Induction of programmed cell death in lily by the fungal pathogen Botrytis elliptica

Molecular Plant Pathology

Volumn 5, Issue 6, 2004, Pages 559-574

  Van Baarlen, Peter ^a   Staats, Martijn ^a   Van Kan, Jan A L ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ARABIDOPSIS; BOTRYOTINIA FUCKELIANA; BOTRYTIS; BOTRYTIS TULIPAE; FUNGI; LILIUM;

EID: 9944222855     PISSN: 14646722     EISSN: None     Source Type: Journal    
DOI: 10.1111/J.1364-3703.2004.00253.X     Document Type: Article

References (74)

1. Alderton, W.K., Cooper, C.E. and Knowles, R.G. (2001) Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357, 593-615.
2. Amarante-Mendes, G.P., Kim, C.N., Liu, L., Huang, Y., Perkins, C.L., Green, D.R. and Bhalla, K. (1998) Bcr-Abl exerts its antiapoptotic effect against diverse apoptotic stimuli through blockage of mitochondrial release of cytochrome C and activation of caspase-3. Blood, 91, 1700-1705.
3. 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.
4. Barroso, J.B., Corpas, F.J., Carreras, A., Sandalio, L.M., Valderrama, R., Palma, J.M., Lupiáñez, J.A. and del Rio, L.A. (1999) Localization of nitric oxide synthase in plant peroxisomes. J. Biol. Chem. 274, 36729-36733.
5. Beers, E.P., Woffenden, B.J. and Zhao, C. (2000) Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol. Biol. 44, 399-415.
6. Benito, E.P., ten Have, A., van 'T Klooster, J.W. and van Kan, J.A.L. (1998) Fungal and plant gene expression during synchronized infection of tomato leaves by Botrytis cinerea. Eur. J. Plant Pathol. 104, 207-220.
7. Brüne, B. (2003) Nitric oxide: no apoptosis or turning it on? Cell Death Differ. 10, 864-869.
8. Chae, H.S. and Lee, W.S. (2001) Ethylene- and enzyme-mediated superoxide production and cell death in carrot cells grown under carbon starvation. Plant Cell Rep. 20, 256-261.
9. Chandok, M.R., Ytterberg, A.J., van Wijk, K.J. and Klessig, D.F. (2003) The pathogen-inducible nitric oxide synthase (iNOS) in plants is a variant of the P protein of the glycine decarboxylase complex. Cell, 113, 469-482.
10. Chichkova, N.V., Kim, S.H., Titova, E.S., Kalkum, M., Morozov, V.S., Rubtsov, Y.P., Kalinina, N.O., Taliansky, M.E. and Vartapatian, A.B. (2004) A plant caspase-like protease activated during the hypersensitive response. Plant Cell, 16, 157-171.
11. Collins, N.C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J.-L., Hückelhoven, R., Stein, M., Freialdenhoven, A., Somerville, S.C. and Schulze-Lefert, P. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature, 425, 973-977.
12. Conrath, U., Amoroso, G., Köhle, H. and Sültemeyer, D.F. (2004) Non-invasive online detection of nitric oxide from plants and some other organisms by mass spectrometry. Plant J. 38, 1015-1022.
13. Corpas, F.J., Barroso, J.B. and del Rio, L.A. (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6, 145-150.
14. Dangl, J.L., Dietrich, R.A. and Thomas, H. (2000) Senescence and programmed cell death. In: Biochemistry and Molecular Biology of Plants (Buchanan, B., Gruissem, W. and Jones, R., eds). Rockwille, MD: American Society of Plant Physiologists, pp. 1044-1100.
15. DeGuzman, R. and Riggs, C.D. (2000) A survey of proteinases active during meiotic development. Planta, 210, 921-924.
16. Delledonne, M., Murgia, I., Ederle, D., Sbicego, P.F., Biondani, A., Polverari, A. and Lamb, C. (2002) Reactive oxygen intermediates modulate nitric oxide signaling in the plant hypersensitive disease-resistance response. Plant Phys. Biochem. 40, 605-610.
17. 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.
18. Denecker, G., Vercammen, D., Steemans, M., van den Berghe, T., Brouckaert, G., van Loo, G., Zhivotovsky, B., Fiers, W., Grooten, J., DecLercq, W. and Vandenabeele, P. (2001) Death receptor-induced apoptotic and necrotic cell death: differential role of caspases and mitochondria. Cell Death Different. 8, 829-840.
19. Drexler, H.C.A. (1997) Activation of the cell death program by inhibition of proteasome function. Proc. Natl Acad. Sci. USA, 94, 855-860.
20. Edlich, W., Lorenz, G., Lyr, H., Nega, E. and Pommer, E.-H. (1989) New aspects on the infection mechanism of Botrytis cinerea Pers. Neth. J. Plant Pathol. 95, 53-62.
21. Farmer, E.E., Alméras, E. and Krishnamurthy, V. (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr. Opin. Plant Biol. 6, 372-378.
22. Foissner, I., Wendehenne, D., Langebartels, C. and Durner, J. (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J. 23, 817-824.
23. Govrin, E.M. and Levine, A. (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10, 751-757.
24. 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, 551-563.
25. Haugland, R.P. (2002) Handbook of Fluorescent Probes and Research Products, 9th edn. Eugene, OR: Molecular Probes, Inc.
26. Hearps, A.C., Burrows, J., Connor, C.E., Woods, G.M., Lowenthal, R.M. and Ragg, S.J. (2002) Mitochondrial cytochrome c release precedes transmembrane depolarisation and caspase-3 activation during ceramide-induced apoptosis of Jurkat cells. Apoptosis, 7, 387-394.
27. Heath, M.C. (2000a) Hypersensitive response-related death. Plant Mol. Biol. 44, 321-334.
28. Heath, M.C. (2000b) Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3, 315-319.
29. Hoeberichts, F.A., ten Have, A. and Woltering, E.J. (2003) A tomato metacaspase gene is upregulated during programmed cell death in Botrytis cinerea-infected leaves. Planta, 217, 517-522.
30. Hoeberichts, F.A. and Woltering, E.J. (2002) Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. Bioessays, 25, 47-57.
31. Iwai, K., Kondo, T., Watanabe, M., Yabu, T., Kitano, T., Taguchi, Y., Umehara, H., Takahashi, A., Uchiyama, T. and Okazaki, T. (2003) Ceramide increases oxidative damage due to inhibition of catalase by caspase-3-dependent proteolysis in HL-60 cell apoptosis. J. Biol. Chem. 278, 9813-9822.
32. Kachroo, A., Lapchyk, L., Fukushige, H., Hildebrand, D., Klessig, D. and Kachroo, P. (2003) Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell, 15, 2952-2965.
33. Kim, Y.-M., Talanian, R.V. and Billiar, T.R. (1997) Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 272, 31138-31148.
34. Korthout, H.A.A.J., Berecki, G., Bruin, W., van Duijn, B. and Wang, M. (2000) The presence and subcellular localization of caspase-3-like proteinases in plant cells. FEBS Lett. 475, 139-144.
35. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
36. Lam, E. and del Pozo, O. (2000) Caspase-like protease involvement in the control of plant cell death. Plant Mol. Biol. 44, 417-428.
37. Lehtonen, J.Y.A., Horiuchi, M., Daviet, L., Akishita, M. and Dzau, V.J. (1999) Activation of the de novo biosynthesis of sphingolipids mediates angiotensin II type 2 receptor-induced apoptosis. J. Biol. Chem. 274, 16901-16909.
38. Liang, H., Yao, N., Song, J.T., Luo, S., Lu, H. and Greenberg, J.T. (2003) Ceramides modulate programmed cell death in plants. Genes Dev. 17, 2636-2641.
39. Lockshin, R.A. and Zakeri, Z. (2002) Caspase-independent cell deaths. Curr. Opin. Cell Biol. 14, 727-733.
40. Mannick, J.B., Schonhoff, C., Papeta, N., Ghafourifar, P., Szibor, M., Fang, K. and Gaston, B. (2001) S-nitrosylation of mitochondrial caspases. J. Cell Biol. 154, 1111-1116.
41. Mengiste, T., Chen, X., Salmeron, J. and Dietrich, R. (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell, 15, 2551-2565.
42. Meyer, R., Slater, V. and Dubery, I.A. (1994) A phytotoxic protein-lipopolysaccharide complex produced by Verticillium dahliae. Phytochemistry, 35, 1449-1453.
43. Morel, J.B. and Dangl, J.L. (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4, 671-683.
44. Navarre, D.A. and Wolpert, T.J. (1999) Victorin induction of an apoptotic/senescence-like response in oats. Plant Cell, 11, 237-249.
45. Overmyer, K., Brosché, M. and Kangasjärvi, J. (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 8, 335-342.
46. Pennell, I.P. and Lamb, C. (1997) Programmed cell death in plants. Plant Cell, 9, 1157-1168.
47. 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.
48. Pružinská, A., Tanner, G., Anders, I., Roca, M. and Hörtensteiner, S. (2003) Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc. Natl Acad. Sci. USA, 100, 15259-15264.
49. 2-generating systems in Botrytis cinerea: the major Cu-Zn-superoxide dismutase (BCSOD1) contributes to virulence on French bean, whereas a glucose oxidase (BCGOD1) is dispensable. Mol. Plant Pathol. 5, 17-27.
50. Ryerson, D.E. and Heath, M.C. (1996) Cleavage of nuclear DNA in oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell, 8, 393-402.
51. Sass, J.E. (1958) Botanical Microtechnique. Ames, IA: Iowa State University Press.
52. Schlegel, J., Peters, I., Orrenius, S., Miller, D.K., Thornberry, N.A., Yamin, T-T. and Nicholson, D.W. (1996) CPP32/Apopain is a key interleukin 1β converting enzyme-like protease involved in Fas-mediated apoptosis. J. Biol. Chem. 271, 1841-1844.
53. Schoenwaelder, S.M. and Burridge, K. (1999) Evidence for a calpeptin-sensitive protein-tyrosine phosphatase upstream of the small GTPase Rho. J. Biol. Chem. 274, 14359-14367.
54. Schotte, P., DecLercq, W., van Huffel, S., Vandenabeele, P. and Beyaert, R. (1999) Non-specific effects of methyl ketone peptide inhibitors of caspases. FEBS Lett. 442, 117-121.
55. Schuurhuis, G.J., Monnee, V., Muijen, M., Oberink, J.W., de Boer, F., Ossenkoppele, G.J. and Broxterman, H.J. (2001) Large populations of non-clonogenic early apoptotic CD34-positive cells are present in frozen-thawed peripheral blood stem cell transplants. Bone Marrow Transplant. 27, 487-498.
56. Shirazu, K. and Schulze-Lefert, P. (2000) Regulators of cell death in disease resistance. Plant Mol. Biol. 44, 371-385.
57. 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.
58. Strelkov, S.E., Lamari, L. and Ballance, G.M. (1999) Characterization of a host-specific protein toxin (PtrToxB) from Pyrenophora tritici-repens. Mol. Plant-Microbe Interact. 12, 728-732.
59. Sullivan, J.A., Shirazu, K. and Deng, X.W. (2003) The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nature Rev. Genet. 4, 948-958.
60. Tada, Y., Hata, S., Takata, Y., Nakayashiki, H., Tosa, Y. and Mayama, S. (2001) Induction and signaling of an apoptotic response typified by DNA laddering in the defense response of oats to infection and elicitors. Mol. Plant-Microbe Interact. 14, 477-486.
61. Tada, Y., Mori, T., Shinogi, T., Yao, N., Takahashi, S., Betsuyaku, S., Sakamoto, M., Park, P., Nakayashiki, H., Tosa, Y. and Mayama, S. (2004) Nitric oxide and reactive oxygen species do not elicit hypersensitive cell death but induce apoptosis in the adjacent cells during the defense response of oats. Mol. Plant-Microbe Interact. 17, 245-253.
62. Tiedemann, A.V. (1997) Evidence for a primary role of active oxygen species in induction of host cell death during infection of bean leaves with Botrytis cinerea. Phys. Mol. Plant Pathol. 50, 151-166.
63. Uren, A.G., O'Rourke, K., Aravind, L., Pisabarro, M.T., Seshagiri, S., Koonin, E.V. and Dixit, V.M. (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell, 6, 961-967.
64. Virág, L., Marmer, D.J. and Szabó, C. (1998) Crucial role of apopain in the peroxynitrite-induced apoptotic DNA fragmentation. Free Radic. Biol. Med. 25, 1075-1082.
65. Walton, J.D. (1996) Host-selective toxins: agents of compatibility. Plant Cell, 8, 1723-1733.
66. Wang, K.K.W. (2000) Calpain and caspase: can you tell the difference? Trends Neurosci. 23, 20-26.
67. Wang, H., Li, J., Bostock, V. 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.
68. Watanabe, N. and Lam, E. (2004) Recent advance in the study of caspase-like proteases and Bax inhibitor-1 in plants: their possible roles as regulator of programmed cell death. Mol. Plant Pathol. 5, 65-70.
69. Wolpert, T.J., Dunkle, L.D. and Ciuffetti, L.M. (2002) Host-selective toxins and avirulence determinants: what's in a name? Annu. Rev. Phytopathol. 40, 251-285.
70. Woltering, E.J., van der Bent, A. and Hoeberichts, F.A. (2002) Do plant caspases exist? Plant Phys. 130, 1764-1769.
71. Xu, H. and Heath, M.C. (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell, 10, 585-597.
72. Zang, Y., Beard, R.L., Chandraratna, R.A.S. and Kang, J.X. (2001) Evidence of a lysosomal pathway for apoptosis induced by the synthetic retinoid CD437 in human leukemia HL-60 cells. Cell Death Differ. 8, 477-485.
73. Zech, B., Köhl, R., von Knethen, A. and Brüne, B. (2003) Nitric oxide donors inhibit formation of the Apaf-1/caspase-9 apoptosome and activation of caspases. Biochem. J. 371, 1055-1064.
74. Zhang, H.-F., Francl, L.J., Jordahl, J.G. and Meinhardt, S.W. (1997) Structural and physical properties of a necrosis-inducing toxin from Pyrenophora tritici-repentis. Phytopathology, 87, 154-160.