arabatzis N., Hahlbrock K., Schmelzer E., Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell death and defense-related gene activation in potato/Phytophtora infestans interactions, Planta 194 (1994) 123-135.
122. [123] Greenberg J.T., Programmed cell death: A way of life for plants, Proc. Natl. Acad. Sci. USA 93 (1996) 12094-12097.
123. [124] Morel J.-B., Dangl J., The hypersensitive response and the induction of cell death in plants, Cell death Diff. 4 (1997) 671-683.
124. [125] Hammond-Kosack K.E., Jones D.A., Jones J.D.G., Identification of two genes required in tomato for full Cf-9-dependent response to Cladosporium fulvum, Plant Cell 6 (1994) 361-374.
125. [126] Yu I.-C., Parker J., Bent A.F., Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant, Proc. Natl. Acad. Sci. USA 95 (1998) 7819-7824.
126. [127] Somssich I., Hahlbrock K., Pathogen defence in plants - a paradigm of biological complexity, Trends Plant Sci. 3 (1998) 86-90.
127. [128] Chappell J., Levine A., Tenhaken R., Lusso M., Lamb C., Characterization of a diffusible signal capable of inducing defense gene expression in tobacco, Plant Physiol. 113 (1997) 621-629.
128. [129] Bowling S.A., Clarke J.D., Liu Y., Klessig D.F., Dong X., The cpr5 mutant of Arabidopsis expressed both NPR1-dependent and NPR1-independent resistance, Plant Cell 9 (1997) 1573-1584.
129. [130] Smith J.A., Hammerschmidt R., Fulbright D.W., Rapid induction of systemic resistance in cucumber by Pseudomonas syringae pv. syringae, Physiol. Mol. Plant. Pathol. 38 (1991) 223-235.
130. 2 in transgenic tobacco, Proc. Natl. Acad. Sci. USA 95 (1998) 5818-5823.
131. [132] Pieterse C.M.J., Van Wees S.C.M., Van Pelt J.A., Van Loon L.C., A novel signaling pathway controlling induced systemic reistance in Arabidopsis, in: 9th International Conference on Arabidopsis Research, Madison, WI, 1998, 14 p.
132. [133] Jones A.M., Dangl J.L., Logjam at the styx: programmed cell death in plants, Trends Plant Sci. 1 (1996) 114-119.
133. [134] Pennell R.I., Lamb C., Programmed cell death in plants, Plant Cell 9 (1997) 1157-1168.
134. [135] Martienssen R., Cell death: Fatal induction in plants, Curr. Biol. 7 (1997) R534-R537.
135. [136] Buchanan-Wollaston V., The molecular biology of leaf senescence, J. Exp. Bot. 48 (1997) 181-199.
136. [137] Noodén L.D., Guiamét J.J., John I., Senescence mechanisms, Physiol. Plant. 101 (1997) 746-753.
137. [138] Vaux D.L., Strasser A., The molecular biology of apoptosis, Proc. Natl. Acad. Sci. USA 93 (1996) 2239-2244.
138. [139] Schwartz L.M., Smith S.W., Jones M.E., OSborne B.A., Do all programmed cell deaths occur via apoptosis?, Proc. Natl. Acad. Sci. USA 90 (1993) 980-984.
139. [140] Gan S., Amasino R.M., Making sense of senescence., Plant Physiol. 113 (1997) 313-319.
140. [141] Lamb C.J., Lawton M.A., Dron M., Dixon R.A., Signals and transduction mechanisms for activation of plant defenses against microbial attack, Cell 56 (1989) 215-224.
141. [142] Dixon R.A., Lamb J., Molecular communication in interactions between plants and microbial pathogens, Annu. Rev. Plant Physiol. Plant Mol. Biol. 41 (1990) 339-367.
142. [143] Lasserre E., Godard F., Bouquin T., Hernandez J.A., Pech J.C., Roby D., Balagué C., Differential activation of two ACC oxidase gene promoters from melon during plant development and in response to pathogen attack, Mol. Gen. Genet. 256 (1997) 211-222.
143. [144] Borochov A., Woodson W.R., Physiology and biochemistry of flower petal senescence, Hortic. Rev. 11 (1989) 15-43.
144. [145] Grbic V., Bleecker A. B., Ethylene regulates the timing of leaf senescence in Arabidopsis, Plant J. 8 (1995) 595-602.
145. [146] Tang X., Gomes A.M.T.R., Bhatia A., Woodson W.R., Pistil-specific and ethylene-regulated expression of 1-aminocyclopropane-1-carboxylate oxidase genes in petunia flowers, Plant Cell 6 (1994) 1227-1239.
146. [147] Zarembinski T.I., Theologis A., Ethylene biosynthesis and action: a case of conservation, Plant. Mol. Biol. 26 (1994) 1579-1597.
147. [148] Pogson B.J., Downs C.G., Davies K.M., Differential expression of two 1-aminocyclopropane-1-carboxylic acid oxidase genes in broccoli after harvest, Plant Physiol. 108 (1995) 651-657.
148. [149] Barry C.S., Blume B., Bouzayen M., Cooper W., Hamilton A.J., Grierson D., Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato, Plant J. 9 (1996) 525-535.
149. [150] Lasserre E., Bouquin T., Hernandez J.A., Bull J., Pech J.C., Balagué C., Structure and expression of three genes encoding ACC oxidase homologs from melon (Cucumis melo L.), Mol. Gen. Genet. 251 (1996) 81-90.
150. [151] Orzaes D., Granell A., DNA fragmentation is regulated by ethylene during carpel senescence in Pisum sativum, Plant J. 11 (1997) 137-144.
151. [152] Boller T., Ethylene in pathogenesis and disease resistance, in: Mattoo A.K., Suttle J.C. (eds.), The Plant Hormone Ethylene, CRC Press Inc., Boca Raton, Florida, 1991, pp. 293-314.
152. [153] Bent A.F., Innes R.W., Ecker J.R., Staskawicz B.J., Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens, Mol. Plant-Microbe Interact. 5 (1992) 372-378.
153. [154] Korsmeyer S.J., Regulators of cell death, Trends Genet. 11 (1995) 101-105.
154. [155] Hengartner M.O., Horvitz H.R., C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2, Cell 76 (1994) 665-676.
155. [156] Golstein P., Controlling cell death, Science 275 (1997) 1081-1082.
156. [157] Salvesen G.S., Dixit V.M., Caspases: Intracellular signaling by proteolysis, Cell 91 (1997) 443-446.
157. [158] Polyak K., Xia Y., Zweier J.L., Kinzler K.W., Vogelstein B., A model for P53-induced apoptosis, Nature 389 (1997) 300-305.
158. [159] Whitham S., Dinesh-Kumar S.P., Choi D., Hehl R., Corr C., Baker B., The product of the tobacco mosaic virus resistance gene N: similarity to Toll and Interleukin-1 receptor, Cell 78 (1994) 1101-1115.
159. 6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N, Plant Cell 7 (1995) 1195-1206.
160. [161] Bent A.F., Plant disease resistance genes: function meets structure, Plant Cell 8 (1996) 1757-1771.
161. [162] Lemaitre B., Nicolas E., Michaut L., Reichhart J.-M., Hoffmann J., The dorsoventral regulatory gene cassete spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults, Cell 86 (1996) 973-983.
162. [163] Beg A.A., Baltimore D., An essential role for NFce encodes a novel protein containing ankyrin repeats, Cell 88 (1997) 57-63.
163. [164] Van Antwerp D.J., Martin S.M., Kafri T., Green D.J., Verma I.M., Suppression of TN-a-induced apoptosis by NK-kB, Science 274 (1996) 787-789.
164. [165] Wang C.Y., Mayo M.W., S.B.J.A., TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kB, Science 274 (1996) 784-787.
165. [166] Cao H., Glazebrook J., Clarke J.D., Volko S., Dong X., The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats, Cell 88 (1997) 57-63.
166. [167] Ryals J., Weimann C., Lawton K., Friedrich L., Ellis D., Steiner H.-Y., Johnson J., Delaney T.P., Jesse T., Vos P., Uknes S., The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IkB, Plant Cell 9 51997) 425-439.
167. [168] Shaham S., Shuman M.A., Herskowitz I., Death-defying yeast identity novel apoptosis genes, Cell (1998) 425-427.
168. [169] Nakashima T., Sekiguchi T., Kuraoka A., Fukushima K., Shibata Y., Komiyama S., Nishimoto T., Molecular cloning of human cDNA encoding a novel protein, DAD1, whose defect causes apoptotic cell death in hamster BHK21 cells, Mol. Cell. Biol. 13 (1993) 6367-6374.
169. [170] Gallois P., Makishima T., Hecht V., Despres B., Laudie M., Nishimoto T., Cooke R., An Arabidopsis thaliana cDNA complementating a hamster apoptosis suppressor mutant, Plant J. 11 (1997) 1325-1331.
170. [171] Tanaka Y., Makishima T., Sasabe M., Ichinose Y., Shiraishi T., Nishimoto T., Yamada T., dad-1, a putative programmed cell death suppressor gene in rice, Plant Cell Physiol. 38 (1997) 379-383.
171. [172] Orzaez D., Granell A., The plant homologue of the defender against apoplotic death gene is down-regulated during senescence of flower petals, FEBS Lett. 404 (1997) 275-278.
172. [173] Vaux D. L., Haecker G., Strasser A., An evolutionary perspective on apoptosis, Cell 76 (1994) 777-779.
173. [174] Ameisen J. C., The origin of programmed cell death, Science 272 (1996) 272-273.