Identification and characterization of Sclerotinia sclerotiorum NADPH oxidases

Applied and Environmental Microbiology

Volumn 77, Issue 21, 2011, Pages 7721-7729

  Kim, Hyo jin ^a   Chen, Changbin ^b   Kabbage, Mehdi ^a   Dickman, Martin ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENEFICIAL EFFECTS; FUNGAL PATHOGEN; GENOME SEQUENCES; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; S. SCLEROTIORUM; SCLEROTINIA SCLEROTIORUM;

ANIMALS; GENE EXPRESSION; RNA;

PLANTS (BOTANY);

OXALIC ACID DERIVATIVE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL; ECONOMIC ANALYSIS; ENZYME ACTIVITY; FUNGAL DISEASE; FUNGUS; GENE EXPRESSION; HOST-PARASITE INTERACTION; IDENTIFICATION METHOD; OXYGEN; PATHOGENICITY; PLANT; SIGNALING; VIRULENCE;

ARTICLE; ASCOMYCETES; DRUG ANTAGONISM; ENZYMOLOGY; FUNGUS HYPHAE; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; PLANT LEAF; RNA INTERFERENCE; TOMATO; VIRULENCE;

ASCOMYCOTA; GENE SILENCING; HYPHAE; LYCOPERSICON ESCULENTUM; NADPH OXIDASE; OXALATES; PLANT DISEASES; PLANT LEAVES; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; VIRULENCE;

EID: 83155190983     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.05472-11     Document Type: Article

References (43)

1. Balmforth, A. J., and A. Thomson. 1984. Isolation and characterization of glyoxylate dehydrogenase from the fungus Sclerotium rolfsii. Biochem. J. 218:113-118.
2. Bateman, D. F., and S. V. Beer. 1965. Simultaneous production and synergistic action of oxalic acid and polygalacturonase during pathogenesis by Sclerotium rolfsii. Phytopathology 55:204-211.
3. Cano-Domínguez, N., K. Alvarez-Delfin, W. Hansberg, and J. Aguirre. 2008. NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot. Cell 7:1352-1361.
4. Cessna, S. G., V. E. Sears, M. B. Dickman, and P. S. Low. 2000. Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell 12:2191-2200.
5. Dickman, M. B., and A. Mitra. 1992. Arabidopsis thaliana as a model for studying Sclerotinia sclerotiorum pathogenesis. Physiol. Mol. Plant Pathol. 41:255-263.
6. Dickman, M. B. 2007. Approaches for crop improvement to soilborne fungal diseases through biotechnology: Sclerotinia sclerotiorum as a case study. Australas. Plant Pathol. 36:116-123.
7. Dutton, M. V., and C. S. Evans. 1996. Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Can. J. Microbiol. 42:881-895.
8. Egan, M. J., J. Y. Wang, M. A. Jones, N. Smirnoff, and N. J. Talbot. 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.
9. Escutia, M. R., et al. 2005. Cloning and sequencing of two Ceriporiopsis subvermispora bicupin oxalate oxidase allelic isoforms: implications for the reaction specificity of oxalate oxidases and decarboxylases. Appl. Environ. Microbiol. 71:3608-3616.
10. Foreman, J., et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-446.
11. Georgiou, C. D., N. Patsoukis, I. Papapostolou, and G. Zervoudakis. 2006. Sclerotial metamorphosis in filamentous fungi is induced by oxidative stress. Integr. Comp. Biol. 46:691-712.
12. Giesbert, S., T. Schürg, S. Scheele, and P. Tudzynski. 2008. The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps pupurea. Mol. Plant Pathol. 9:317-327.
13. Godoy, G., J. R. Steadman, M. B. Dickman, and R. Dam. 1990. Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiol. Mol. Plant Pathol. 37:179-191.
14. 2 recycling during oxidation of the arylglycerol-β-aryl ether lignin structure by lignin peroxidase and glyoxal oxidase. Biochemistry 33:13349-13354.
15. Hansberg, W., H. de Groot, and H. Sies. 1993. Reactive oxygen species associated with cell differentiation in Neurospora crassa. Free Radic. Biol. Med. 14:287-293.
16. Hegedus, D. D., and S. R. Rimmer. 2005. Sclerotinia sclerotiorum: when "to be or not to be" a pathogen? FEMS Microbiol. Lett. 251:177-184.
17. Kim, J. H., et al. 2008. Elucidation of the functional genomics of antioxidantbased inhibition of aflatoxin biosynthesis. Int. J. Food Microbiol. 122:49-60.
18. Kim, K. S., J. Y. Min, and M. B. Dickman. 2008. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol. Plant Microbe Interact. 21:605-612.
19. Kubicek, C. P., G. Schreferl-Kunar, W. Wöhrer, and M. Röhr. 1988. Evidence for a cytoplasmic pathway of oxalate biosynthesis in Aspergillus niger. Appl. Environ. Microbiol. 54:633-637.
20. Kwak, J. M., et al. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22: 2623-2633.
21. Lalucque, H., and P. Silar. 2003. NADPH oxidase: an enzyme for multicellularity? Trends Microbiol. 11:9-12.
22. Reference deleted
23. Lara-Ortíz, T., H. Riveros-Rosas, and J. Aguirre. 2003. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol. Microbiol. 50:1241-1255.
24. Malagnac, F., H. Lalucque, G. Lepère, and P. Silar. 2004. Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet. Biol. 41:982-997.
25. + in the regulation of intramitochondrial energy production in heart. Biomed. Biochim. Acta 46:S487-S492.
26. Nakayashiki, H., et al. 2005. RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet. Biol. 42:275-283.
27. Nauseef, W. M. 2008. Biological roles for the NOX family NADPH oxidases. J. Biol. Chem. 283:16961-16965.
28. Noyes, R. D., and J. G. Hancock. 1981. Role of oxalic acid in the Sclerotinia wilt of sunflower. Physiol. Plant Pathol. 18:123-132.
29. Reverberi, M., et al. 2008. Modulation of antioxidant defense in Aspergillus parasiticus is involved in aflatoxin biosynthesis: a role for the ApyapA gene. Eukaryot. Cell 7:988-1000.
30. Rollins, J. A., and M. B. Dickman. 1998. Increase in endogenous and exogenous cyclic AMP levels inhibits sclerotial development in Sclerotinia sclerotiorum. Appl. Environ. Microbiol. 64:2539-2544.
31. Rollins, J. A., and M. B. Dickman. 2001. pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 homolog. Appl. Environ. Microbiol. 67:75-81.
32. Rollins, J. A. 2003. The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol. Plant Microbe Interact. 16:785-795.
33. Scott, B., and C. J. Eaton. 2008. Role of reactive oxygen species in fungal cellular differentiations. Curr. Opin. Microbiol. 11:488-493.
34. Segal, A. W. 2005. How neutrophils kill microbes. Annu. Rev. Immunol. 23:197-223.
35. Segmüller, N., et al. 2008. NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol. Plant Microbe Interact. 21:808-819.
36. Reference deleted
37. Takemoto, D., A. Tanaka, and B. Scott. 2006. A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18:2807-2821.
38. Tanaka, A., M. J. Christensen, D. Takemoto, P. Park, and B. Scott. 2006. Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic association. Plant Cell 18:1052-1066.
39. Thines, E., R. W. Weber, and N. J. Talbot. 2000. MAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell 12:1703-1718.
40. phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen species intermediates in the plant defense response. Proc. Natl. Acad. Sci. U. S. A. 99:517-522.
41. Torres, M. A., J. D. G. Jones, and J. L. Dangl. 2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 37:1130-1134.
42. Williams, B., M. Kabbage, H. J. Kim, R. Britt, and M. B. Dickman. 2011. Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog. 7:e1002107.
43. Yajima, W., and N. N. V. Kav. 2006. The proteome of the phytopathogenic fungus Sclerotinia sclerotiorum. Proteomics 6:5995-6007.