Victorin triggers programmed cell death and the defense response via interaction with a cell surface mediator

Plant and Cell Physiology

Volumn 46, Issue 11, 2005, Pages 1787-1798

  Tada, Yasuomi ^a,b   Kusaka, Koh ^a,c   Betsuyaku, Shigeyuki ^a,c   Shinogi, Takeshi ^a,d   Sakamoto, Masaru ^a   Ohura, Yasuko ^a   Hata, Shingo ^a   Mori, Tomoyo ^a   Tosa, Yukio ^a   Mayama, Shigeyuki ^a  

^a KOBE UNIVERSITY   (Japan)

^b DUKE UNIVERSITY   (United States)

^c MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^d HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Apoptosis; Avena sativa; Cochliobolus victoriae; Programmed cell death; Vb; Victorin

Indexed keywords

CALCIUM; FUNGAL PROTEIN; MYCOTOXIN; VICTORIN PROTEIN, COCHLIOBOLUS VICTORIAE;

APOPTOSIS; ARTICLE; CELL MEMBRANE; CYTOLOGY; METABOLISM; OAT; PH; PHYSIOLOGY; PLANT LEAF;

APOPTOSIS; AVENA SATIVA; CALCIUM; CELL MEMBRANE; FUNGAL PROTEINS; HYDROGEN-ION CONCENTRATION; MYCOTOXINS; PLANT LEAVES;

AVENA; AVENA SATIVA; BOVINAE; COCHLIOBOLUS; COCHLIOBOLUS VICTORIAE;

EID: 28544437389     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pci193     Document Type: Article

References (42)

1. Akimitsu, K., Hart, L.P. and Walton, J.D. (1993a) Density gradient study of victorin-binding proteins in oat (Avena sativa) cells. Plant Physiol. 103: 67-72.
2. Akimitsu, K., Hart, L.P. and Walton, J.D. (1993b) Immunological evidence for a cell surface receptor of victorin using anti-victorin anti-idiotypic polyclonal antibodies. Mol. Plant-Microbe Interact. 6: 429-433.
3. Akimitsu, K., Hart, L.P., Walton, J.D. and Hollingsworth, R. (1992) Covalent binding sites of victorin in oat leaf tissues detected by anti-victorin polyclonal antibodies. Plant Physiol. 98: 121-126.
4. Atkinson, S.J., Hosford, M.A. and Molitoris, B.A. (2004) Mechanism of actin polymerization in cellular ATP depletion. J. Biol. Chem. 279: 5194-5199.
5. + efflux, and extracellular alkalization in soybean cells carrying the disease-resistance gene Rpg4. Plant Physiol. 112: 297-302.
6. Blume, B., Nurnberger, T., Nass, N. and Scheel, D. (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12: 1425-1440.
7. Chin, D. and Means, A.R. (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10: 322-328.
8. Curtis, M.J. and Wolpert, T.J. (2002) The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death. Plant J. 29: 295-312.
9. Curtis, M.J. and Wolpert, T.J. (2004) The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity. Plant J. 38: 244-259.
10. Dangl, J.L. and Jones, J.D. (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
11. Govrin, E.M. and Levine, A. (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10: 751-757.
12. Keen, N.T. and Buzzell, R.I. (1991) New disease resistance genes in soybean against Pseudomonas syringae pv. glycinea: evidence that one of them interacts with a bacterial elicitor. Theor. Appl. Genet. 81: 133-138.
13. Knodler, L.A., Celli, J. and Finlay, B.B. (2001) Pathogenic trickery: deception of host cell processes. Nat. Rev. Mol. Cell. Biol. 2: 578-588.
14. Kroemer, G., Dallaporta, B. and Resche-Rigon, M. (1998) The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60: 619-642.
15. Kusaka, K., Tada, Y., Shigemi, T., Sakamoto, M., Nakayashiki, H., Tosa, Y. and Mayama, S. (2004) Coordinate involvement of cysteine protease and nuclease in the executive phase of plant apoptosis. FEBS Lett. 578: 363-367.
16. Lam, E., Kato, N. and Lawton, M. (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411: 848-853.
17. Lincoln, J.E., Richael, C., Overduin, B., Smith, K., Bostock, R. and Gilchrist, D.G. (2002) Expression of the antiapoptotic baculovirus p35 gene in tomato blocks programmed cell death and provides broad-spectrum resistance to disease. Proc. Natl Acad Sci. USA 99: 15217-15221.
18. Mackey, D., Holt, BF 3rd, Wiig, A. and Dangl, J.L. (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108: 743-754.
19. Mayama, S., Bordin, A.P.A., Morikawa, T., Tanpo, H. and Kato, H. (1995) Association of avenalumin accumulation with co-segregation of victorin sensitivity and crown rust resistance in oat lines carrying the Pc-2 gene. Physiol. Mol. Plant Pathol. 46: 263-274.
20. Mayama, S., Tani, T., Midland, S.L., Sims, J.J. and Keen, N.T. (1986) The purification of victorin and its phytoalexin elicitor activity in oat leaves. Physiol. Mol. Plant Pathol. 29: 1-18.
21. Meehan, F. and Murphy, H.C. (1946) A new Helminthosporium blight of oats. Science 104: 413-414.
22. Meehan, F. and Murphy, H.C. (1947) Differential phytotoxicity of metabolic by-products of Helminthosporium victoriae. Science 106: 270-271.
23. 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.
24. Navarre, D.A. and Wolpert, T.J. (1995) Inhibition of the glycine decarboxylase multienzyme complex by the host-selective toxin victorin. Plant Cell 7: 463-471.
25. Navarre, D.A. and Wolpert, T.J. (1999) Victorin induction of an apoptosis/senescence-like response in oats. Plant Cell 11: 237-249.
26. Nurnberger, 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.
27. Pontier, D., Mittler, R. and Lam, E. (2002) Mechanism of cell death and disease resistance induction by transgenic expression of bacterio-opsin. Plant J. 30: 499-509.
28. Rines, H.W. and Luke, H.H. (1985) Selection and regeneration of toxin-insensitive plants from tissue cultures of oats (Avena sativa) susceptible to Helminthosporium victoriae. Theor. Appl. Genet. 71: 16-21.
29. 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.
30. 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 oat. Mol. Plant-Microbe Interact. 17: 245-253.
31. Ullrich, C.I. and Novacky, A.J. (1991) Electrical membrane properties of leaves, roots and single root cap cells of susceptible Avena sativa: effect of victorin C. Plant Physiol. 95: 675-681.
32. Walton, J.D. (1996) Host-selective toxins: agents of compatibility. Plant Cell 8: 1723-1733.
33. Walton, J.D. and Earle, E.D. (1985) Stimulation by victorin of extracellular polysaccharide synthesis in oat mesophyll protoplasts. Planta 165: 407-415.
34. Wheeler, H. and Black, H.S. (1962) Change in permeability induced by victorin. Science 137: 983-984.
35. 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.
36. Wolpert, T.J. and Macko, V. (1989) Specific binding of victorin to a 100-kDa protein from oats. Proc. Natl Acad. Sci. USA 86: 4092-4096.
37. Wolpert, T.J., Macko, Y., Acklin, W., Jaun, B., Seibl, J., Meili, J. and Arigoni, D. (1985) Structure of victorin C, the major host-selective toxin from Cochliobolus victoriae. Experientia 41: 1524-1529.
38. Wolpert, T.J., Navarre, D.A., Moore, D.L. and Macko, V. (1994) Identification of the 100-kD victorin binding protein from oats. Plant Cell 6: 1145-1155.
39. Yang, Q., Trinh, H.X., Imai, S., Ishihara, A., Zhang, L., Nakayashiki, H., Tosa, Y and Mayama, S. (2004) Analysis of the involvement of hydroxyanthranilate hydroxycinnamoyltransferase and caffeoyl-CoA 3-O-methyltransferase in phytoalexin biosynthesis in oat. Mol. Plant-Microbe Interact. 17: 81-89.
40. Yao, N., Tada, Y., Park, P., Nakayashiki, H., Tosa, Y. and Mayama, S. (2001) Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats. Plant J. 28: 13-26.
41. Yao, N., Tada, Y., Sakamoto, M., Nakayashiki, H., Park, P., Tosa, Y. and Mayama, S. (2002) Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J. 30: 567-579.
42. Zamzami, N., Susin, S.A., Marchetti, P., Hirsch, T., Gomez-Monterrey, I., Castedo, M. and Kroemer, G. (1996) Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183: 1533-1544.