Molecular characterization of the NADPH oxidase complex in the ergot fungus claviceps purpurea: CpNox2 and CpPls1 are important for a balanced host-pathogen interaction

Molecular Plant-Microbe Interactions

Volumn 26, Issue 10, 2013, Pages 1151-1164

  Schürmann, Janine ^a   Buttermann, Dagmar ^a   Herrmann, Andrea ^a   Giesbert, Sabine ^a   Tudzynski, Paul ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; GUANOSINE TRIPHOSPHATASE; HYBRID PROTEIN; MULTIENZYME COMPLEX; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TETRASPANIN;

ARTICLE; CLAVICEPS; CYTOLOGY; DNA SEQUENCE; FLOWER; FLUORESCENCE MICROSCOPY; FUNGUS HYPHAE; FUNGUS SPORE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; PATHOGENICITY; PLANT DISEASE; POACEAE; TWO HYBRID SYSTEM;

CLAVICEPS; FLOWERS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GTP PHOSPHOHYDROLASES; HOST-PATHOGEN INTERACTIONS; HYPHAE; MICROSCOPY, FLUORESCENCE; MULTIENZYME COMPLEXES; NADPH OXIDASE; OXIDATIVE STRESS; PLANT DISEASES; POACEAE; REACTIVE OXYGEN SPECIES; RECOMBINANT FUSION PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION; SPORES, FUNGAL; TETRASPANINS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84884796656     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-03-13-0064-R     Document Type: Article

References (79)

1. Aguirre, J., Ríos-Momberg, M., Hewitt, D., and Hansberg, W. 2005. Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 13:111-118.
2. Alderman, S. C. 2003. Diversity and speciation in Claviceps. Pages 195-24 in: Clavicipitalean Fungi: Evolutionary Biology, Chemistry, Biocontrol and Cultural Impacts. Mycology 19. J. F. White, C. W. Bacon, N. L. Hywel-Jones, and J. W. Spatafora, eds. Marcel Dekker, New York.
3. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 24:3389-3402.
4. Ambasta, R. K., Kumar, P., Griendling, K. K., Schmidt, H. H., Busse, R., and Brandes, R. P. 2004. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J. Biol. Chem. 279:45935-45941.
5. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidmann, J. G., Smith, J. A., and Struhl, K. 1987. Current Protocols in Molecular Biology. John Wiley and Sons, New York.
6. Bertani, G. 1951. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62:293-300.
7. Bretscher, M. S., and Munro, S. 1993. Cholesterol and the golgi-apparatus. Science 261:1280-1281.
8. Brockmann, B., Smit, R., and Tudzynski, P. 1992. Characterization of an extracellular ?-1,3-glucanase of Claviceps purpurea. Physiol. Mol. Plant Pathol. 40:191-201.
9. Cano-Dominguez, N., Alvarez-Delfín, K., Hansberg, W., and Aguirre, J. 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.
10. Cardenas, M. E., Hemenway, C., Muir, R. S., Ye, R., Fiorentino, D., and Heitman, J. 1994. Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands. EMBO (Eur. Mol. Biol. Organ.) J. 13:5944-5957.
11. Cenis, J. L. 1992. Rapid extraction of fungal DNA for PCR amplification. Nucleic Acid Res. 20:2380.
12. Chenevert, J., Corrado, K., Bender A., Pringle, J., and Herskowitz, I. 1992. A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains. Nature 356:77-79.
13. Chin, C.F., Bennett, A. M., Ma, W. K., Hall, M. C., and Yeong F. M. 2012. Dependence of Chs2 ER export on dephosphorylation by cytoplasmic Cdc14 ensures that septum formation follows mitosis. Mol. Biol. Cell 23:45-58.
14. Christianson, T. W., Sikorski, R. S., Dante, M., Shero, J. H., and Hieter, P. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110:119-122.
15. Clergeot, P. H., Gourgues, M., Cots, J., Laurans, F., Latorse, M. P., Pepin, R., Tharreau, D., Notteghem, J. L., and Lebrun, M. H. 2001. PLS1, a gene encoding a tetraspanin-like protein, is required for penetration of rice leaf by the fungal pathogen Magnaporthe grisea. Proc. Natl. Acad. Sci. U.S.A. 98:6963-6968.
16. Colot, H. V., Park, G., Turner, G. E., Ringelberg, C., Crew, C. M., Litvinkova, L., Richard, L., Weiss, R. L., Borkovich, K. A., and Dunlap J. C. 2006. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U.S.A. 103:10352-10357.
17. Corbett, K., Dickerson, A. G., and Mantle, P. G. 1975. Metabolism of the Germinating Sclerotium of Claviceps purpurea. J. Gen. Microbiol. 90:55-68.
18. Däubner, T., Fink, A., Seitz, A., Tenzer S., Müller J., Strand, D., Seckert, C. K., Janssen, C., Renzaho, A., Grzimek, N. K. A., Simon, C. O., Ebert, S., Reddehase, M. J., Oehrlein-Karpi, S. A., and Lemmermann, N. A. W. 2010. A novel transmembrane domain mediating retention of a highly motile herpesvirus glycoprotein in the endoplasmic reticulum. J. Gen. Virol. 91:1524-1534.
19. Egan, M. J., Wang, Z. Y., Jones, M. A., Smimoff, N., and Talbot, N. J. 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.
20. Fields, S., and Song, 0. K. 1989. A novel genetic system to detect proteinprotein interactions. Nature 340:245-246.
21. Franck, B. 1969. Structure and biosynthesis of the Ergot pigments. Angew. Chem. Int. Ed. Engl. 8:251-260.
22. Georgiou, C. D., Tairis, N., and Sotiropoulou, A. 2000. Hydroxyl radical scavengers inhibit sclerotial differentiation and growth in Sclerotinia sclerotiorum and Rhizoctonia solani. Mycol. Res. 104:1191-1196.
23. Georgiou, C. D., Patsoukis, N., Papapostolou, I., and Zervoudakis, G. 2006. Sclerotial metamorphosis in filamentous fungi is induced by oxidative stress. Integr. Compar. Biol. 46:691-712.
24. Giesbert, S., Schürg, T., Scheele, S., and Tudzynski, P. 2008. The NADPH oxidase Cpnox1 is required for full pathogenicity of the Ergot fungus Claviceps purpurea. Mol. Plant Pathol. 9:317-327.
25. Gourgues, M., Brunet-Simon, A., Lebrun, M. H., and Levis, C. 2004. The tetraspanin BcPls1 is required for appressorium-mediated penetration of Botrytis cinerea into host plant leaves. Mol. Microbiol. 51:619-629.
26. Haarmann, T., Rolke, Y., Giesbert, S., and Tudzynski, P. 2009. Ergot: From witchcraft to biotechnology. Mol. Plant Pathol. 10:563-577.
27. Hansberg, W., and Aguirre, J. 1990. Hyperoxidant states cause microbial cell differentiation by cell isolation from dioxygen. J. Theor. Biol. 142:201-221.
28. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K., and Elledge, S. J. 1993. The p21 Cdk-interacting protein Cipl is a potent inhibitor of Gl cyclin-dependent kinases. Cell 75:805-816.
29. Heller, J., and Tudzynski, P. 2011. Reactive oxygen species in phytopathogenic fungi: Signaling, development, and disease. Annu. Rev. Phytopathol. 49:369-390.
30. Hemler, M. E. 2003. Tetraspanin proteins mediate cellular penetration, invasion and fusion events, and define a novel type of membrane microdomain. Annu. Rev. Cell Dev. Biol.19 397-422.
31. Hemler, M. E. 2005. Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 6:801-811.
32. Hüsgen, U., Büttner, P., Müller, U., and Tudzynski, P. 1999. Variation in karyotype and ploidy level among field isolates of Claviceps purpurea. J. Phytopathol. 147:591-597.
33. James, P., Halladay, J., and Craig, E. A. 1996. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144:1425-1436.
34. Jungehülsing, U., Arntz, C., Smit, R., and Tudzynski, P. 1994. The Claviceps purpurea glyceraldehyde-3-phosphate dehydrogenase gene: Cloning, characterization, and use for the improvement of a dominant selection system. Curr. Genet. 25:101-106.
35. Kangatharalingam, N., and Ferguson, M. W. 1984. A simple and rapid technique for fluorescence staining of fungal nuclei. Curr. Microbiol. 10:99-104.
36. Kawahara, T., and Lambeth, J. D. 2007. Molecular evolution of Phoxrelated regulatory subunits for NADPH oxidase enzymes. BMC Evol. Biol. 7:178.
37. Kim, H. J., Chen, C., Kabbage, M., and Dickman, M. B. 2011. Identification and characterization of Sclerotinia sclerotiorum NADPH oxidases. Appl. Environ. Microbiol. 77:7721-7729.
38. Kirchhoff, H. 1929. Beiträge zur Biologie und Physiologie des Mutterkornpilzes. Centralbl. Bakteriol. Parasitenk. Abt. II. 77:310-369.
39. Lambeth, J. D. 2004. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4:181-189.
40. Lambou, K., Malagnac, F., Barbisan, C., Tharreau D., Lebrun, M. H., and Silar, P. 2008. The crucial role of the Pls1 tetraspanin during ascospore germination in Podospora anserina provides an example of the convergent evolution of morphogenetic processes in fungal plant pathogens and saprobes. Eukaryot. Cell 7:1809-1818.
41. 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. Mol. Microbiol. 50:1241-1255.
42. Levy, S., and Shoham T. 2005. The tetraspanin web modulates immunesignalling complexes. Nat. Rev. Immunol. 5:136-148.
43. Luttrell, E. S. 1980. Host-parasite relationships and development of the Ergot sclerotium in Claviceps purpurea. Can. J. Bot. 58:942-958.
44. Malagnac, F., Lalucque, H., Lepère, G., and Silar, P. 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.
45. Mantle, P. G., and Nisbet, L. J. 1976. Differentiation of Claviceps purpurea in axenic culture. J. Gen. Microbiol. 93:321-334.
46. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Lu, F., Marchler, G. H., Mullokandov, M., Omelchenko, M. V., Robertson, C. L., Song, J. S., Thanki, N., Yamashita, R. A., Zhang, D., Zhang, N., Zheng, C., and Bryant, S. H. 2011. CDD: A conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 39:D225-D229.
47. Moore, S., de Vries, O. M., and Tudzynski, P. 2002. The major Cu, Zn SOD of the phytopathogen Claviceps purpurea is not essential for pathogenicity. Mol. Plant Pathol. 3:9-22.
48. Müller, U., Tenberge, K. B., Oeser, B., and Tudzynski, P. 1997. Cel1, probably encoding a cellobiohydrolase lacking the substrate binding domain, is expressed in the initial phase of Claviceps purpurea on Secale cereale. Mol. Plant-Microbe Interact. 10:268-279.
49. Petry, A., Djordjevic, T., Weitnauer, M., Kietzmann, T., Hess, J., and Görlach, A. 2006. NOX2 and NOX4 mediate proliferative response in endothelial cells. Antioxid. Redox. Signal. 8:1473-1484.
50. Rinnerthaler, M., Büttner, S., Laun, P., Heeren, G., Felder, T. K., Klinger, H., Weinberger, M., Stolze, K., Grousl, T., Hasek, J., Benada, O., Frydlova, I., Klocker, A., Simon-Nobbe, B., Jansko, B., Breitenbach-Koller, H., Eisenberg, T., Gourlay, C. W., Madeo, F., Burhans, W. C., and Breitenbach, M. 2012. Yno1p/Aim14p, a NADPH-oxidase ortholog, controls extramitochondrial reactive oxygen species generation, apoptosis, and actin cable formation in yeast. Proc. Natl. Acad. Sci. U.S.A. 109:8658-8663.
51. Rolke, Y., and Tudzynski, P. 2008. The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: Interaction and impact on polarity, development and pathogenicity. Mol. Microbiol. 68:405-423.
52. Ryder, L. S., Dagdas, Y. F., Mentlak, T. A, Kershawa, M. J., Thornton, C. R., Schuster, M., Chen, J., Wang, Z., and Talbot, N. J. 2013. NADPH oxidases regulate septin-mediated cytoskeletal remodeling during plant infection by the rice blast fungus. Proc. Natl. Acad. Sci. U.S.A. 110:3179-3184.
53. San Martín A., and Griendling, K. K. 2010. Redox control of vascular smooth muscle migration. Antioxid. Redox. Signal. 12:625-640.
54. Schardl, C., Young, C., Hesse, U., Amyotte, S. G., Andreeva, K., Calie, P. J., Fleetwood, D. J., Haws, D. C., Moore, N., Oeser, B., Panaccione, D. G. , Schweri, K. K., Voisey, C. R., Farman, M. L., Jaromczyk, J. W., Roe, B. A., O'Sullivan, D. M. , Scott, B., Tudzynski, P., An, Z., Arnaoudova, E. G., Bullock, C. T., Charlton, N. D., Chen, L., Cox, M., Dinkins, R. D., Florea, S., Glenn, A. E., Gordon, A., Güldener, U., Harris, D. R., Hollin, W., Jaromczyk, J., Johnson, R. D., Khan, A. K., Leistner E., Leuchtmann, A., Li, C., Liu, J. G., Liu, J., Liu, M., Mace, W., Machado, C., Nagabhyru, P., Pan, J., Schmid, J., Sugawara, K., Steiner, U., Takach, J. E., Tanaka, E., Webb, J. S., Wilson, E. V., Wiseman, J. L., Yoshida, R., and Zeng, Z. 2013. Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet. 9:e1003323.
55. Scheffer, J., and Tudzynski, P. 2006. In vitro pathogenicity assay for the Ergot fungus Claviceps purpurea. Mycol. Res. 110:465-470.
56. Scheffer, J., Chen, C., Heidrich, P., Dickman, M. B., and Tudzynski, P. 2005. A CDC42 homologue in C. purpurea is involved in vegetative differentiation and is essential for pathogenicity. Eukaryot. Cell 4:1228-1238.
57. Schumacher, J. 2012. Tools for Botrytis cinerea: New expression vectors make the gray mold fungus more accessible to cell biology approaches. Fungal Genet. Biol. 49:483-497.
58. Schürg, T., Brandt, U., Adis, C., and Fleissner, A. 2012. The Saccharomyces cerevisiae BEM1 homologue in Neurospora crassa promotes coordinated cell behaviour resulting in cell fusion. Mol. Microbiol. 86:349-66.
59. Schürmann, J., and Tudzynski, P. Claviceps: The ergot fungus. In: Molecular Biology of Food and Water Borne Mycotoxigenic and Mycotic Fungi of Humans. R. Russell and M. Paterson, eds. CRC Press, Boca Raton, FL, U.S.A. In press.
60. Segmüller, N., Kokkelink, L., Giesbert, S., Odinius, D., van Kan, J., and Tudzynski, P. 2008. NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol. Plant-Microbe Interact. 21:808-819.
61. Shaw, B. I., and Mantle, P. G. 1980. Host infection by Claviceps purpurea. Trans. Br. Mycol. Soc. 75:77-90.
62. Siegmund, U., Heller, J., van Kan, J., and Tudzynski, P. 2013. The NADPH oxidase complexes in Botrytis cinerea: Evidence for a close association with the ER and the tetraspanin Pls1. PLoS One 8:e55879.
63. Smit, R., and Tudzynski, P. 1992. Efficient transformation of Claviceps purpurea using pyrimidine auxotrophic mutants: Cloning of the OMP decarboxylase gene. Mol. Gen. Genet. 234:297-305.
64. Sonnhammer, E. L. L., von Heijne, G., and Krogh, A. 1998. A hidden Markov model for predicting transmembrane helices in protein sequences. Pages 175-182 in: Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology. J. Glasgow, T. Littlejohn, F. Major, R. Lathrop, D. Sankoff, and C. Sensen, eds. AAAI Press, Menlo Park, CA, U.S.A.
65. Sumimoto, H., Kamakura, S., and Ito, T. 2007. Structure and function of the PB1 domain, a protein interaction module conserved in animals, fungi, amoebas, and plants. Sci. STKE. 10.1126/stke.4012007re6.
66. Taber, W. A. 1985. Biology of Claviceps. Pages 449-486 in: Biotechnology Series, Vol. 6. Biology of Industrial Microorganisms. A. L. Demain and A. S. Nadine, eds. The Benjamin Cummings Publishing Co., Inc., New York.
67. 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.
68. Takemoto, D., Tanaka, A., and Scott, B. 2007. NADPH oxidases in fungi: Diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet. Biol. 44:1065-1076.
69. Takemoto, D., Kamakura, S., Saikia, S., Becker, Y., Wrenn, R., Tanaka, A., Sumimoto, H., and Scott, B. 2011. Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex. Proc. Natl. Acad. Sci. U.S.A. 108:2861-2866.
70. 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.
71. Tenberge, K. B., Homann, V., Oeser, B., and Tudzynski, P. 1996. Structure and expression of two polygalacturonase genes of Claviceps purpurea oriented in tandem: Cytological evidence for pectinolytic enzyme activity during infection of rye. Phytopathology 86:1084-1097.
72. Thines, E., Weber, R. W. S., and Talbot, N. J. 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.
73. Tu, L., Sun, T. T., and Kreibich, G. 2002. Specific heterodimer formation is a prerequisite for uroplakins to exit from the endoplasmic reticulum. Mol. Biol. Cell 13:4221-4230.
74. Tudzynski, P., Heller J., and Siegmund U., 2012. Reactive oxygen species generation in fungal development and pathogenesis. Curr. Opin. Microbiol. 15:653-659.
75. Veneault-Fourrey, C., Parisot, D., Gourgoues, M., Laugé, R., Lebrun, M. H., and Langin, T. 2005. The tetraspanin gene CIPLS1 is essential for appressorium-mediated penetration of the fungal pathogen Colletotrichum lindemuthianum. Fungal Genet. Biol. 42:306-318.
76. Winston, F., Dollard, C., and Ricupero-Hovasse, S. L. 1995. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11:53-55.
77. Woods, R. A., and Gietz, R. D. 2001. High-efficiency transformation of plasmid DNA into yeast. Methods Mol. Biol. 177:85-97.
78. Wu, R. F., Ma, Z., Liu, Z., and Terada, L. S. 2010. Nox4-derived H2O2 mediates endoplasmatic reticulum signaling through local Ras activation. Mol. Cell. Biol. 30:3553-3568.
79. Zhang, L., Nguyen, M. V., Lardy, B., Jesaitis, A.J., Grichine, A., Rousset, F., Talbot, M., Paclet, M., Qian, G., and Morel, F. 2011. New insight into the Nox4 subcellular localization in HEK293 cells: First monoclonal antibodies against Nox4. Biochimie 93:457-468.