Differential roles of the phospholipase C genes in fungal development and pathogenicity of Magnaporthe oryzae

Fungal Genetics and Biology

Volumn 48, Issue 4, 2011, Pages 445-455

  Choi, Jinhee ^a   Kim, Kyoung Su ^a   Rho, Hee Sool ^a   Lee, Yong Hwan ^a  

^a Seoul National University   (South Korea)

Author keywords

Calcium signaling; Multiple appressoria; Phospholipase C; Rice blast

Indexed keywords

CALCIUM ION; PHOSPHOLIPASE C;

APPRESSORIUM; ARTICLE; CONIDIUM; CONTROLLED STUDY; FEEDBACK SYSTEM; FUNGAL DEVELOPMENT; FUNGAL MORPHOLOGY; FUNGAL VIRULENCE; MAGNAPORTHE; MAGNAPORTHE ORYZAE; MEMBRANE BINDING; NONHUMAN; PHOSPHOLIPASE C GENE; PHOSPHOLIPASE C2 GENE; PHOSPHOLIPASE C3 GENE; PHOSPHOLIPASE C4 GENE; PHOSPHOLIPASE C5 GENE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

CALCIUM; GENE DELETION; GENETIC COMPLEMENTATION TEST; ISOENZYMES; MAGNAPORTHE; ORYZA SATIVA; PLANT DISEASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SPORES, FUNGAL; TYPE C PHOSPHOLIPASES;

MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE;

EID: 79952043614     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2011.01.001     Document Type: Article

References (67)

1. Bechinger C., Giebel K.F., Schnell M., Leiderer P., Deising H.B., Bastmeyer M. Optical measurements of invasive forces exerted by appresoria of a plant pathogenic fungus. Science 1999, 286:1896-1899.
2. Borkovich K.A., Alex L.A., Yarden O., Freitag M., Turner G.E., Read N.D., et al. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol. Mol. Biol. Rev. 2004, 68:1-108.
3. Bristol A., Hall S.M., Kriz R.W., Stahl M.L., Fan Y.S., Byers M.G., Eddy R.L., Shows T.B., Knopf J.L. Phospholipase C-148: chromosomal location and deletion mapping of functional domains. Cold Spring Harb. Symp. Quant. Biol. 1988, 53:915-920.
4. Choi W., Dean R.A. The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 1997, 9:1973-1983.
5. Choi J., Park J., Jeon J., Chi M.-H., Goh J., Yoo S.-Y., Jung K., Kim H., Park S.-Y., Rho H.-S., Kim S., Kim B.-R., Han S.-S., Kang S., Lee Y.-H. Genome-wide analysis of T-DNA integration into the chromosomes of Magnaporthe oryzae. Mol. Microbiol. 2007, 66:371-382.
6. Choi J., Kim Y., Kim S., Park J., Lee Y.-H. MoCRZ1, a gene encoding a calcineurin-responsive transcription factor, regulates fungal growth and pathogenicity of Magnaporthe oryzae. Fungal Genet. Biol. 2009, 46:243-254.
7. Choi J., Kim Y., Lee Y.-H. Functional analysis of MCNA, a gene encoding a catalytic subunit of calcineurin, in the rice blast fungus Magnaporthe oryzae. J. Microbiol. Biotechnol. 2009, 19:11-16.
8. Chung H.-J., Kim M.-J., Lim J.-Y., Park S.-M., Cha B.-J., Kim Y.-H., Yang M.-S., Kim D.-H. A gene encoding phosphatidyl inositol-specific phospholipase C from Cryphonectria parasitica modulates the lac1 expression. Fungal Genet. Biol. 2006, 43:326-336.
9. Clapham D.E. Calcium signaling. Cell 2007, 131:1047-1058.
10. Dean R.A., Talbot N.J., Ebbole D.J., Farman M.L., Mitchell T.K., Orbach M.J., et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 2005, 434:980-986.
11. Ebbole D.J. Magnaporthe as a model for understanding host-pathogen interactions. Annu. Rev. Phytopathol. 2007, 45:437-456.
12. 2+ activates phospholipase C. Trends Neurosci. 1988, 11:517-520.
13. Flick J.S., Thorner J. Genetic and biochemical characterization of a phosphatidylinositol-specific phospholipase C in Saccharomyces cerevisiae. Mol. Cell. Biol. 1993, 13:5861-5876.
14. Galagan J.E., Calvo S.E., Borkovich K.A., Selker E.U., Read N.D., Jaffe D., et al. The genome sequence of the filamentous fungus Neurospora crassa. Nature 2003, 422:859-868.
15. Gavric O., dos Santos D.B., Griffiths A. Mutation and divergence of the phospholipase C gene in Neurospora crassa. Fungal Genet. Biol. 2007, 44:242-249.
16. Greenspan P., Mayer E.P., Fowler S.D. Nile red: a selective fluorescent stain for intracellular lipid droplets. J. Cell Biol. 1985, 100:965-973.
17. Gritz L., Davis J. Plasmid-encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisiae. Gene 1983, 25:179-188.
18. Holsbeeks I., Lagatie O., Van Nuland A., Van de Velde S., Thevelein J.M. The eukaryotic plasma membrane as a nutrient-sensing device. Trends Biochem. Sci. 2004, 29:556-564.
19. Howard R.J., Ferrari M.A., Roach D.H., Money N.P. Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc. Natl. Acad. Sci. USA 1991, 88:11281-11284.
20. Jeon J., Park S.-Y., Chi M.-H., Choi J., Park J., Rho H.-S., Kim S., Goh J., Yoo S., Choi J., Park J.-Y., Yi M., Yang S., Kwon M.-J., Han S.-S., Kim B.-R., Khang C.-H., Park B., Lim S.-E., Jung K., Kong S., Karunakaran M., Oh H.-S., Kim H., Kim S., Park J., Kang S., Choi W.-B., Kang S., Lee Y.-H. Genome-wide functional analysis of pathogenicity genes in the rice blast fungus. Nat. Genet. 2007, 39:561-565.
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., Lee Y.-H. 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. 2008, 21:525-534.
22. Kim S., Ahn I.-P., Rho H.-S., Lee Y.-H. MHP1, a Magnaporthe grisea hydrophobin gene, is required for fungal development and plant colonization. Mol. Miocrobiol. 2005, 57:1224-1237.
23. Koh Y.J., Hwang B.K., Chung H.S. Adult-plant resistance of rice to leaf blast. Phytopathology 1987, 77:232-236.
24. Kolattukudy P.E., Rogers L.M., Li D., Hwang C.-S., Flaishman M.A. Surface signaling in pathogenesis. Proc. Natl. Acad. Sci. USA 1995, 92:4080-4087.
25. Kurioka S., Matsuda M. Phospholipase C assay using p-nitrophenylphosphorylcholine together with sorbitol and its application to studying the metal and detergent requirement of the enzyme. Anal. Biochem. 1976, 75:281-289.
26. Lee Y.-H., Dean R.A. CAMP regulates infection structure formation in the plant pathogenic fungus Magnaporthe grisea. Plant Cell 1993, 5:693-700.
27. Lee S.C., Lee Y.-H. Calcium/calmodulin-dependent signaling for appressorium formation in the plant pathogenic fungus Magnaporthe grisea. Mol. Cells 1998, 8:698-704.
28. Leeuw T., Wu C., Schrag J.D., Whiteway M., Thomas D.Y., Leberer E. Interaction of a G-protein beta-subunit with a conserved sequence in Ste20/PAK family protein kinases. Nature 1998, 391:191-195.
29. Liu S., Dean R.A. G protein alpha subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol. Plant-Microbe Interact. 1997, 10:1075-1086.
30. Liu Z.M., Kolattukudy P.E. Early expression of the calmodulin gene, which precedes appressorium formation in Magnaporthe grisea, is inhibited by self-inhibitors and requires surface attachment. J. Bacteriol. 1999, 181:3571-3577.
31. Liu H., Suresh A., Willard F.S., Siderovski D.P., Lu S., Naqvi N.I. Rgs1 regulates multiple G alpha subunits in Magnaporthe pathogenesis, asexual growth and thigmotropism. EMBO J. 2007, 26:690-700.
32. Meyer T., Stryer L. Molecular model for receptor-stimulated calcium spiking. Proc. Natl. Acad. Sci. USA 1988, 85:5051-5055.
33. 2+ (SERCA)-pumps: link to heart beats and calcium waves. Cell Calcium 1999, 25:277-290.
34. Mitchell T.K., Dean R.A. The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 1995, 7:1869-1878.
35. Money N.P. Osmotic pressure of aqueous polyethylene glycols: the relationship between molecular weight and vapor pressure deficit. Plant Physiol. 1989, 91:766-769.
36. Nguyen Q.B., Kadotani N., Kasahara S., Tosa Y., Mayama S., Nakayashiki H. Systematic functional analysis of calcium-signalling proteins in the genome of the rice-blast fungus, Magnaporthe oryzae, using a high-throughput RNA-silencing system. Mol. Microbiol. 2008, 68:1348-1365.
37. Nishimura M., Park G., Xu J.R. The G-beta subunit MGB1 is involved in regulating multiple steps of infection-related morphogenesis in Magnaporthe grisea. Mol. Microbiol. 2003, 50:231-243.
38. Odenbach D., Breth B., Thines E., Weber R.W., Anke H., Foster A.J. The transcription factor Con7p is a central regulator of infection-related morphogenesis in the rice blast fungus Magnaporthe grisea. Mol. Microbiol. 2007, 64:293-307.
39. Ou S.H. Rice Disease 1985, Commonwealth Mycological Institute, Kew, UK. second ed.
40. Payne W.E., Fitzgerald-Hayes M. A mutation in PLC1, a candidate phosphoinositide-specific phospholipase C gene from Saccharomyces cerevisiae, causes aberrant mitotic chromosome segregation. Mol. Cell. Biol. 1993, 13:4351-4364.
41. Pryce-Jones E., Crver T., Gurr S.J. The roles of cellulase enzymes and mechanical force in host penetration by Erysiphe graminis f.sp. hordei. Physiol. Mol. Plant Pathol. 1999, 55:175-182.
42. Rhee S.G., Bae Y.S. Regulation of phosphoinositide-specific phospholipase C isozymes. J. Biol. Chem. 1997, 272:15045-15048.
43. Rhee S.G., Suh P.G., Ryu S.H., Lee S.Y. Studies of inositol phospholipid-specific phospholipase C. Science 1989, 244:546-550.
44. Rho H.-S., Kang S., Lee Y.-H. Agrobacterium tumefaciens-mediated transformation of the plant pathogenic fungus, Magnaporthe grisea. Mol. Cells 2001, 12:407-411.
45. Rho H.-S., Jeon J., Lee Y.-H. Phospholipase C-mediated calcium signalling is required for fungal development and pathogenicity in Magnaporthe oryzae. Mol. Plant Pathol. 2009, 10:337-346.
46. Roncero C., Durán A. Effect of calcofluor white and Congo red on fungal cell wall morphogenesis: in vitro activation of chitin polymerization. J. Bacteriol. 1985, 163:1180-1185.
47. Schumacher J., Viaud M., Simon A., Tudzynski B. The G alpha subunit BCG1, the phospholipase C (BcPLC1) and the calcineurin phosphatase co-ordinately regulate gene expression in the grey mould fungus Botrytis cinerea. Mol. Microbiol. 2008, 67:1027-1050.
48. Skamnioti P., Gurr S.J. Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 2007, 19:2674-2689.
49. 2+/phospholipids-binding fold. Cell 1995, 80:929-938.
50. Sweigard J.A., Chumley F.G., Valent B. Disruption of a Magnaporthe grisea cutinase gene. Mol. Gen. Genet. 1992, 232:183-190.
51. Talbot N.J. On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu. Rev. Microbiol. 2003, 57:177-202.
52. Terhune B.T., Bojko R.J., Hoch H.C. Deformation of stomatal guard cell lips and microfabricated artificial topographies during appressorium formation by Uromyces. Exp. Mycol. 1993, 17:70-78.
53. Tisi R., Baldassa S., Belotti F., Martegani E. Phospholipase C is required for glucose-induced calcium influx in budding yeast. FEBS Lett. 2002, 520:133-138.
54. Tuckwell D., Lavens S.E., Birch M. Two families of extracellular phospholipase C genes are present in aspergilli. Mycol. Res. 2006, 110:1140-1151.
55. Valent B. Rice blast as a model system for plant pathology. Phytopathology 1990, 80:33-36.
56. Venkatachalam K., van Rossum D.B., Patterson R.L., Ma H.-T., Gill D.L. The cellular and molecular basis of store-operated calcium entry. Nat. Cell Biol. 2002, 4:E263-272.
57. Viaud M.C., Balhadere P.V., Talbot N.J. A Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection. Plant Cell 2002, 14:917-930.
58. 1 with lipid bilayers and the βγ subunits of heterotrimeric G proteins. Biochemistry (Mosc.) 1999, 38:1517-1524.
59. Xu J.R., Hamer J.E. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 1996, 10:2696-2706.
60. Xu J.R., Staiger C.J., Hamer J.E. 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 1998, 95:12713-12718.
61. 2+-dependent binding of the pleckstrin homology domain to phosphoinositides. Eur. J. Biochem. 1999, 265:481-490.
62. Yoko-o T., Matsui Y., Yagisawa H., Nojima H., Uno I., Toh-e A. The putative phosphoinositide-specific phospholipase C gene, PLC1, of the yeast Saccharomyces cerevisiae is important for cell growth. Proc. Natl. Acad. Sci. USA 1993, 90:1804-1808.
63. Yu J., Hu S., Wang J., Wong G.K., Li S., Liu B., Deng Y., Dai L., Zhou Y., Zhang X., Cao M., Liu J., Sun J., Tang J., Chen Y., Huang X., Lin W., Ye C., Tong W., Cong L., Geng J., Han Y., Li L., Li W., Hu G., Li J., Liu Z., Qi Q., Li T., Wang X., Lu H., Wu T., Zhu M., Ni P., Han H., Dong W., Ren X., Feng X., Cui P., Li X., Wang H., Xu X., Zhai W., Xu Z., Zhang J., He S., Xu J., Zhang K., Zheng X., Dong J., Zeng W., Tao L., Ye J., Tan J., Chen X., He J., Liu D., Tian W., Tian C., Xia H., Bao Q., Li G., Gao H., Cao T., Zhao W., Li P., Chen W., Zhang Y., Hu J., Liu S., Yang J., Zhang G., Xiong Y., Li Z., Mao L., Zhou C., Zhu Z., Chen R., Hao B., Zheng W., Chen S., Guo W., Tao M., Zhu L., Yuan L., Yang H. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 2002, 296:79-92.
64. Yu J.H., Hamari Z., Han K.H., Seo J.A., Reyes-Dominguez Y., Scazzocchio C. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 2004, 41:973-981.
65. Zelter A., Bencina M., Bowman B.J., Yarden O., Read N.D. A comparative genomic analysis of the calcium signaling machinery in Neurospora crassa, Magnaporthe grisea, and Saccharomyces cerevisiae. Fungal Genet. Biol. 2004, 41:827-841.
66. Zhao X., Xu J.R. A highly conserved MAPK-docking site in Mst7 is essential for Pmk1 activation in Magnaporthe grisea. Mol. Microbiol. 2007, 63:881-894.
67. Zhou C., Horstman D., Carpenter G., Roberts M.F. Action of phosphatidylinositol-specific phospholipase Cγ1 on soluble and micellar substrates. J. Biol. Chem. 1999, 274:2786-2793.