A MADS-box transcription factor MoMcm1 is required for male fertility, microconidium production and virulence in Magnaporthe oryzae

Molecular Microbiology

Volumn 80, Issue 1, 2011, Pages 33-53

  Zhou, Xiaoying ^a   Liu, Wende ^a   Wang, Chenfang ^b   Xu, Qijun ^b   Wang, Yang ^b   Ding, Shengli ^a   Xu, Jin Rong ^a  

^a PURDUE UNIVERSITY   (United States)

^b NORTHWEST A F UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; PROTEIN MATA 1; PROTEIN MST12; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MCM1; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; CONIDIUM; CONTROLLED STUDY; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS HYPHAE; FUSION GENE; GENE DELETION; GENE EXPRESSION; HYDROPHILICITY; MAGNAPORTHE; MAGNAPORTHE ORYZAE; MALE FERTILITY; MCM1 GENE; MST12 GENE; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

FUNGAL PROTEINS; IMMUNOPRECIPITATION; MAGNAPORTHE; MASS SPECTROMETRY; ORYZA SATIVA; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES; VIRULENCE;

MAGNAPORTHE ORYZAE;

EID: 79953036304     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07556.x     Document Type: Article

References (80)

1. Arora, R., Agarwal, P., Ray, S., Singh, A.K., Singh, V.P., Tyagi, A.K., and Kapoor, S. (2007) MADS-box gene family in rice: genome-wide identification organization and expression profiling during reproductive development and stress. BMC Genomics 8: 242-262.
2. Balciunas, D., and Ronne, H. (1999) Yeast genes GIS1-4: multicopy suppressors of the Gal(-) phenotype of snf1 mig1 srb8/10/11 cells. Mol Gen Genet 262: 589-599.
3. 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.
4. Cervantes-Chavez, J.A., Kronberg, F., Passeron, S., and Ruiz-Herrera, J. (2009) Regulatory role of the PKA pathway in dimorphism and mating in Yarrowia lipolytica. Fungal Genet Biol 46: 390-399.
5. Chao, C.C.T., and Ellingboe, A.H. (1991) Selection for mating competence in Magnaporthe grisea pathogenic to rice. Can J Bot 69: 2130-2134.
6. Choi, J., Kim, Y., Kim, S., Park, J., and Lee, Y.H. (2009) MoCRZ1, a gene encoding a calcineurin-responsive transcription factor, regulates fungal growth and pathogenicity of Magnaporthe oryzae. Fungal Genet Biol 46: 243-254.
7. Chou, S., Lane, S., and Liu, H.P. (2006) Regulation of mating and filamentation genes by two distinct Ste12 complexes in Saccharomyces cerevisiae. Mol Cell Biol 26: 4794-4805.
8. Damveld, R.A., Arentshorst, M., Franken, A., vanKuyk, P.A., Klis, F.M., van den Hondel, C., and Ram, A.F.J. (2005) The Aspergillus niger MADS-box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress. Mol Microbiol 58: 305-319.
9. Didmon, M., Davis, K., Watson, P., Ladds, G., Broad, P., and Davey, J. (2002) Identifying regulators of pheromone signalling in the fission yeast Schizosaccharomyces pombe. Curr Genet 41: 241-253.
10. Ding, S.L., Mehrabi, R., Koten, C., Kang, Z.S., Wei, Y.D., Seong, K.Y., etal. (2009) Transducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearum. Eukaryot Cell 8: 867-876.
11. Ding, S.L., Liu, W., Iliuk, A., Ribot, C., Vallet, J., Tao, A., etal. (2010) The Tig1 HDAC complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22: 2495-2508.
12. Dixon, K.P., Xu, J.R., Smirnoff, N., and Talbot, N.J. (1999) Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11: 2045-2058.
13. Ebbole, D.J. (2007) Magnaporthe as a model for understanding host-pathogen interactions. Annu Rev Phytopathol 45: 437-456.
14. Fang, E.G.C., and Dean, R.A. (2000) Site-directed mutagenesis of the MAGB gene affects growth and development in Magnaporthe grisea. Mol Plant Microbe Interact 13: 1214-1227.
15. Fornara, F., Marziani, G., Mizzi, L., Kater, M., and Colombo, L. (2003) MADS-box genes controlling flower development in rice. Plant Biol 5: 16-22.
16. Fujikawa, T., Kuga, Y., Yano, S., Yoshimi, A., Tachiki, T., Abe, K., and Nishimura, M. (2009) Dynamics of cell wall components of Magnaporthe grisea during infectious structure development. Mol Microbiol 73: 553-570.
17. Gavin, A.C., Aloy, P., Grandi, P., Krause, R., Boesche, M., Marzioch, M., etal. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440: 631-636.
18. Gobeil, L.A., Plante, P., Rohani, M., Ouellette, M., and Provost, P. (2008) Involvement of Dcr1 in post-transcriptional regulation of gene expression in Schizosaccharomyces pombe. Front Biosci 13: 2203-2215.
19. Hoi, J.W.S., Herbert, C., Bacha, N., Connell, R.O., Lafitte C., Borderies, G., etal. (2007) Regulation and role of a STE12-like transcription factor from the plant pathogen Colletotrichum lindemuthianum. Mol Microbiol 64: 68-82.
20. 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.
21. Jeon, J., Goh, J., Yoo, S., Chi, M.H., Choi, J., Rho, H.S., etal. (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. de Jong, J.C., McCormack, B.J., Smirnoff, N., and Talbot, N.J. (1997) Glycerol generates turgor in rice blast. Nature 389: 244-245.
23. Jung, U.S., Sobering, A.K., Romeo, M.J., and Levin, D.E. (2002) Regulation of the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP kinase. Mol Microbiol 46: 781-789.
24. Kankanala, P., Czymmek, K., and Valent, B. (2007) Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19: 706-724.
25. Kato, H., Mayama, S., Sekine, R., Kanazawa, E., Izutani, Y., Urashima, A.S., and Kunoh, H. (1994) Microconidium formation in Magnaporthe grisea. Ann Phytopathol Soc Jpn 60: 175-185.
26. Koga, H. (1994) Hypersensitive death, autofluorescence, and ultrastructural-changes in cells of leaf sheaths of susceptible and resistant near-isogenic lines of rice (PI-Z(T)) in relation to penetration and growth of Pycularia oryza. Can J Bot 72: 1463-1477.
27. Krogan, N.J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., etal. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637-643.
28. Krueger, J., Aichinger, C., Kahmann, R., and Boelker, M. (1997) A MADS-box homologue in Ustilago maydis regulates the expression of pheromone-inducible genes but is nonessential. Genetics 147: 1643-1652.
29. Kuo, M.H., Nadeau, E.T., and Grayhack, E.J. (1997) Multiple phosphorylated forms of the Saccharomyces cerevisiae Mcm1 protein include an isoform induced in response to high salt concentrations. Mol Cell Biol 17: 819-832.
30. Li, L., Xue, C.Y., Bruno, K., Nishimura, M., and Xu, J.R. (2004) Two PAK kinase genes, CHM1 and MST20, have distinct functions in Magnaporthe grisea. Mol Plant Microbe Interact 17: 547-556.
31. Li, L., Ding, S.L., Sharon, A., Orbach, M., and Xu, J.R. (2007) Mir1 is highly upregulated and localized to nuclei during infectious hyphal growth in the rice blast fungus. Mol Plant Microbe Interact 20: 448-458.
32. Liu, W., Ding, S., Iliuk, A., and Tao, A. (2011a) Identifying protein complexes by affinity purification and mass spectrometry analysis in the rice blast fungus. In Fungal Genomics: Methods and Protocols. Xu, J.R., and Bluhm, B. (eds). Philadelphia, PA, USA: Humana Press, Springer Science + Business Media, LLC. (in press).
33. Liu, W., Zhou, X., Li, G., Li, L., Kong, L., Wang, C., etal. (2011b) Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog 7: e1001261.
34. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
35. Mead, J., Bruning, A.R., Gill, M.K., Steiner, A.M., Acton, T.B., and Vershon, A.K. (2002) Interactions of the Mcm1 MADS box protein with cofactors that regulate mating in yeast. Mol Biol Cell 22: 4607-4621.
36. 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.
37. Messenguy, F., and Dubois, E. (2003) Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316: 1-21.
38. Mitchell, T.K., and Dean, R.A. (1995) The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7: 1869-1878.
39. Neeley, L.A., and Hoffman, C.S. (2000) Protein kinase A and mitogen-activated protein kinase pathways antagonistically regulate fission yeast fbp1 transcription by employing different modes of action at two upstream activation sites. Mol Cell Biol 20: 6426-6434.
40. Nishimura, M., Park, G., and Xu, J.R. (2003) The G-beta subunit MGB1 is involved in regulating multiple steps of infection-related morphogenesis in Magnaporthe grisea. Mol Microbiol 50: 231-243.
41. Nolting, N., and Poggeler, S. (2006a) A STE12 homologue of the homothallic ascomycete Sordaria macrospora interacts with the MADS box protein MCM1 and is required for ascosporogenesis. Mol Microbiol 62: 853-868.
42. Nolting, N., and Poggeler, S. (2006b) A MADS box protein interacts with a mating-type protein and is required for fruiting body development in the homothallic ascomycete Sordaria macrospora. Eukaryot Cell 5: 1043-1056.
43. Odenbach, D., Breth, B., Thines, E., Weber, R.W.S., Anke, H., and Foster, A.J. (2007) The transcription factor Con7p is a central regulator of infection-related morphogenesis in the rice blast fungus Magnaporthe grisea. Mol Microbiol 64: 293-307.
44. Oehlen, L.J.W.M., Mckinney, J.D., and Cross, F.R. (1996) Ste12 and Mcm1 regulate cell cycle-dependent transcription of FAR1. Mol Cell Biol 16: 2830-2837.
45. Park, G., Xue, G.Y., Zheng, L., Lam, S., and Xu, J.R. (2002) MST12 regulates infectious growth but not appressorium formation in the rice blast fungus Magnaporthe grisea. Mol Plant Microbe Interact 15: 183-192.
46. 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.
47. Park, G., Xue, C., Zhao, X., Kim, Y., Orbach, M., and Xu, J.R. (2006) Multiple upstream signals converge on an adaptor protein Mst50 to activate the PMK1 pathway in Magnaporthe grisea. Plant Cell 18: 2822-2835.
48. Rispail, N., and Pietro, A.D. (2009) Fusarium oxysporum Ste12 controls invasive growth and virulence downstream of the fmk1 mapk cascade. Mol Plant Microbe Interact 22: 830-839.
49. Rottmann, M., Dieter, S., Brunner, H., and Rupp, S. (2003) A screen in Saccharomyces cerevisiae identified CaMCM1, an essential gene in Candida albicans crucial for morphogenesis. Mol Microbiol 47: 943-959.
50. Rupp, S., Summers, E., Lo, H.J., Madhani, H., and Fink, G. (1999) MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J 18: 1257-1269.
51. Saunders, D.G.O., Aves, S.J., and Talbot, N.J. (2010) Cell cycle-mediated regulation of plant infection by the rice blast fungus. Plant Cell 22: 497-507.
52. Schamber, A., Leroch, M., Diwo, J., Mendgen, K., and Hahn, M. (2010) The role of mitogen-activated protein (MAP) kinase signalling components and the Ste12 transcription factor in germination and pathogenicity of Botrytis cinerea. Mol Plant Pathol 11: 105-119.
53. Shi, Z.X., and Leung, H. (1995) Genetic analysis of sporulation in Magnaporthe grisea by chemical and insertional mutagenesis. Mol Plant Microbe Interact 8: 949-959.
54. Shore, P., and Sharrocks, A.D. (1995) The MADS-box family of transcription factors. Eur J Biochem 229: 1-13.
55. Sweigard, J.A., Chumley, F.G., and Valent, B. (1992) Disruption of a Magnaporthe grisea cutinase gene. Mol Gen Genet 232: 183-190.
56. Tabb, D.L., Eng, J.K., and Yates, J.R. (2001) Protein identification by SEQUEST. In Proteome Research: Mass Spectrometry. James, P. (ed.). New York: Springer-Verlag Berlin Heidelberg, pp. 125-142.
57. Takada, H., Nishida, A., Domae, M., Kita, A., Yamano, Y., Uchida, A., etal. (2010) The cell surface protein gene Ecm33+ is a target of the two transcription factors Atf1 and Mbx1 and negatively regulates pmk1 mapk cell integrity signaling in fission yeast. Mol Biol Cell 21: 674-685.
58. Tao, W.A., Wollscheid, B., O'Brien, R., Eng, J., Li, X., Bodenmiller, B., etal. (2005) Quantitative phosphoproteome analysis using a dendrimer conjugation chemistry and mass spectrometry. Nat Methods 2: 591-598.
59. Tatebayashi, K., Tanaka, K., Yang, H.Y., Yamamoto, K., Matsushita, Y., Tomida, T., etal. (2007) Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J 26: 3521-3533.
60. 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.
61. Tsuji, G., Fujii, S., Tsuge, S., Shiraishi, T., and Kubo, Y. (2003) The Colletotrichum lagenarium Ste12-like gene CST1 is essential for appressorium penetration. Mol Plant Microbe Interact 16: 315-325.
62. Tucker, S.L., Thornton, C.R., Tasker, K., Jacob, C., Giles, G., Egan, M., and Talbot, N.J. (2004) A fungal metallothionein is required for pathogenicity of Magnaporthe grisea. Plant Cell 16: 1575-1588.
63. Tucker, S.L., Besi, M.I., Galhano, R., Franceschetti, M., Goetz, S., Lenhert, S., etal. (2010) Common genetic pathways regulate organ-specific infection-related development in the rice blast fungus. Plant Cell 22: 953-972.
64. Urban, M., Bhargava, T., and Hamer, J.E. (1999) An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J 18: 512-521.
65. Wilson, R.A., and Talbot, N.J. (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7: 185-195.
66. Xu, H.P., Rajavashisth, T., Grewal, N., Jung, V., Riggs, M., Rodgers, L., and Wigler, M. (1992) A gene encoding a protein with 7 zinc finger domains acts on the sexual-differentiation pathways of Schizosaccharomyces pombe. Mol Biol Cell 3: 721-734.
67. Xu, J.R., and Hamer, J.E. (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10: 2696-2706.
68. Xu, J.R., Urban, M., Sweigard, J.A., and Hamer, J.E. (1997) The CPKA gene of Magnaporthe grisea is essential for appressorial penetration. Mol Plant Microbe Interact 10: 187-194.
69. 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.
70. Xu, J.R., Peng, Y.L., Dickman, M.B., and Sharon, A. (2006) The dawn of fungal pathogen genomics. Annu Rev Phytopathol 44: 337-366.
71. Xu, J.R., Zhao, X., and Dean, R.A. (2007) From genes to genomes; a new paradigm for studying fungal pathogenesis in Magnaporthe oryzae. Adv Genet 57: 175-218.
72. Xue, C.Y., Park, G., Choi, W.B., Zheng, L., Dean, R.A., and Xu, J.R. (2002) Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus. Plant Cell 14: 2107-2119.
73. Yang, J., Zhao, X., Sun, J., Kang, Z., Ding, S., Xu, J.R., and Peng, Y.L. (2010) A novel protein Com1 is required for normal conidium morphology and full virulence in Magnaporthe oryzae. Mol Plant Microbe Interact 23: 112-123.
74. Zeigler, R.S. (1998) Recombination in Magnaporthe grisea. Annu Rev Phytopathol 36: 249-275.
75. Zhao, X.H., and Xu, J.R. (2007) A highly conserved MAPK-docking site in Mst7 is essential for Pmk1 activation in Magnaporthe grisea. Mol Microbiol 63: 881-894.
76. Zhao, X.H., Xue, C., Kim, Y., and Xu, J.R. (2004) A ligation-PCR approach for generating gene replacement constructs in Magnaporthe grisea. Fungal Genet Newsl 51: 17-18.
77. 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.
78. Zhao, X., Mehrabi, R., and Xu, J.-R. (2007) Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6: 1701-1714.
79. Zhou, F., Galan, J., Geahlen, R.L., and Tao, W.A. (2007) A novel quantitative proteomics strategy to study phosphorylation-dependent peptide-protein interactions. J Proteome Res 6: 133-140.
80. Zhou, Z.Z., Li, G.H., Lin, C.H., and He, C.Z. (2009) Conidiophore Stalk-less1 encodes a putative zinc-finger protein involved in the early stage of conidiation and mycelial infection in Magnaporthe oryzae. Mol Plant Microbe Interact 22: 402-410.