Functional analysis of H2O2-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

Molecular Plant Pathology

Volumn 5, Issue 1, 2004, Pages 17-27

  Rolke, Yvonne ^a   Liu, Songji ^a   Quidde, Thomas ^a   Williamson, Brian ^b   Schouten, Alexander ^c   Weltring, Klaus Michael ^a   Siewers, Verena ^a   Tenberge, Klaus B ^a   Tudzynski, Bettina ^a   Tudzynski, Paul ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BOTRYOTINIA FUCKELIANA; BOTRYTIS; EMBRYOPHYTA; FUNGI; PHASEOLUS (ANGIOSPERM); PHASEOLUS VULGARIS;

EID: 0842302365     PISSN: 14646722     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2004.00201.x     Document Type: Article

References (43)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Beauchamp, C. and Fridovich, I. (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44, 276-287.
3. Cenis, J.L. (1992) Rapid extraction of fungal DNA for PCR amplification. Nucl. Acids Res. 20, 2380.
4. Chary, P., Dillon, D., Schroeder, A.L. and Natvig, D.O. (1994) Superoxide dismutase (sod1) null mutants of Neurospora crassa: oxidative stress sensitivity, spontaneous mutation rate and response to mutagens. Genetics, 137, 723-730.
5. Colmenares, A.J., Aleu, J., Duran-Patron, R., Collado, I.G. and Hernandez-Galan, R. (2002) The putative role of botrydial and related metabolites in the infection mechanism of Botrytis cinerea. J. Chem. Ecol. 28, 997-1005.
6. Deighton, N., Muckenschnabel, I., Colmenares, A.J., Collado, I.G. and Williamson, B. (2001) Botrydial is produced in plant tissues infected by Botrytis cinerea. Phytochem. 57, 689-692.
7. Deighton, N., Muckenschnabel, I., Goodman, B.A. and Williamson, B. (1999) Lipid peroxidation and the oxidative burst associated with infection of Capsicum annuum by Botrytis cinerea. The Plant J. 20, 485-492.
8. Edlich, W., Lorenz, G., Lyr, H., Nega, E. and Pommer, E.H. (1989) New aspects in the infection mechanism of Botrytis cinerea. Neth. J. Plant Pathol. 95(Suppl.1), 53-62.
9. Frederick, K.R., Tung, J., Emerick, R.S., Masiarz, F.R., Chamberlain, S.H., Vasavada, A., Rosenberg, S., Chakroborty, S., Schopter, L.M. and Massey, V. (1990) Glucose oxidase from Aspergillus niger. J. Biol. Chem. 265, 3793-3802.
10. Garre, V., Müller, U. and Tudzynski, P. (1998) Cloning, characterization and targeted disruption of cpcatl, coding for an in planta secreted catalase of Claviceps purpurea. Mol. Plant-Microbe Interact. 11, 772-783.
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. Halliwell, B. and Gutteridge, J.M.C. (1989) Free Radicals in Biology and Medicine. Oxford, UK: Clarendon Press.
13. Hamilton, A.J., Holdom, M.D. and Jeavons, L. (1996) Expression of the Cu,Zn superoxide dismutases of Aspergillus fumigatus as determined by immunochemistry and immunoelectron microscopy. FEMS Immun. Med. Microbiol. 14, 95-102.
14. Hatzinikolaou, D.G., Hansen, O.C., Macris, B.J., Tingey, A., Kekos, K., Goodenough, P. and Stougaard, P. (1996) A new glucose oxidase from Aspergillus niger: characterization and regulation studies of enzyme and gene. Appl. Microbiol. Biotechnol. 46, 371-381.
15. ten Have, A., Mulder, W., Visser, J. and van Kan, J.A.L. (1998) The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol. Plant-Microbe Interact. 11, 1009-1016.
16. van Heijne, G. (1990) The signal peptide. J. Membrane Biol. 115, 195-200.
17. Kiess, M., Hecht, H.J. and Kalisz, H.M. (1998) Glucose oxidase from Penicillium amagasakiense primary structure and comparison with other glucose-methanol-choline (GMC) oxidoreductases. Eur. J. Biochem. 252, 90-99.
18. Klimpel, A., Schluze Gronover, C., Williamson, B., Stewart, J.A. and Tudzynski, B. (2002) The adenylate cyclase (BAC) in Botrytis cinerea is required for full pathogenicity. Mol. Plant Pathol. 3, 439-450.
19. Lara-Ortiz, T., Riveros-Rosas, H. and Aguirre, J. (2003) Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Molec. Microbiol. 50, 1247-1255.
20. Liu, S., Oeljeklaus, S., Gerhardt, B. and Tudzynski, B. (1998) Purification and characterization of glucose oxidase of Botrytis cinerea. Physiol. Mol. Plant Pathol. 53, 123-132.
21. Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R. (1951) Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265.
22. Mey, G., Oeser, B., Lebrun, M.H. and Tudzynski, P. (2002) The biotrophic, non-appressoria forming grass pathogen Claviceps purpurea needs a Fus3/Pmk1 homologous MAP kinase for colonization of rye ovarian tissue. Mol. Plant Microbe-Interact. 15, 303-312.
23. Moore, S., de Vries, O.M.H. and Tudzynski, P. (2002) The major Cu, Zn SOD of the phytopathogen Claviceps purpurea is not essential for pathogenicity. Molec. Plant Pathol. 3, 9-22.
24. Muckenschnabel, I., Goodman, B.A., Deighton, N., Lyon, G.D. and Williamson, B. (2001b) Botrytis cinerea induces the formation of free radicals in fruits of Capsicum annuum at positions remote from the site of infection. Protoplasma, 218, 112-116.
25. Muckenschnabel, I., Goodman, B.A., Williamson, B. and Lyon, G.D. and Deighton, N. (2002) Infection of leaves of Arabidopsis thaliana by Botrytis cinerea: changes in ascorbic acid, free radicals and lipid peroxidation products. J. Exp. Bot. 53, 207-214.
26. Muckenschnabel, I., Schulze Gronover, C., Deighton, N., Goodman, B.A., Lyon, G.D., Stewart, D. and Williamson, B. (2003) Oxidative effects in uninfected tissue in leaves of French bean (Phaseolus vulgaris) containing soft rots caused by Botrytis cinerea. J. Sci. Food Agric. 83, 507-514.
27. Muckenschnabel, I., Williamson, B., Goodman, B.A., Lyon, G.D., Stewart, D. and Deighton, N. (2001a) Markers for oxidative stress associated with soft rots in French beans (Phaseolus vulgaris) infected by Botrytis cinerea. Planta, 212, 376-381.
28. Murray, F.R., Llewellyn, D.J., Peacock, W.J. and Dennis, E.S. (1997) Isolation of the glucose oxidase gene from Talaromyces flavus and characterisation of its role in the biocontrol of Verticillium dahliae. Curr. Genet. 32, 367-375.
29. Nathues, E., Joshi, S., Tenberge, K.T., von den Driesch, M., Oeser, B., Bäumer, N., Mihlan, M. and Tudzynski, P. (2004) CPTF1, a CREB-like transciption factor is involved in the oxidative stress response in the phytopathogen Claviceps purpurea and modulates ROS level in its host Secale cereale. Mol. Plant Microbe-Interact., in press.
30. Pontecorvo, G.V., Roper, J.A., Hemmonns, L.M., MacDonald, K.D. and Buften, A.W.J. (1953) The genetics of Aspergillus nidulans. Adv. Genet. 141, 141-238.
31. Prins, T.W., Wagemakers, L., Schouten, A. and van Kan, J.A.L. (2000) Cloning and characterization of a glutathione S-transferase homologoue from the plant pathogenic fungus Botrytis cinerea. Mol. Plant Pathol. 1, 169-178.
32. Quidde, T., Büttner, P. and Tudzynski, P. (1999) Evidence for three different specific saponin-detoxifying activities in Botrytis cinerea and cloning and functional analysis of a gene coding for a putative avenacinase. Eur. J. Plant Pathol. 105, 273-283.
33. Robertson, E.F., Dannelly, H.K., Malloy, P.J. and Reeves, H.C. (1987) Rapid isoelectric focusing in a vertical polyacrylamide minigel system. Anal. Biochem. 167, 290-294.
34. Saiki, R.K., Gelfand, D.H., Stoffel, S., Scharf, S.J., Higuchi, R., Horn, G.T., Mullis, K.B. and Erlich, H.A. (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science, 239, 487-491.
35. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring. Harbor Laboratory Press.
36. Schouten, A., Tenberge, K.B., Vermeer, J., Stewart, J., Wagemakers, L., Williamson, B. and van Kan, J.A.L. (2002) Functional analysis of an extracellular catalase of Botrytis cinerea. Mol. Plant Pathol. 3, 227-238.
37. Schüller, C., Brewster, J.L., Alexander, M.R., Gustin, M.C. and Ruis, H. (1994) The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of Saccharomyces cerevisiae CTT1 gene. EMBO J. 13, 4382-4389.
38. Schulze Gronover, C., Kasulke, D., Tudzynski, P. and Tudzynski, B. (2001) The role of G protein alpha subunits in the infection process of the gray mould fungus Botrytis cinerea. Mol. Plant-Microbe Interact. 14, 1293-1302.
39. Tenberge, K.B., Beckedorf, M., Hoppe, B., Schouten, A., Solf, M. and von den Driesch, M. (2002) In situ localization of AOS in host-pathogen interactions. Microsc. Microanal. 8(Suppl. 2), 250-251.
40. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22, 4673-4680.
41. von Tiedemann, A. (1997) Evidence for a primary role of active oxygen species in induction of host cell death during infection of bean leaves with Botrytis cinerea. Physiol. Molec. Plant Pathol. 50, 151-166.
42. van der Vlugt-Bergmans, C.J.B., Wagemakers, C.A.M., Dees, D.C.T. and van Kan, J.A.L. (1997) Catalase A from Botrytis cinerea is not expressed during infection on tomato leaves. Physiol. Mol. Plant Pathol. 50, 1-15.
43. Yannish-Perron, C., Vieria, J. and Messing, J. (1985) Improved M13 phage cloning vectors and host strain: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene, 33, 103-109.