MoSwi6, an APSES family transcription factor, interacts with MoMps1 and is required for hyphal and conidial morphogenesis, appressorial function and pathogenicity of Magnaporthe oryzae

Molecular Plant Pathology

Volumn 13, Issue 7, 2012, Pages 677-689

  Qi, Zhongqiang ^a   Wang, Qi ^a   Dou, Xianying ^a   Wang, Wei ^a   Zhao, Qian ^a   Lv, Ruili ^a   Zhang, Haifeng ^a   Zheng, Xiaobo ^a   Wang, Ping ^b   Zhang, Zhengguang ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; FUNGAL PROTEIN; HYDROGEN PEROXIDE; LACCASE; MELANIN; TRANSCRIPTION FACTOR;

ADAPTATION; ARTICLE; BIOSYNTHESIS; CELL WALL; CYTOLOGY; DRUG EFFECT; FUNGUS HYPHAE; FUNGUS SPORE; GENE DELETION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAGNAPORTHE; METABOLISM; MICROBIOLOGY; MORPHOGENESIS; MUTATION; PATHOGENICITY; PHYSIOLOGICAL STRESS; PROTEIN BINDING; RICE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; CELL WALL; CHITIN; FUNGAL PROTEINS; GENE DELETION; GENETIC COMPLEMENTATION TEST; HYDROGEN PEROXIDE; HYPHAE; LACCASE; MAGNAPORTHE; MAP KINASE SIGNALING SYSTEM; MELANINS; MORPHOGENESIS; MUTATION; ORYZA SATIVA; PROTEIN BINDING; SEQUENCE ANALYSIS, PROTEIN; SPORES, FUNGAL; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

MAGNAPORTHE; MAGNAPORTHE ORYZAE; SACCHAROMYCES CEREVISIAE;

EID: 84861695808     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2011.00779.x     Document Type: Article

References (59)

1. Aramayo, R., Peleg, Y., Addison, R. and Metzenberg, R. (1996) Asm-1+, a Neurospora crassa gene related to transcriptional regulators of fungal development. Genetics, 144, 991-1003.
2. Borneman, A.R., Hynes, M.J. and Andrianopoulos, A. (2002) A basic helix-loop-helix protein with similarity to the fungal morphological regulators, Phd1p, Efg1p and StuA, controls conidiation but not dimorphic growth in Penicillium marneffei. Mol. Microbiol. 44, 621-631.
3. Bourett, T.M., Sweigard, J.A., Czymmek, K.J., Carroll, A. and Howard, R.J. (2002) Reef coral fluorescent proteins for visualizing fungal pathogens. Fungal Genet. Biol. 37, 211-220.
4. Bruno, K.S., Tenjo, F., Li, L., Hamer, J.E. and Xu, J.R. (2004) Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot. Cell, 3, 1525-1532.
5. Caracuel-Rios, Z. and Talbot, N.J. (2007) Cellular differentiation and host invasion by the rice blast fungus Magnaporthe grisea. Curr. Opin. Microbiol. 10, 339-345.
6. Chi, M.H., Park, S.Y., Kim, S. and Lee, Y.H. (2009) A novel pathogenicity gene is required in the rice blast fungus to suppress the basal defenses of the host. PLoS Pathog. 5, e1000401.
7. Cid, V.J., Durán, A., del Rey, F., Snyder, M.P., Nombela, C. and Sánchez, M. (1995) Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae. Microbiol. Rev. 59, 345-386.
8. 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. USA, 98, 6963-6968.
9. D'Souza, C.A. and Heitman, J. (2001) Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol. Rev. 25, 349-364.
10. Doedt, T., Krishnamurthy, S., Bockmuhl, D.P., Tebarth, B., Stempel, C., Russell, C.L., Brown, A.J. and Ernst, J.F. (2004) APSES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell, 15, 3167-3180.
11. Dou, X.Y., Wang, Q., Qi, Z.Q., Song, W.W., Wang, W., Guo, M., Zhang, H.F., Zhang, Z.G., Wang, P. and Zheng, X.B. (2011) MoVam7, a conserved SNARE involved in vacuole assembly, is required for growth, endocytosis, ROS accumulation, and pathogenesis of Magnaporthe oryzae. PLoS ONE, 6, e16439.
12. Ebbole, D.J. (2007) Magnaporthe as a model for understanding host-pathogen interactions. Annu. Rev. Phytopathol. 45, 437-456.
13. Fujioka, T., Mizutani, O., Furukawa, K., Sato, N., Yoshimi, A., Yamagata, Y., Nakajima, T. and Abe, K. (2007) MpkA-dependent and -independent cell wall integrity signaling in Aspergillus nidulans. Eukaryot. Cell, 6, 1497-1510.
14. Guo, M., Guo, W., Chen, Y., Dong, S.M., Zhang, X., Zhang, H.F., Song, W.W., Wang, W., Wang, Q., Lv, R.L., Zhang, Z.G., Wang, Y.C. and Zheng, X.B. (2010) The basic leucine zipper transcription factor Moatf1 mediates oxidative stress responses and is necessary for full virulence of the rice blast fungus Magnaporthe oryzae. Mol. Plant-Microbe Interact. 23, 1053-1068.
15. Guo, M., Chen, Y., Du, Y., Dong, Y.H., Guo, W., Zhai, S., Zhang, H.F., Dong, S.M., Zhang, Z.G., Wang, Y.C., Wang, P. and Zheng, X.B. (2011) The bZIP transcription factor MoAP1 mediates the oxidative stress response and is crucial for pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog. 7, e1001302.
16. Hansberg, W., de Groot, H. and Sies, H. (1993) Reactive oxygen species associated with cell differentiation in Neurospora crassa. Free Radic. Biol. Med. 14, 287-293.
17. Harris, S.D., Morrell, J.L. and Hamer, J.E. (1994) Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis. Genetics, 136, 517-532.
18. Henson, J.M., Butler, M.J. and Day, A.W. (1999) The dark side of the mycelium: melanins of phytopathogenic fungi. Annu. Rev. Phytopathol. 37, 447-471.
19. Howard, R.J., Ferrari, M.A., Roach, D.H. and Money, N.P. (1991) Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc. Natl. Acad. Sci. USA, 88, 11281-11284.
20. Iyer, V.R., Horak, C.E., Scafe, C.S., Botstein, D., Snyder, M. and Brown, P.O. (2001) Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature, 409, 533-538.
21. Jeon, J., Goh, J., Yoo, S., Chi, M.H., Choi, J., Rho, H.S., Park, J., Han, S.S., Kim, B.R., Park, S.Y., Kim, S. and Lee, Y.H. (2008) A putative MAP kinase kinase kinase, MCK1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Mol. Plant-Microbe Interact. 21, 525-534.
22. Krasley, E., Cooper, K.F., Mallory, M.J., Dunbrack, R. and Strich, R. (2006) Regulation of the oxidative stress response through Slt2p-dependent destruction of cyclin C in Saccharomyces cerevisiae. Genetics, 172, 1477-1486.
23. Kumar, S., Tamura, K. and Nei, M. (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5, 150-163.
24. Levin, D.E. (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69, 262-291.
25. Malagnac, F., Lalucque, 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 Genet. Biol. 41, 982-997.
26. McGinnis, S. and Madden, T.L. (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res. 32, W20-W25.
27. Mehrabi, R., Ding, S. and Xu, J.R. (2008) MADS-box transcription factor mig1 is required for infectious growth in Magnaporthe grisea. Eukaryot. Cell, 7, 791-799.
28. Mitchison, J.M. and Nurse, P. (1985) Growth in cell length in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 75, 357-376.
29. 2 detoxification is required for virulence. Plant Cell, 19, 2293-2309.
30. Nishimura, M., Fukada, J., Moriwaki, A., Fujikawa, T., Ohashi, M., Hibi, T. and Hayashi, N. (2009) Mstu1, an APSES transcription factor, is required for appressorium-mediated infection in Magnaporthe grisea. Biosci. Biotechnol. Biochem. 73, 1779-1786.
31. Odenbach, D., Thines, E., Anke, H. and Foster, A.J. (2009) The Magnaporthe grisea class VII chitin synthase is required for normal appressorial development and function. Mol. Plant Pathol. 10, 81-94.
32. Ohara, T. and Tsuge, T. (2004) FoSTUA, encoding a basic helix-loop-helix protein, differentially regulates development of three kinds of asexual spores, macroconidia, microconidia, and chlamydospores, in the fungal plant pathogen Fusarium oxysporum. Eukaryot. Cell, 3, 1412-1422.
33. Park, G., Bruno, K.S., Staiger, C.J., Talbot, N.J. and Xu, J.R. (2004) Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol. Microbiol. 53, 1695-1707.
34. Park, G., Xue, C., Zhao, X., Kim, Y., Orbach, M. and Xu, J.R. (2006) Multiple upstream signals converge on the adaptor protein Mst50 in Magnaporthe grisea. Plant Cell, 18, 2822-2835.
35. Roncero, C. (2002) The genetic complexity of chitin synthesis in fungi. Curr. Genet. 41, 367-378.
36. Sheppard, D.C., Doedt, T., Chiang, L.Y., Kim, H.S., Chen, D., Nierman, W.C. and Filler, S.G. (2005) The Aspergillus fumigatus StuA protein governs the up-regulation of a discrete transcriptional program during the acquisition of developmental competence. Mol. Biol. Cell, 16, 5866-5879.
37. Shindler, J.S., Childs, R.E. and Bardsley, W.G. (1976) Peroxidase from human cervical mucus. The isolation and characterisation. Eur. J. Biochem. 65, 325-331.
38. Skamnioti, P., Henderson, C., Zhang, Z., Robinson, Z. and Gurr, S.J. (2007) A novel role for catalase B in the maintenance of fungal cell-wall integrity during host invasion in the rice blast fungus Magnaporthe grisea. Mol. Plant-Microbe Interact. 20, 568-580.
39. Sohn, K., Urban, C., Brunner, H. and Rupp, S. (2003) EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol. Microbiol. 47, 89-102.
40. Song, W.W., Dou, X.Y., Qi, Z.Q., Wang, Q., Zhang, X., Zhang, H.F., Guo, M., Dong, S.M., Zhang, Z.G., Wang, P. and Zheng, X.B. (2010) R-SNARE homolog MoSec22 is required for conidiogenesis, cell wall integrity, and pathogenesis of Magnaporthe oryzae. PLoS ONE, 5, e13193.
41. Talbot, N.J. (2003) On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu. Rev. Microbiol. 57, 177-202.
42. Talbot, N.J., Ebbole, D.J. and Hamer, J.E. (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell, 5, 1575-1590.
43. Tebarth, B., Doedt, T., Krishnamurthy, S., Weide, M., Monterola, F., Dominguez, A. and Ernst, J.F. (2003) Adaptation of the Efg1p morphogenetic pathway in Candida albicans by negative autoregulation and PKA-dependent repression of the EFG1 gene. J. Mol. Biol. 329, 949-962.
44. 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. Nucleic Acids Res. 22, 4673-4680.
45. Tong, X., Zhang, X., Plummer, K.M., Stowell, K.M., Sullivan, P.A. and Farley, P.C. (2007) GcSTUA, an APSES transcription factor, is required for generation of appressorial turgor pressure and full pathogenicity of Glomerella cingulata. Mol. Plant-Microbe Interact. 20, 1102-1111.
46. Tucker, S.L. and Talbot, N.J. (2001) Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu. Rev. Phytopathol. 39, 385-417.
47. Valent, B., Farrall, L. and Chumley, F.G. (1991) Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics, 127, 87-101.
48. Veneault-Fourrey, C., Barooah, M., Egan, M., Wakley, G. and Talbot, N.J. (2006) Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science, 312, 580-583.
49. Wang, Q. and Szaniszlo, P.J. (2007) WdStuAp, an APSES transcription factor, is a regulator of yeast-hyphal transitions in Wangiella (Exophiala) dermatitidis. Eukaryot. Cell, 6, 1595-1605.
50. Ward, M.P., Gimeno, C.J., Fink, G.R. and Garrett, S. (1995) SOK2 may regulate cyclic AMP-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription. Mol. Cell. Biol. 15, 6854-6863.
51. Watanabe, Y., Irie, K. and Matsumoto, K. (1995) Yeast Rlm1 encodes a serum response factor-like protein that may function downstream of the Mpk1 (Slt2) mitogen-activated protein-kinase pathway. Mol. Cell. Biol. 15, 5740-5749.
52. Watanabe, Y., Takaesu, G., Hagiwara, M., Irie, K. and Matsumoto, K. (1997) Characterization of a serum response factor-like protein in Saccharomyces cerevisiae, Rlm1, which has transcriptional activity regulated by the Mpk1 (Slt2) mitogen-activated protein kinase pathway. Mol. Cell. Biol. 17, 2615-2623.
53. Xu, J.R., Staiger, C.J. and Hamer, J.E. (1998) Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc. Natl. Acad. Sci. USA, 95, 12713-12718.
54. Zhang, H.F., Zhao, Q., Liu, K.Y., Zhang, Z.G., Wang, Y.C. and Zheng, X.B. (2009) MgCRZ1, a transcription factor of Magnaporthe grisea, controls growth, development and is involved in full virulence. FEMS Microbiol. Lett. 293, 160-169.
55. Zhang, H.F., Liu, K.Y., Zhang, X., Song, W.W., Zhao, Q., Dong, Y.H., Guo, M., Zheng, X.B. and Zhang, Z.G. (2010a) A two-component histidine kinase, MoSLN1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Curr. Genet. 56, 517-528.
56. Zhang, H.F., Liu, K.Y., Zhang, X., Tang, W., Wang, J.S., Guo, M., Zhao, Q., Zheng, X.B., Wang, P. and Zhang, Z.G. (2010b) Two phosphodiesterase genes, PDEL and PDEH, regulate development and pathogenicity by modulating intracellular cyclic AMP levels in Magnaporthe oryzae. PLoS ONE, 6, e17241.
57. Zhang, H.F., Tang, W., Liu, K.Y., Huang, Q., Zhang, X., Yan, X., Chen, Y., Wang, J.S., Qi, Z.Q., Wang, Z.Y., Zheng, X.B., Wang, P. and Zhang, Z.G. (2011a) Eight RGS and RGS-like proteins orchestrate growth, differentiation, and pathogenicity of Magnaporthe oryzae. PLoS Pathog. 7, e1002450.
58. Zhang, L.S., Lv, R.L., Dou, X.Y., Qi, Z.Q., Hua, C.L., Zhang, H.F., Wang, Z., Zheng, X.B. and Zhang, Z.G. (2011b) The function of MoGlk1 in integration of glucose and ammonium utilization in Magnaporthe oryzae. PLoS ONE, 6, e22809.
59. Zhao, X., Kim, Y., Park, G. and Xu, J.R. (2005) A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell, 17, 1317-1329.