NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea

Molecular Plant-Microbe Interactions

Volumn 21, Issue 6, 2008, Pages 808-819

  Segmüller, Nadja ^a   Kokkelink, Leonie ^a   Giesbert, Sabine ^a   Odinius, Daniela ^a   Van Kan, Jan ^b   Tudzynski, Paul ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Reactive oxygen species (ROS)

Indexed keywords

CATION; DIPHENYLIODONIUM SALT; FUNGAL PROTEIN; HYDROGEN PEROXIDE; ISOENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; BIOLOGICAL MODEL; BOTRYTIS; CLASSIFICATION; CYTOLOGY; DNA SEQUENCE; DRUG EFFECT; ENZYMOLOGY; FUNGUS SPORE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LEGUME; METABOLISM; MICROBIOLOGY; MUTATION; NORTHERN BLOTTING; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; PLANT LEAF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRULENCE;

BLOTTING, NORTHERN; BLOTTING, SOUTHERN; BOTRYTIS; FABACEAE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN PEROXIDE; ISOENZYMES; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, BIOLOGICAL; MUTATION; NAD; NADPH OXIDASE; ONIUM COMPOUNDS; PHYLOGENY; PLANT LEAVES; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SPORES, FUNGAL; VIRULENCE;

BOTRYOTINIA FUCKELIANA; FUNGI; MAMMALIA;

EID: 41049116116     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-21-6-0808     Document Type: Article

References (53)

1. Aguirre, J., Rios-Momberg, M., Hweitt, D., and Hansberg, W. 2005. Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 13:111-118.
2. Arnold, R. S., Shi, J., Murad, E., Whalen, A. M., Sun, C. Q., Polavarapu, R., Parthasarathy, S., Petros, J. A., and Lambeth, J. D. 2001. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc. Natl. Acad. Sci., U.S.A. 98:5550-5555.
3. Babior, B. M. 1992. The respiratory burst oxidase. Adv. Enzymol. Relat. Areas Mol. Biol. 65:49-95.
4. Baker, C. J., and Orlandi, E. W. 1995. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33:299-321.
5. Bedard, K., and Krause, K.-H. 2007. Nox family NADPH oxidases: Not just in mammals. Physiol. Rev. 87:245-313.
6. Bestwick, C. S., Brown, I. R., Bennett, M. H., and Mansfield, J. W. 1997. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell 9:209-221.
7. Briggs, R. T., Drath, D. B., Karnovsky, M. L., and Karnovski, M. J. 1975. Localization of NADH oxidase on the surface of human polymorphonuclear leukocytes by a new cytochemical method. J. Cell Biol. 67:566-586.
8. Cenis, J. L. 1992. Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Res. 20:2380.
9. Cross, A. R., and Jones, O. T. G. 1991. Enzyme mechanisms of superoxide production. Biochim. Biophys. Acta 1057:281-298.
10. Dinauer, M. 1993. The respiratory burst oxidase and the molecular genetics of chronic granulomatous disease. Crit. Rev. Clin. Lab. Sci. 30:329-369.
11. Doehlemann, G., Molitor, F., and Hahn, M. 2005. Molecular and functional characterization of a fructose specific transporter from the gray mold fungus Botrytis cinerea. Fungal Gen. Biol. 42:601-610.
12. Doehlemann, G., Berndt, B. and Hahn, M. 2006. Different signalling pathways involving a Gα protein, cAMP and a MAP kinase control germination in Botrytis cinerea conidia. Mol. Microbiol. 59:821-835.
13. Egan, M. J., Wang, Z.-Y., Jones, M. A., Smirnoff, N., and Talbot, J. T. 2007. Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc. Natl. Acad. Sci. U.S.A. 104:11772-11777.
14. Finkel, T. 2003 Oxidant signals and oxidative stress. Curr. Opin. Cell Biol. 15:247-254.
15. Foremanm, J., Demidchik, V., Bothwell, J. H. F., Mylona, P., Miedema, H., Torres, M. A., Linstead, P., Costa, S., Brownlee, C., Jones, J. D. G., Davies, J. M., and Dolan, L. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-446.
16. Geiszt, M., Kopp, J. B., Varnai, P., and Leto, T. L. 2000. Identification of renox, an NAD(P)H oxidase in kidney. Proc. Natl. Acad. Sci. U.S.A. 97:8010-8014.
17. Giesbert, S., Schürg, T., Scheele, S., and Tudzynski, P. The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps purpurea. Mol. Plant Pathol. In press.
18. Govrin, E. M., and Levine, A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10:751-757.
19. Herve, C., Tonon, T., Cooen, J., Borre, E., and Boyen, C. 2006. NADPH oxidases in Eukaryotes: Red algae provide new hints! Curr. Genet. 49:190-204.
20. Klimpel, A., Schulze 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.
21. Kwak, J. M., Mori, I. C., Pei, Z.-M., Leonhardt, N., Torres, M. A., Dangl, J. L., Bloom, R. E., Bodde, S., Jones, J. D. G., and Schroeder, J. I. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO (Eur. Mol. Biol. Organ.) J. 22:2623-2633.
22. Lamb, C., and Dixon, R. A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251-275.
23. Lambeth, J. D. 2004. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4:181-189.
24. Lara-Ortiz, T., Riveros-Rosas, H., and Aguirre, J. 2003. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulated sexual development in Aspergillus nidulans. Mol. Microbiol. 50:1241-1255.
25. Lyon, G. D., Goodman, B. A., and Williamson, B. 2004. Botrytis cinerea perturbs redox processes as an attack strategy in plants. Pages 119-141 in: Botrytis: Biology, Pathology and Control. Y. Elad, B. Williamson, P. Tudzynski, and N. Delen, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
26. Malagnac, F., Laluque, H., Lepere, G., and Silar, P. 2004. Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Gen. Biol. 41:982-997.
27. Parkos, C. A., Allen, R. A., Cochrane, C. G., and Jesiatis, A. J. 1988. The quaternary structure of the plasma membrane b-type cytochrome of human granulocytes. Biochim. Biophys. Acta 932:71-83.
28. Pontecorvo, G. V., Roper, J. A., Hummonns, L. M., MacDonald, K. D., and Buften, A. W. J. 1953. The genetics of Aspergillus nidulans. Adv. Genet. 141:141-238.
29. Quidde, T., Büttner, P., and Tudzynski, P. 1999. Evidence for three different specific saponin-detoxyfying activities in Botrytis cinerea and cloning and functional analysis of a gene coding for a putative avenacinase. Eur. J. Plant Pathol. 105:273-283.
30. 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.
31. Rui, O., and Hahn, M. 2007. The Slt2-type MAP kinase Bmp3 of Botrytis cinerea is required for normal saprotrophic growth, conidiation, plant surface sensing and host tissue colonization. Mol. Plant Pathol. 8:173-184.
32. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
33. Schulze Gronover, C., Kasulke, D., Tudzynski, P., and Tudzynski, B. 2001. The role of G protein alpha subunits in the infection process of the grey mould fungus Botrytis cinerea. Mol. Plant-Microbe Interact. 14:1293-1302.
34. Segal, A. W. 2005. How neutrophils kill microbes. Annu. Rev. Immunol. 23:197-223.
35. Segmüller, N., Ellendorf, U., Tudzynski, B., and Tudzynski, P. 2007. BcSAK1, a stress-activated mitogen-activated protein kinase is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot. Cell 6:211-221.
36. Shinogi, T., Suzuki T., Kurihara, T., Narusake, Y., and Park, P. 2003. Microscopic detection of reactive oxygen species generation in the compatible and incompatible interactions of Alternaria alternata Japanese pear pathotype and host plants. J. Gen. Plant Pathol. 69:7-16.
37. Siewers, V., Viaud, M., Jimez-Teja, D., Collado, I. G., Schulze Gronover, C., Pradier, J.-M., Tudzynski, B., and Tudzynski, P. 2005. Functional analysis of the cytochrome P450 monooxygenase gene bcbot1 of Botrytis cinerea indicates that botrydial is a strain-specific virulence factor. Mol. Plant-Microbe Interact. 18:602-612.
38. Spurr, A. R. 1969. A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26:31-43.
39. Suh, Y. A., Arnold, R. S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., Chiung, A. B., Griendling, K. K., and Lambeth, J. D. 1999. Cell transformation by the superoxide-generating oxidase Mox1. Nature 401:79-82.
40. Takemoto, D., Tanaka, A., and Scott, B. 2006. A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18:2807-2821.
41. Takemoto, P., Tanaka, and A., Scott, B. 2007. NADPH oxidases in fungi: Diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet. Biol. 44:1065-1076.
42. Tanaka, A., Christensen, M. J., Takemoto, D., Park, P., and Scott, B. 2006. Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18:1052-1066.
43. 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.
44. 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.
45. Torres, M. A., Jones, J. D. G., and Dangl, J. L. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373-378.
46. van der Vlugt-Bergmans, C. J. B., Brandwagt, B. F., Van't Klooster, J. W., Wagemakers, C. A. M., and Van Kan, J. A. L. 1993. Genetic variation and segregation of DNA polymorphisms in Botrytis cinerea. Mycol. Res. 97:1193-1200.
47. Veenhuis, M., van Dijken, J. P., and Harder, W. 1976. Cytochemical studies on localization of methanol oxidase and other oxidases in peroxisomes of methanol-grown Hansenula polymorpha. Arch. Microbiol. 111:123-135.
48. 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. Mol. Plant Pathol. 50:151-166.
49. Wientjes, F. B., and Segal, A. W. 1995. NADPH oxidase and the respiratory burst. Semin. Cell Biol. 6:357-365.
50. Williamson, B, Tudzynski, B., Tudzynski, P., and vanKan, J. A. L. 2007. Botrytis cinerea: The cause of grey mould disease. Mol. Plant Pathol. 8:561-580.
51. Wojtaszek, P. 1997. Oxidative burst: An early plant response to pathogen infection. Biochem. J. 322 (Pt. 3):681-692.
52. Zheng, L., Campbell, M., Murphy, J., Lam, S., and Xu, J.-R. 2000. The BMP1 gene is essential for pathogenicity in the gray mold fungus Botrytis cinerea. Mol. Plant-Microbe Interact. 13:724-732.
53. Broad Institute's Botrytis cinerea database: www.broad.mit.edu/ annotation/genome/botrytis _cinerea/Home.html