Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco

Plant Journal

Volumn 33, Issue 4, 2003, Pages 621-632

  Dat, James F ^a,d   Pellinen, Riikka ^b,e   Beeckman, Tom ^a   Van De Cotte, Brigitte ^f   Langebartels, Christian ^c   Kangasjärvi, Jaakko ^b   Inzé, Dirk ^a   Van Breusegem, Frank ^a  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF HELSINKI   (Finland)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d université Bourgogne Franche Comté   (France)

^e UNIVERSITY OF EASTERN FINLAND   (Finland)

^f NONE

Author keywords

Abiotic stress; Cell death; Hydrogen peroxide; Oxidative burst; Signal transduction; Tobacco

Indexed keywords

CELLS; GENES; HYDROGEN PEROXIDE; OXIDATION; PLANTS (BOTANY); PROTEINS;

HOMEOSTASIS;

TOBACCO;

APOPTOSIS; CATALASE; CELL RESPIRATION; HOMEOSTASIS; HYDROGEN PEROXIDE; LIGHT; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION; TOBACCO;

CELLS; GENES; HYDROGEN PEROXIDE; OXIDATION; PLANTS; PROTEINS; TOBACCO;

NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

EID: 0345103736     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01655.x     Document Type: Article

References (93)

1. 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.
2. Asai, T., Stone, J.M., Heard, J.E., Kovtun, Y., Yorgey, P., Sheen, J. and Ausubel, F.M. (2000) Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell, 12, 1823-1835.
3. 2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol. 107, 1241-1247.
4. Bauer, C.S., Plieth, C., Bethmann, B., Popescu, O., Hansen, U.-P., Simonis, W. and Schönknecht, G. (1998) Strontium-induced repetitive calcium spikes in a unicellular green alga. Plant Physiol. 117, 545-557.
5. Beeckman, T. and Engler, G. (1994) An easy technique for the clearing of histochemically stained plant tissue. Plant Mol. Biol. Rep. 12, 37-42.
6. Bernardi, P., Petronilli, V., Di Lisa, F. and Forte, M. (2001) A mitochondrial perspective on cell death. Trends Biochem. Sci. 26, 112-117.
7. Bowler, C., Alliotte, T., De Loose, M., Van Montagu, M. and Inzė, D. (1989) The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia. EMBO J. 8, 31-38.
8. Bowler, C., Slooten, L., Vandenbranden, S., De Rycke, R., Botterman, J., Sybesma, C., Van Montagu, M. and Inzė, D. (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J. 10, 1723-1732.
9. Buckner, B., Johal, G.S. and Janick-Buckner, D. (2000) Cell death in maize. Physiol. Plant. 108, 231-239.
10. Carmody, R.J. and Cotter, T.G. (2000) Oxidative stress induces caspase-dependent retinal apoptosis in vitro. Cell Death Differ. 7, 282-291.
11. Cazalé, A.-C., Droillard, M.-J., Wilson, C., Heberle-Bors, E., Barbier-Brygoo, H. and Laurière, C. (1999) MAP kinase activation by hypoosmotic stress of tobacco cell suspensions: towards the oxidative burst response? Plant J. 19, 297-307.
12. Cazalé, A.-C., Rouet-Mayer, M.-A., Barbier-Brygoo, H., Mathieu, Y. and Laurière, C. (1998) Oxidative burst and hypoosmotic stress in tobacco cell suspensions. Plant Physiol. 116, 659-669.
13. Cessna, S.G., Sears, V.E., Dickman, M.B. and Low, P.S. (2000) Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell, 12, 2191-2199.
14. 2 in Transgenic Tobacco. PhD Thesis. Laboratorium voor Genetica: Universiteit Gent.
15. Chamnongpol, S., Willekens, H., Langebartels, C., Van Montagu, M., Inzé, D. and Van Camp, W. (1996) Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Plant J. 10, 491-503.
16. 2 in transgenic plants. Proc. Natl. Acad. Sci. USA, 95, 5818-5823.
17. Chivasa, S., Murphy, A.M., Naylor, M. and Carr, J.P. (1997) Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell, 9, 547-557.
18. Danon, A. and Gallois, P. (1998) UV-C radiation induces apoptotic-like changes in Arabidopsis thaliana. FEBS Lett. 437, 131-136.
19. Dat, J.F., Inzé, D. and Van Breusegem, F. (2001) Catalase-deficient tobacco plants: tools for in planta studies on the role of hydrogen peroxide. Redox Report, 6, 37-42.
20. Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzé, D. and Van Breusegem, F. (2000) Dual action of the active oxygen species during plant stress responses. Cell. Mol. Life Sci. 57, 779-795.
21. Delledonne, M., Zeier, J., Marocco, A. and Lamb, C. (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. USA, 98, 13454-13459.
22. - generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophthora infestans. Physiol. Plant Pathol. 27, 311-322.
23. Doke, N., Miura, Y., Sanchez, L.M. and Kawakita, K. (1994) Involvement of superoxide in signal transduction: responses to attack by pathogens, physical and chemical shocks, and UV irradiation. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants (Foyer, C.H. and Mullineaux, P.M., eds). Boca Raton: CRC Press, pp. 177-197.
24. Dong, X. (1998) SA, JA, ethylene, and disease resistance in plants. Curr. Opin. Plant Biol. 1, 316-323.
25. Draper, J. (1997) Salicylate, superoxide synthesis and cell suicide in plant defence. Trends Plant Sci. 2, 162-165.
26. Fiers, W., Beyaert, R., Declercq, W. and Vandenabeele, P. (1999) More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene, 18, 7719-7730.
27. Fleury, C., Mignotte, B. and Vayssìere, J.-L. (2002) Mitochondrial reactive oxygen species in cell death signaling. Biochimie, 84, 131-141.
28. 2- level in tobacco seedlings in relation to thermotolerance. Plant Physiol. 116, 429-437.
29. Greenberg, J.T. (1996) Programmed cell death: a way of life for plants. Proc. Natl. Acad. Sci. USA, 93, 12094-12097.
30. Halestrap, A.P., McStay, G.P. and Clarke, S.J. (2002) The permeability transition pore complex: another view. Biochimie, 84, 153-166.
31. Hancock, J.T., Desikan, R. and Neill, S.J. (2001) Does the redox status of cytochrome c act as a fail-safe mechanism in the regulation of programmed cell death? Free Radic. Biol. Med. 31, 697-703.
32. Jabs, T. (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem. Pharmacol. 57, 231-245.
33. - from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. USA, 94, 4800-4805.
34. Johansson, I., Karlsson, M., Shukla, V.K., Chrispeels, M.J., Larsson, C. and Kjellbom, P. (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell, 10, 451-459.
35. Jonak, C., Beisteiner, D., Beyerly, J. and Hirt, H. (2000) Wound-induced expression and activation of WIG, a novel glycogen synthase kinase 3. Plant Cell, 12, 1467-1475.
36. Jones, A. (2000) Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci. 5, 225-230.
37. Katsuhara, M. (1997) Apoptosis-like cell death in barley roots under salt stress. Plant Cell Physiol. 38, 1091-1093.
38. Koch, E. and Slusarenko, A. (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell, 2, 437-445.
39. Kratsch, H.A. and Wise, R.R. (2000) The ultrastructure of chilling stress. Plant Cell Environ. 23, 337-350.
40. Kroemer, G., Dallaporta, B. and Resche-Rigon, M. (1998) The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60, 619-642.
41. Kuo, A., Cappelluti, S., Cervantes-Cervantes, M., Rodriguez, M. and Bush, D.S. (1996) Okadaic acid, a protein phosphatase inhibitor blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells. Plant Cell, 8, 259-269.
42. Lam, E., Pontier, D. and del Pozo, O. (1999) Die and let live - programmed cell death in plants. Curr. Opin. Plant Biol. 2, 502-507.
43. Lamb, C. and Dixon, R.A. (1997) The oxidative burst in plant disease resistance. Ann. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
44. Lambeth, J.D. (2002) Nox/Duox family of nicotinamide adenine dinucleotide (phosphate) oxidases. Curr. Opin. Hematol. 9, 11-17.
45. Lee, J.H., Hübel, A. and Schöffl, F. (1995) Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis. Plant J. 8, 603-612.
46. 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.
47. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 79, 583-593.
48. Li, P.-F., Dietz, R. and von Harsdorf, R. (1999) p53 regulates mitochondrial membrane potential through reactive oxygen species and induces cytochrome c-independent apoptosis blocked by Bcl-2. EMBO J. 18, 6027-6036.
49. Loake, G. (2001) Plant cell death: unmasking the gatekeepers. Curr. Biol. 11, R1028-R1031.
50. Long, J.C. and Jenkins, G.I. (1998) Involvement of plasma membrane redox activity and calcium homeostasis in the UV-B and UV-A/blue light induction of gene expression in Arabidopsis. Plant Cell, 10, 2077-2086.
51. Lotan, T. and Fluhr, R. (1990) Xylanase, a novel elicitor of pathogenesis-related proteins in tobacco, uses a non-ethylene pathway for induction. Plant Physiol. 93, 811-817.
52. Low, P.S. and Merida, J.R. (1996) The oxidative burst in plant defense: function and signal transduction. Physiol. Plant. 96, 533-542.
53. McDowell, J.M. and Dangl, J.L. (2000) Signal transduction in the plant immune response. Trends Biochem. Sci. 25, 79-82.
54. Mittler, R., Simon, L. and Lam, E. (1997) Pathogen-induced programmed cell death in tobacco. J. Cell Sci. 110, 1333-1344.
55. 2+-dependent protein kinase activity during pollen tube reorientation. Plant Cell, 10, 1499-1509.
56. Navarre, D.A. and Wolpert, T.J. (1999) Victorin induction of an apoptotic/senescence-like response in oats. Plant Cell, 11, 237-249.
57. Noodén, L.D., Hillsberg, J.W. and Schneider, M.J. (1996) Induction of leaf senescence in Arabidopsis thaliana by long days through a light-dosage effect. Physiol. Plant. 96, 491-495.
58. O'Brien, I.E.W., Baguley, B.C., Murray, B.G., Morris, B.A.M. and Ferguson, I.B. (1998) Early stages of the apoptotic pathway in plant cells are reversible. Plant J. 13, 803-814.
59. Orozco-Cardenas, M. and Ryan, C.A. (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA, 96, 6553-6557.
60. Overmyer, K., Tuominen, H., Kettunen, R., Betz, C., Langebartels, C., Sandermann, H., Jr. and Kangasjärvi, J. (2000) Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell, 12, 1849-1862.
61. Papadakis, A.K. and Roubelakis-Angelakis, K.A. (1999) The generation of active oxygen species differs in tobacco and grapevine mesophyll protoplasts. Plant Physiol. 121, 197-205.
62. Pellinen, R., Palva, T. and Kangasjärvi, J. (1999) Subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. Plant J. 20, 349-356.
63. Pennell, R.I. and Lamb, C. (1997) Programmed cell death in plants. Plant Cell, 9, 1157-1168.
64. Pingret, J.-L., Journet, E.-P. and Barker, D.G. (1998) Rhizobium Nod factor signaling: evidence for a G protein-mediated transduction mechanism. Plant Cell, 10, 659-671.
65. Price, A.H., Taylor, A., Ripley, S.J., Griffiths, A., Trewavas, A.J. and Knight, M.R. (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell, 6, 1301-1310.
66. 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.
67. Rao, M.V., Lee, H.-i., Creelman, R.A., Mullet, J.E. and Davis, K.R. (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell, 12, 1633-1646.
68. Rhoads, D.M. and McIntosh, L. (1992) Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. Plant Cell, 4, 1131-1139.
69. Romeis, T., Piedras, P. and Jones, J.D.G. (2000) Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell, 12, 803-815.
70. phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 126, 1281-1290.
71. Scheel, D. (1998) Resistance response physiology and signal transduction. Curr. Opin. Plant Biol. 1, 305-310.
72. Schraudner, M., Moeder, W., Wiese, C., Van Camp, W., Inzé, D., Langebartels, C. and Sandermann, H., Jr. (1998) Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3. Plant J. 16, 235-245.
73. Solomon, M., Belenghi, B., Delledonne, M., Menachem, E. and Levine, A. (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell, 11, 431-443.
74. 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.
75. Takahashi, H., Chen, Z., Du, H., Liu, Y. and Klessig, D.F. (1997) Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. Plant J. 11, 993-1005.
76. Tamagnone, L., Merida, A., Parr, A., Mackay, S., Culianez-Macia, F.A., Roberts, K. and Martin, C. (1998) The AmMYB308 and AmMYB330 transcription factors from Antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell, 10, 135-154.
77. Tang, X., Xie, M., Kim, Y.J., Zhou, J., Klessig, D.F. and Martin, G.B. (1999) Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell, 11, 15-29.
78. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
79. Tiwari, B.S., Belenghi, B. and Levine, A. (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol. 128, 1271-1281.
80. phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA, 99, 517-522.
81. 2 and NO: redox signals in disease resistance. Trends Plant Sci. 3, 330-334.
82. - synthase from other NADPH oxidoreductases. Plant Physiol. 115, 543-550.
83. L regulates the membrane potential and volume homeostasis of mitochondria. Cell, 91, 627-637.
84. Vanlerberghe, G.C. and McIntosh, L. (1994) Mitochondrial electron transport regulation of nuclear gene expression. Studies with the alternative oxidase gene of tobacco. Plant Physiol. 105, 867-874.
85. Vera-Estrella, R., Blumwald, E. and Higgins, V.J. (1992) Effect of specific elicitors of Cladosporium fulvum on tomato suspension cells. Evidence for the involvement of active oxygen species. Plant Physiol. 99, 1208-1215.
86. Wang, H., Li, J., Bostock, R.M. and Gilchrist, D.G. (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.
87. Waterhouse, N.J. and Green, D.R. (1999) Mitochondria and apoptosis: HQ or high-security prison? J. Clin. Immunol. 19, 378-387.
88. Wendehenne, D., Pugin, A., Klessig, D.F. and Durner, J. (2001) Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci. 6, 177-183.
89. 3 plants. EMBO J. 16, 4806-4816.
90. Willekens, H., Inzé, D., Van Montagu, M. and Van Camp, W. (1995) Catalases in plants. Mol. Breed. 1, 207-228.
91. Willekens, H., Van Camp, W., Van Montagu, M., Inzé, D., Sandermann, H., Jr. and Langebartels, C. (1994) Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia (L.). Plant Physiol. 106, 1007-1014.
92. Xu, P. and Roossinck, M.J. (2000) Cucumber mosaic virus D satellite RNA-induced programmed cell death in tomato. Plant Cell, 12, 1079-1092.
93. Yano, A., Suzuki, K. and Shinshi, H. (1999) A signaling 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.