Mosfl1 is important for virulence and heat tolerance in magnaporthe oryzae

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Li, Guotian ^a   Zhou, Xiaoying ^a   Kong, Lingan ^a   Wang, Yuling ^b   Zhang, Haifeng ^a   Zhu, Heng ^c   Mitchell, Thomas K ^d   Dean, Ralph A ^e   Xu, Jin Rong ^a  

^a PURDUE UNIVERSITY   (United States)

^b NORTHWEST A F UNIVERSITY   (China)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d OHIO STATE UNIVERSITY   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BARLEY; CONTROLLED STUDY; FUNGAL GENE; FUNGAL PLANT DISEASE; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; FUNGUS MUTANT; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEAT TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; MAGNAPORTHE; MAGNAPORTHE ORYZAE; MOHSP30 GENE; MOHSP98 GENE; MOSFL1 GENE; NONHUMAN; ORTHOLOGY; PMK1 GENE; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RICE; TEMPERATURE SENSITIVITY; YEAST; ADAPTATION; GENETICS; HEAT; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

ASCOMYCOTA; FUNGI; HORDEUM; MAGNAPORTHE ORYZAE; SACCHAROMYCETALES;

ADAPTATION, PHYSIOLOGICAL; GENES, FUNGAL; HOT TEMPERATURE; MAGNAPORTHE; VIRULENCE;

EID: 79956261317     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019951     Document Type: Article

References (71)

1. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, et al. (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980-986.
2. Valent B, (1990) Rice blast as a model system for plant pathology. Phytopathology 80: 33-36.
3. Wilson RA, Talbot NJ, (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7: 185-195.
4. Howard RJ, Ferrari MA, Roach DH, Money NP, (1991) Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci USA 88: 11281-11284.
5. Thines E, Weber RW, Talbot NJ, (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.
6. Kankanala P, Czymmek K, Valent B, (2007) Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19: 706-724.
7. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B, (2009) Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21: 1273-1290.
8. Zhao X, Mehrabi R, Xu J-R, (2007) Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6: 1701-1714.
9. Xu JR, Hamer JE, (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.
10. Bruno KS, Tenjo F, Li L, Hamer JE, Xu JR, (2004) Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot Cell 3: 1525-1532.
11. Choi WB, Dean RA, (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9: 1973-1983.
12. Adachi K, Hamer JE, (1998) Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grisea. Plant Cell 10: 1361-1373.
13. Xu JR, Urban M, Sweigard JA, Hamer JE, (1997) The CPKA gene of Magnaporthe grisea is essential for appressorial penetration. Mol Plant-Microbe Interact 10: 187-194.
14. Mitchell TK, Dean RA, (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.
15. D'Souza CA, Heitman J, (2001) Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol Rev 25: 349-364.
16. Rispail N, Soanes DM, Ant C, Czajkowski R, Grunler A, et al. (2009) Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet Biol 46: 287-298.
17. Hartmann HA, Kruger J, Lottspeich F, Kahmann R, (1999) Environmental signals controlling sexual development of the corn smut fungus Ustilago maydis through the transcriptional regulator prf1. Plant Cell 11: 1293-1305.
18. Kaffarnik F, Muller P, Leibundgut M, Kahmann R, Feldbrugge M, (2003) PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J 22: 5817-5826.
19. Park G, Xue C, Zhao X, Kim Y, Orbach M, et al. (2006) Multiple upstream signals converge on the adaptor protein Mst50 in Magnaporthe grisea. Plant Cell 18: 2822-2835.
20. Zhao X, Kim Y, Park G, Xu JR, (2005) A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell 17: 1317-1329.
21. Xue CY, Park G, Choi WB, Zheng L, Dean RA, et al. (2002) Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus. Plant Cell 14: 2107-2119.
22. Park G, Bruno KS, Staiger CJ, Talbot NJ, Xu JR, (2004) Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol Microbiol 53: 1695-1707.
23. Park G, Xue GY, Zheng L, Lam S, Xu JR, (2002) MST12 regulates infectious growth but not appressorium formation in the rice blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 15: 183-192.
24. Mitchell TK, Dean RA, Xu JR, Zhu H, Oh YY, et al. (2009) Protein chips and chromatin immunoprecipitation- emerging technologies to study macromolecule interactions in Magnaporthe grisea. In: Wang GL, Valent B, editors. Advances in genetics, genomics and control of rice blast disease Berlin Springer-Verlag pp. 73-82.
25. Zhu H, Snyder M, (2003) Protein chip technology. Curr Opin Chem Biol 7: 55-63.
26. Lin YY, Lu JY, Zhang JM, Walter W, Dang WW, et al. (2009) Protein acetylation microarray reveals that NuA4 controls key metabolic target regulating gluconeogenesis. Cell 136: 1073-1084.
27. Hu SH, Xie Z, Onishi A, Yu XP, Jiang LZ, et al. (2009) Profiling the human protein-DNA interactome reveals ERK2 as a transcriptional repressor of interferon signaling. Cell 139: 610-622.
28. Fujita A, Kikuchi Y, Kuhara S, Misumi Y, Matsumoto S, et al. (1989) Domains of the SFL1 protein of yeasts are homologous to Myc oncoproteins or yeast heat-shock transcription factor. Gene 85: 321-328.
29. Galeote VA, Alexandre H, Bach B, Delobel P, Dequin S, et al. (2007) Sfl1p acts as an activator of the HSP30 gene in Saccharomyces cerevisiae. Curr Genet 52: 55-63.
30. Xu JR, Staiger CJ, Hamer JE, (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.
31. Ptacek J, Devgan G, Michaud G, Zhu H, Zhu XW, et al. (2005) Global analysis of protein phosphorylation in yeast. Nature 438: 679-684.
32. Mok J, Im H, Snyder M, (2009) Global identification of protein kinase substrates by protein microarray analysis. Nature Protocols 4: 1820-1827.
33. Breeden L, Nasmyth K, (1987) Cell-cycle control of the yeast Ho gene: cis-and trans-acting regulators. Cell 48: 389-397.
34. Bourett TM, Sweigard JA, Czymmek KJ, Carroll A, Howard RJ, (2002) Reef coral fluorescent proteins for visualizing fungal pathogens. Fungal Genet Biol 37: 211-220.
35. Conlan RS, Tzamarias D, (2001) Sfl1 functions via the co-repressor Ssn6-Tup1 and the cAMP-dependent protein kinase Tpk2. J Mol Biol 309: 1007-1015.
36. Giaever G, Chu AM, Ni L, Connelly C, Riles L, et al. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
37. Villalba F, Collemare J, Landraud P, Lambou K, Brozek V, et al. (2008) Improved gene targeting in Magnaporthe grisea by inactivation of MgKU80 required for non-homologous end joining. Fungal Genet Biol 45: 68-75.
38. Chumley FG, Valent B, (1990) Genetic analysis of melanin-deficient, nonpathogenic mutants of Magnaporthe grisea. Mol Plant-Microbe Interact 3: 135-143.
39. Zhou Z, Li G, Lin C, He C, (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.
40. Shi ZX, Leung H, (1995) Genetic analysis of sporulation in Magnaporthe grisea by chemical and insertional mutagenesis. Mol Plant-Microbe Interact 8: 949-959.
41. Liu WD, Xie SY, Zhao XH, Chen X, Zheng WH, et al. (2010) A homeobox gene is essential for conidiogenesis of the rice blast fungus Magnaporthe oryzae. Mol Plant-Microbe Interact 23: 366-375.
42. Bauer J, Wendland J, (2007) Candida albicans Sfl1 suppresses flocculation and filamentation. Eukaryot Cell 6: 1736-1744.
43. Li Y, Su C, Mao X, Cao F, Chen J, (2007) Roles of Candida albicans Sfl1 in hyphal development. Eukaryot Cell 6: 2112-2121.
44. Masloff S, Poggeler S, Kuck U, (1999) The pro1(+) gene from Sordaria macrospora encodes a C6 zinc finger transcription factor required for fruiting body development. Genetics 152: 191-199.
45. Nishimura M, Fukada J, Moriwaki A, Fujikawa T, Ohashi M, et al. (2009) Mstu1, an APSES transcription factor, is required for appressorium-mediated infection in Magnaporthe grisea. Biosci Biotechnol Biochem 73: 1779-1786.
46. Patzold AJ, Lehming N, (2001) Why Ppr1p is a weak activator of transcription. FEBS Lett 494: 64-68.
47. Taba MRM, Muroff I, Lydall D, Tebb G, Nasmyth K, (1991) Changes in a Swi4,6-DNA-binding complex occur at the time of Ho gene activation in yeast. Genes Dev 5: 2000-2013.
48. Flor-Parra I, Vranes M, Kamper J, Perez-Martin J, (2006) Biz1, a zinc finger protein required for plant invasion by Ustilago maydis, regulates the levels of a mitotic cyclin. Plant Cell 18: 2369-2387.
49. Robertson LS, Fink GR, (1998) The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc Natl Acad Sci USA 95: 13783-13787.
50. Guo B, Styles CA, Feng Q, Fink GR, (2000) A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc Natl Acad Sci USA 97: 12158-12163.
51. Pan X, Heitman J, (2002) Protein kinase A operates a molecular switch that governs yeast pseudohyphal differentiation. Mol Cell Biol 22: 3981-3993.
52. Rupp S, Summers E, Lo HJ, Madhani H, 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.
53. Kim TS, Lee SB, Kang HS, (2004) Glucose repression of STA1 expression is mediated by the Nrg1 and Sfl1 repressors and the Srb8-11 complex. Mol Cell Biol 24: 7695-7706.
54. Song W, Carlson M, (1998) Srb/mediator proteins interact functionally and physically with transcriptional repressor Sfl1. EMBO J 17: 5757-5765.
55. Zhang TT, Li D, Li WJ, Wang Y, Sang JL, (2008) CaSfl1 plays a dual role in transcriptional regulation in Candida albicans. Chin Sci Bull 53: 2624-2631.
56. Grunler A, Walther A, Lammel J, Wendland J, (2010) Analysis of flocculins in Ashbya gossypii reveals FIG2 regulation by TEC1. Fungal Genet Biol 47: 619-628.
57. Tsuji G, Kenmochi Y, Takano Y, Sweigard J, Farrall L, et al. (2000) Novel fungal transcriptional activators, Cmr1p of Colletotrichum lagenarium and Pig1p of Magnaporthe grisea, contain Cys2His2 zinc finger and Zn(II)2Cys6 binuclear cluster DNA-binding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol Microbiol 38: 940-954.
58. Kim S, Park SY, Kim KS, Rho HS, Chi MH, et al. (2009) Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLoS Genet 5: e1000757.
59. Odenbach D, Breth B, Thines E, Weber RW, Anke H, et al. (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.
60. Ding SL, Liu W, Iliuk A, Ribot C, Vallet J, et al. (2010) The tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22: 2495-2508.
61. Mehrabi R, Ding S, Xu JR, (2008) MADS-box transcription factor Mig1 is required for infectious growth in Magnaporthe grisea. Eukaryot Cell 7: 791-799.
62. Talbot NJ, Ebbole DJ, Hamer JE, (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5: 1575-1590.
63. Cullen PJ, Sabbagh W Jr, Graham E, Irick MM, van Olden EK, et al. (2004) A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18: 1695-1708.
64. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
65. Yu JH, Hamari Z, Han KH, Seo JA, Reyes-Dominguez Y, et al. (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41: 973-981.
66. Liu W, Zhou X, Li G, Li L, Kong L, et al. (2011) Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog 7: e1001261.
67. Zhou X, Liu W, Wang C, Xu Q, Wang Y, et al. (2011) A MADS box transcription factor MoMcm1 is required for male fertility, microconidium production, and virulence in Magnaporthe oryzae. Mol Microbiol 80: 33-53.
68. Koga H, Dohi K, Nakayachi O, Mori M, (2004) A novel inoculation method of Magnaporthe grisea for cytological observation of the infection process using intact leaf sheaths of rice plants. Physiol Mol Plant Pathol 64: 67-72.
69. Valent B, Farral L, Chumley FG, (1991) Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics 127: 87-101.
70. Talbot NJ, Kershaw MJ, Wakley GE, deVries OMH, Wessels JGH, et al. (1996) MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8: 985-999.
71. Chao CCT, Ellingboe AH, (1991) Selection for mating competence in Magnaporthe grisea pathogenic to rice. Can J Bot 69: 2130-2134.