Pathogen-induced programmed cell death in plants, a possible defense mechanism

Developmental Genetics

Volumn 21, Issue 4, 1997, Pages 279-289

  Mittler, Ron ^a,c   Del Pozo, Olga ^c   Meisel, Lee ^c   Lam, Eric ^b,c  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b RUTGERS UNIVERSITY   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Apoptosis; Hypersensitive response; Pathogen; Plant; Programmed cell death

Indexed keywords

APOPTOSIS; ARTICLE; CELL DEATH; DEFENSE MECHANISM; INFECTION; PLANT; PRIORITY JOURNAL; PROTEIN ISOLATION; RNA ANALYSIS; SIGNAL TRANSDUCTION;

APOPTOSIS; ARABIDOPSIS; IMMUNITY, NATURAL; PSEUDOMONAS; PSEUDOMONAS INFECTIONS;

EID: 0031445388     PISSN: 0192253X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1520-6408(1997)21:4<279::AID-DVG5>3.0.CO;2-4     Document Type: Article

References (84)

1. + exchange in suspension-cultured tobacco cells. Plant Physiol 91:298-303.
2. Baker CJ, Orlandi EW (1995): Active oxygen in plant pathogenesis. Annu Rev Phytopatol 33:299-321.
3. Becker F, Buschfeld E, Schell J, Bachmair A (1993): Altered response to viral infection by tobacco plants perturbed in ubiquitin system. Plant J 3:875-881.
4. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ (1994): RPS2 of Arabidopsis thaliana: A leucine-rich repeat class of plant disease resistance genes. Science 265:1856-1860.
5. Boise LH, Gonzalez-Gracia M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G, Thompson CB (1993): bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597-608.
6. Bortner CD, Oldenburg NBE, Cidlowski JA (1995): The role of DNA fragmentation in apoptosis. Trends Cell Biol 5:21-25.
7. Bowles DJ (1990): Defense-related proteins in higher plants. Annu Rev Biochem 59:873-907.
8. Bowling CA, Guo A, Cao H, Gordon SA, Klessig DF, Dong X (1994): A mutation in Arabidopsis that leades to constitutive expression of systemic acquired resistance. Plant Cell 6:1845-1857.
9. Boyes DC, McDowell JM, Dangl JL (1996): Many roads to resistance. Curr. Biol. 6:634-637.
10. Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor-and wound-induced oxidative cross-linking of proline-rich plant cell wall protein: A novel, rapid defense response. Cell 70:21-30.
11. Bump NJ, Hackett M, Hunginin M, Sheshagiri S, Brady K, Patrick C, Ferenz C, Franklin S, Ghayur T, Li P, Licari P, Mankovich J, Shi L, Greenberg AH, Miller LK, Wong WW (1995): Inhibition of ICE family proteases by Baculovirus antiapoptotic protein p35. Science 269:1885-1888.
12. Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, Van Daelen R, Van der Lee T, Diergaade P, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P (1997): The barley Mlo Gene: A novel control element of plant pathogen resistance. Cell 88:695-705.
13. Century KS, Holub EB, Staskawicz BJ (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.
14. Clarke AR, Purdie CA, Harrison DJ, Morris RG, Bird CC, Hooper ML, Wyllie AH (1993): Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 362:849-852.
15. Cornillon S, Foa C, Davoust J, Buonavista N, Gross JD, Golstein P (1994): Programmed cell death in Dictyostelium. J Cell Sci 107:2691-2704.
16. de Wit PJGM (1992): Molecular characterization of gene-for-gene systems in plant-fungus interactions and application of avirulance genes in control of plant pathogens. Ann Rev Phytopathol 30:391-418.
17. Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL (1994): Arabidopsis mutants simulating disease resistance response. Cell 77:565-577.
18. Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (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.
19. Ellis HM, Horvitz RH (1986): Genetic control of programmed cell death in the nematode C. elegans. Cell 44:817-829.
20. Felix G, Grosskopf DG, Regenass M, Boller T (1991): Rapid changes of the protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proc Natl Acad Sci USA 88:8831-8834.
21. Fraser A, Evan G (1996): A license to kill. Cell 85:781-784.
22. Fukuda H (1996): Xylogenesis: Initiation, progression, and cell death. Annu Rev Plant Physiol Plant Mol Biol 47:299-325.
23. Glazebrook J, Ausubel FM (1994): Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91:8955-8959.
24. Glazebrook J, Rogers EE, Ausubel FM (1996): Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143:973-982.
25. Glazener JA, Orlandi EW, Baker CJ (1996): The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause hypersensitive cell death. Plant Physiol 110:759-763.
26. Godiard L, Grant MR, Dietrich RA, Kiedrowski S, Dangl JL (1994): Perception and response in plant disease resistance. Curr Biol 4:662-671.
27. Goodman RN, Novacky AJ (1994): "The Hypersensitive Response Reaction in Plants to Pathogens, A Resistance Phenomenon." St. Paul, MN: American Phytopathological Society Press.
28. Gray J, Close PS, Briggs SP, Johal GS (1997): A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89:25-31.
29. Greenberg JT, Ausubel FM (1993): Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J. 4:327-342.
30. Greenberg JT, Ailan G, Klessig DF, Ausubel FM (1994): Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions. Cell 77:551-563.
31. Greenberg JT (1996): Programmed cell death: A way of life for plants. Proc Natl Acad Sci USA 93:12094-12097.
32. Gross P, Julius C, Schmelzer E, Hahlbrock K (1993): Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerization of microtubules and defence gene activation in infected, cultured parsley cells. EMBO J 12:1735-1744.
33. Hammond-Kosack KE, Harrison K, Jones JDG (1994): Developmentally regulated cell death on expression of the fungal avirulence gene Avr9 in tomato seedlings carrying the disease-resistance gene Cf-9. Proc Natl Acad Sci USA 91:10445-10449.
34. Hammond-Kosack KE, Silverman P, Raskin I, Jones JDG (1996): Race-specific elicitors of cladosporium fulvum induce changes in cell morphology and the synthesis of ethylene and salicylic acid in tomato plants carrying the corresponding Cf disease resistance gene. Plant Physiol 110:1381-1394.
35. He SY, Huang HC, Collmer A (1993): Pseudomonas syringae pv. syringae Harpin: a protein that is secreted via the hrp pathway and elicits the hypersensitive response in plants. Cell 73:1255-1266.
36. He SY, Bauer DW, Collmer A, Beer SV (1994): Hypersensitive response elicited by Erwinia amylovora harpin requires active plant metabo-lism. Mol Plant Micro Inter 7:289-292.
37. Henderson S, Rowe M, Gregory C, Croom-Carter D, Wang F, Longnecker R, Kieff E, Rickinson A (1991): Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from Programmed cell death. Cell 65:1107-1115.
38. Jacobson MD, Raff M (1995): Programmed cell death and Bcl-2 protection in very low oxygen. Nature 374:814-816.
39. Jakobek JL, Lindgren PB (1993): Generalized induction of defense response in bean is not correlated with the induction of the hypersensitive reaction. Plant Cell 5:49-56.
40. Jones DA, Thomas CM, Hammond-kosack KE, Balint-Kurti P, Jones JDG (1994): Isolation of the tomato Cf-9 gene for resistance to cladosporium fluvum by transposon tagging. Science 266:789-792.
41. Jones AM, Dangl JL (1996): Logjam at the Styx: Programmed cell death in plants. Trends Plant Sci 1:114-119.
42. Keen NT (1990): Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447-463.
43. Kerr JFR, Wyllie AH, Currie AR (1972): Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257.
44. Kerr JFR (1995): Neglected opportunities in apoptosis research. Trends Cell Biol 5:55-57.
45. Korsmeyer SG (1995). Regulators of cell death. Trends Genet 11:101-105.
46. Lakshmi R, Debbas M, Sabbatini P, Hockenbery D, Korsmeyer S, White E (1992): The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19kDa and Bcl-2 proteins. Proc Natl Acad Sci USA 89:7742-7746.
47. Lawton K, Uknes S, Friedrich L, Gaffney T, Alexander D, Goodman R, Metraux JP, Kessmann H, Ahl-Goy P, Gutrella M, Ward E, Ryals J (1993): The molecular biology of systemic acquired resistance. In Fritig B, Legrand M (eds): Mechanisms of Plant Defence Responses. Dordrecht, Netherlands: Kluwer, pp. 422-432.
48. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-593.
49. Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C (1996): Calcium-mediated apoptosis in plant hypersensitive disease resistance response. Curr Biol 6:427-437.
50. Linthorst JM (1991): Pathogenesis-related proteins of plants. Critical Rev Plant Sci 10:123-150.
51. Malamy J, Carr JP, Klessig DF, Raskin I (1990): Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002-1004.
52. Martin JS, Green RD, Cotter TG (1994): Dicing with death: Dissecting the components of the apoptosis machinery. Trends Biol Sci 19:26-30.
53. McLaughlin KA, Osborne BA, Goldsby RA (1996): The role of oxygen in thymocyte apoptosis. Eur J Immunol 26:1170-1174.
54. Metraux J-P, Singer H, Rayais J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B (1990): Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250:1004-1006.
55. Mindrinos M, Katagiri F, Yu G, Ausubel FM (1994): The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and a leucine-rich repeats. Cell 78:1089-1099.
56. Mittler R, Lam E (1995a): Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death. Plant Cell 7:1951-1962.
57. Mittler R, Lam E (1995b): In situ detection of nDNA fragmentation during the differentiation of tracheary elements in higher plants. Plant Physiol 108:489-493.
58. Mittler R, Shulaev V, 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.
59. Mittler R, Lam E (1996): Sacrifice in the face of foes: Pathogen-induced programmed cell death in higher plants. Trends Microbiol 4:10-15.
60. Mittler R, Shulaev V, Seskar M, Lam E (1996): Inhibition of programmed cell death in tobacco plants during pathogen-induced hypersensitive response at low oxygen pressure. Plant Cell 8:1991-2001.
61. Mittler R, Lam E (1997): Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress. Plant Mol Biol 34:209-221.
62. Mittler R, Simon L, Lam E (1997): Ultrastructural changes and fragmentation of nuclear and chloroplast DNA during the hypersensitive response in tobacco. J Cell Sci 110:1333-1344.
63. Nakashima T, Sekiguch T, Kuraoka A, Fukushima K, Shibata Y, Komiyama S, Nishimoto T (1993): Molecular cloning of a human cDNA encoding a novel protein, DAD1, whose defect causes apoptotic cell death in Hamster BHK21 cells. Molec Cell Biol 13:6367-6374.
64. Nurnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, Scheel D (1994): High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78:449-460.
65. Peitsch MC, Georg M, Tschopp J (1994): The apoptosis endonucleases: cleaning up after cell death. Trends Cell Biol. 4:37-41.
66. Raff CM (1992): Social controls on cell survival and cell death. Nature 356:397-400.
67. Ray CA, Pickup DJ (1996): The mode of death of pig kidney cells infected with cowpox virus is governed by the expression of the crmA gene. Virology 217:384-391.
68. Reyerson DE, Heath MC (1996): Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 8:393-402.
69. Schwartz LM, Smith SW, Jones MEE, Osborne BA (1993): Do all programmed cell death occur via apoptosis? Proc Natl Acad Sci USA 90:980-984.
70. Schwartzman RA, Cidlowski JA (1993): Apoptosis: The biochemistry and molecular biology of programmed cell death. Endocrine Rev 14:133-151.
71. Shimizu S, Eguchl Y, Kosaka H, Kamiike W, Matsuda H, Tsujimoto Y (1995): Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL. Nature 374:811-813.
72. Silberstein S, Collins PG, Kelleher DJ, Gilmore R (1995): The essential OST2 gene encodes the 16-kD subunit of the yeast oligosaccharyltransferase, a highly conserved protein expressed in diverse eukaryotic organisms. J Cell Biol 131:371-383.
73. Sugimoto A, Hozak RR, Nakashima T, Nishimoto T, Rothman H (1995): dad1, an endogenous programmed cell death suppressor in Caenorhabditis elegans and vertebrates. EMBO J. 14:4434-4441.
74. Takahashi H, Shimamoto K, Ehara Y (1989): Cauliflower mosaic virus gene VI causes growth suppression, development of necrotic spots and expression of defense-related genes in transgenic tobacco plants. Mol Gen Genet 216:188-194.
75. Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C (1995): Function of the oxidative burst in hypersensitive disease resistance. Proc Natl Acad Sci USA 92:4158-4163.
76. Vaux DL (1993): Toward an understanding of the molecular mechanisms of physiological cell death. Proc Natl Acad Sci USA 90:786-789.
77. Walbot V, Hoisington DA, Neuffer MG (1983): Disease lesion mimic mutations. In Kosuge T, Meredith C (eds): "Genetic Engineering of Plants." New York: Plenum, pp. 431-442.
78. Wang H, Li J, Bostock RM, Gilchrist DG (1996): Apoptosis: A functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8:375-391.
79. Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Metraux J-P, Ryals JA (1991): Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085-1094.
80. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994): The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor. Cell 78:1101-1115.
81. Wolter M, Hollricher K, Salamini F, Schulze-Lefert P (1993): The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defense mimic phenotype. Mol Gen Genet 239:122-128.
82. Wyllie AH, Morris RG, Smith AL, Dunlop D (1984): Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J Pathol 142:67-77.
83. Yarmolinsky MB (1995): Programmed cell death in bacterial populations. Science 267:836-837.
84. Zychlinsky A, Prevost MC, Sansonetti PJ (1992): Shigella flexneri induces apoptosis in infected macrophages. Nature 358:167-169.