Systematic functional analysis of calcium-signalling proteins in the genome of the rice-blast fungus, Magnaporthe oryzae, using a high-throughput RNA-silencing system

Molecular Microbiology

Volumn 68, Issue 6, 2008, Pages 1348-1365

  Nguyen, Quoc Bao ^a   Kadotani, Naoki ^a   Kasahara, Seiji ^a   Tosa, Yukio ^a   Mayama, Shigeyuki ^a   Nakayashiki, Hitoshi ^a  

^a KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM BINDING PROTEIN; CALMODULIN; CALNEXIN; CALRETICULIN; ENHANCED GREEN FLUORESCENT PROTEIN; LIPOCORTIN; PROTEIN KINASE (CALCIUM,CALMODULIN);

ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; GENE FUNCTION; GENE SILENCING; GENE TARGETING; GENETIC TRANSCRIPTION; GENOME; GERMINATION; MAGNAPORTHE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PRIORITY JOURNAL; RICE BLAST; RNA INTERFERENCE; SPOROGENESIS;

CALCIUM SIGNALING; FUNGAL PROTEINS; GENES, REPORTER; GENETIC VECTORS; GENOME, FUNGAL; GREEN FLUORESCENT PROTEINS; HORDEUM; MAGNAPORTHE; ORYZA SATIVA; PLANT DISEASES; PROMOTER REGIONS (GENETICS); RNA INTERFERENCE; RNA, SMALL INTERFERING; TRITICUM;

FUNGI; MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE;

EID: 44249084246     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06242.x     Document Type: Article

References (83)

1. Adamikova, L., Straube, A., Schulz, I. Steinberg, G. (2004) Calcium signaling is involved in dynein-dependent microtubule organization. Mol Biol Cell 15 : 1969 1980.
2. Ahn, I.P. Suh, S.C. (2007) Calcium/calmodulin-dependent signaling for prepenetration development in Cochliobolus miyabeanus infecting rice. J Gen plant Pathol 73 : 113 120.
3. Ahn, I.P., Uhm, K.H., Kim, S. Lee, Y.H. (2003) Signaling pathways involved in preinfection development of Colletotrichum gloeosporioides, C. coccodes, and C. dematium pathogenic on red pepper. Physiol Mol Plant Pathol 63 : 281 289.
4. Allen, J.B., Zhou, Z., Siede, W., Friedberg, E.C. Elledge, S.J. (1994) The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage induced transcription in yeast. Genes Dev 8 : 2416 1428.
5. Beck, E., Ludwid, G., Auerswald, E.A., Reiss, B. Schaller, H. (1982) Nucleotide sequence and exact location of the neomycin phosphotransferase gene from transposon Tn5. Gene 19 : 327 336.
6. Bencina, M., Legisa, M. Read, N.D. (2005) Cross-talk between cAMP and calcium signaling in Aspergillus niger. Mol Microbiol 56 : 268 281.
7. Berridge, M.J., Bootman, M.D. Roderick, H.L. (2003) Calcium signaling: dynamics, homeostasis and remodeling. Nat Rev Mol Cell Biol 4 : 517 529.
8. Bilsland, E., Arino, J., Saito, H., Sunnerhagen, P. Posas, F. (2000) Rck2 kinase is a substrate for the osmotic stress-activated mitogen-activated protein kinase Hog1. Mol Cellular Biol 20 : 3887 3895.
9. Bilsland, E., Molin, C., Swaminathan, S., Ramne, A. Sunnerhagen, P. (2004) Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol Microbiol 53 : 1743 1756.
10. Brand, A., Shanks, S., Duncan, V.M.S., Yang, M., Mackenzie, K. Gow, N.A.R. (2007) Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr Biol 17 : 347 352.
11. Bush, S.C. (1993) Regulation of cytosol calcium in plants. Plant Physiol 103 : 7 13.
12. Carvalho, M.J.A., Jesuino, R.S.A., Daher, B.S., Pereira, I.S., Freitas, S.M., Soares, C.M.A. Felipe, M.S.S. (2003) Functional and genetic characterization of calmodulin from the dimorphic and pathogenic fungus Paracoccidioides brasiliensis. Fungal Genet Biol 39 : 204 210.
13. Chen, S.H., Smolka, M.B. Zhou, H. (2007) Mechanism of Dun1 activation by Rad53 phosphorylation in Saccharomyces cerevisae. J Biol Chem 282 : 986 995.
14. Chung, H.J., Kim, M.J., Lim, J.Y., Park, S.M., Cha, B.J., Kim, Y.H., et al. (2006) A gene encoding phosphatidyl inositol-specific phospholapase C from Cryphonectria parasitica modulates the lac1 expression. Fungal Genet Biol 43 : 326 336.
15. Chung, K.R. (2003) Involvement of calcium/calmodulin signaling in cercosporin toxin biosynthesis by Cercospora nicotianae. Appl Environ Microbiol 69 : 1187 1196.
16. 2+ homeostasis. J Cell Biol 157 : 1017 1028.
17. D'Aquino, K.E., Monje-Casas, F., Paulson, J., Reiser, V., Charles, G.M., Lai, L., et al. (2005) The protein kinase Kin4 inhibits exit from mitosis in response to spindle position defects. Mol Cell 19 : 223 234.
18. Dalmay, T., Hamilton, A., Rudd, S., Angell, S. Baulcombe, D.C. (2000) An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 26 : 543 553.
19. 2+/calmodulin-dependent kinase is essential for both growth and nuclear division in Aspergillus nidulans. Mol Biol Cell 7 : 1511 1519.
20. 2+/calmodulin-dependent kinase in Aspergillus nidulans spores prevents germination and entry into the cell cycle. J Biol Chem 272 : 3233 3230.
21. Dean, R.A., Talbot, N.J., Ebbole, D.J., Farman, M.L., Mitchell, T.K., Orbach, M.J., et al. (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434 : 980 986.
22. 2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol 156 : 29 34.
23. Dux, M.P. Inan, M. (2006) Identification and characterization of calcium and manganese transporting ATPase (PMR1) gene of Pichia pastoris. Yeast 23 : 613 621.
24. Fitzgerald, A., Kan, J.A. Plummer, K.M. (2004) Simultaneous silencing of multiple genes in the apple scab fungus, Venturia inaequalis, by expression of RNA with chimeric inverted repeats. Fungal Genet Biol 41 : 963 971.
25. Fox, D.S., Cruz, M.C., Sia, R.A., Ke, H., Cox, G.M., Cardenas, M.E. Heitman, J. (2001) Calcineurin regulatory subunit is essential for virulence and mediates interactions with FKBP12-FK506 in Cryptococcus neoformans. Mol Microbiol 39 : 835 849.
26. Gavric, O., dos Santos, D.B. Griffiths, A. (2007) Mutation and divergence of the phospholipase C gene in Neurospora crassa. Fungal Genet Biol 44 : 242 249.
27. Gehring, C.A., Ivring, H.R. Parish, R.W. (1990) Effects of auxin and abscisic acid on cytosolic calcium and pH in plant cells. Proc Natl Acad Sci USA 87 : 9645 9649.
28. Greene, V., Cao, H., Schanne, F.A.X. Bartelt, D.C. (2002) Oxidative stress-induced calcium signaling in Aspergillus nidulans. Cell Signal 14 : 381 476.
29. Gritz, L. Davies, J. (1983) Plasmid encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisae. Gene 25 : 170 188.
30. Hepler, P.K. (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17 : 2142 2155.
31. Howard, R.J. Valent, B. (1996) Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu Rev Microbiol 50 : 491 512.
32. Hua, Z. Graham, T.R. (2003) Requirement for neo1p in retrograde transport from the Golgi complex to the endoplasmic reticulum. Mol Biol Cell 14 : 4971 4983.
33. Jackson, A.L., Bartz, S.R., Schelter, J., Kobayashi, S.V., Burchard, J., Mao, M., et al. (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 21 : 635 637.
34. Jackson, A.L., Burchard, J., Schelter, J., Chau, N., Cleary, M., Lim, L. Linsley, P.S. (2006) Widespread siRNA 'off-target' transcript silencing mediated by seed region sequence complementarity. RNA 12 : 1179 1187.
35. Joseph, J.D. Means, A.R. (2002) Calcium binding is required for calmodulin function in Aspergillus nidulans. Eukaryot Cell 1 : 119 125.
36. Judelson, H.S. Roberts, S. (2002) Novel protein kinase induced during sporangial cleavage in the Oomycete Phytophthora infestans. Eukaryotic Cell 1 : 687 695.
37. Kadotani, N., Nakayashiki, H., Tosa, Y. Mayama, S. (2003) RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol Plant Microbe Interact 16 : 769 775.
38. Kadotani, N., Nakayashiki, H., Tosa, Y. Mayama, S. (2004) One of the two Dicer-like proteins in the filamentous fungi Magnaporthe oryzae genome is responsible for hairpin RNA-trigger RNA silencing and related small interfering RNA accumulation. J Biol Chem 279 : 44467 44474.
39. Kornstein, L.B., Gaiso, M.L., Hammell, R.L. Bartelt, D.C. (1992) Cloning and sequence determination of a cDNA encoding Aspergillus nidulans calmodulin-dependent multifunctional protein kinase. Gene 113 : 75 82.
40. Kothe, G.O. Free, S.J. (1998) Calcineurin subunit B is required for normal vegetative growth in Neurospora crassa. Fungal Genet Biol 23 : 248 258.
41. Kraus, P.R. Heitman, J. (2003) Coping with stress: calmodulin and calcineurin in model and pathogenic fungi. Biochem Biophys Res Commun 311 : 1151 1157.
42. Lee, S.C. Lee, Y.H. (1998) Calcium/calmodulin-dependent signaling for appressorium formation in the plant pathogenic fungus Magnaporthe grisea. Mol Cells 8 : 698 704.
43. Liu, Z.M. Kolattukudy, P.E. (1999) Early expression of the calmodulin gene, which precedes appressorium formation in Magnaporthe grisea, is inhibited by self-inhibitors and requires surface attachment. J Bacteriol 181 : 3571 3577.
44. Liu, H., Cottrell, T.R., Pierini, L.M., Goldman, W.E. Doering, T.M. (2002) RNA interference in the pathogenic fungus Cryptococcus neoformans. Genetics 160 : 463 470.
45. McDonald, T., Brown, D., Keller, N.P. Hammond, T.M. (2005) RNA silencing of mycotoxin production in Aspergillus and Fusarium species. Mol Plant Microbe Interact 18 : 539 545.
46. Magalhaes, B.P., Wayne, R., Humber, R.A., Shields, E.J. Roberts, D.W. (1991) Calcium-regulated appressorium formation of the entomopathogenic fungus Zoophthora radicans. Protoplasma 160 : 77 88.
47. 2+-ATPase PMR1. J Biol Chem 278 : 35292 35298.
48. Mouyna, I., Henry, C., Doering, T.L. Latge, J.P. (2004) Gene silencing with RNA interference in the human pathogenic fungus Aspergillus fumigatus. FEMS Microbiol Lett 237 : 317 324.
49. Murakami, J., Tosa, Y., Kataoka, T., Tomita, R., Kawasaki, J., Chuma, I., et al. (2000) Analysis of host species specificity of Magnaporthe grisea toward wheat using a genetic cross between isolates from wheat and foxtail millet. Phytopathology 90 : 1060 1067.
50. Murata, T., Kadotani, N., Yamaguchi, M., Tosa, Y., Mayama, S. Nakayashiki, H. (2007) siRNA-dependent and -independent post-transcriptional cosuppression of the LTR-retrotransposon MAGGY in the phytopathogenic fungus Magnaporthe oryzae. Nucleic Acids Res 35 : 5987 5994.
51. Nakayashiki, H., Kiyotomi, K., Tosa, Y. Mayama, S. (1999) Transposition of the retrotransposon MAGGY in heterologous species of filamentous fungi. Genetics 153 : 693 703.
52. Nakayashiki, H., Hanada, S., Quoc, N.B., Kadotani, N., Tosa, Y. Mayama, S. (2005) RNA silencing as a tool for exploring gene function in Ascomycete fungi. Fungal Genet Biol 42 : 275 283.
53. Namiki, F., Matsunaga, M., Okuda, M., Inoue, I., Nishi, K., Fujita, Y. Tsuge, T. (2001) Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol Plant Microbe Interact 14 : 580 584.
54. Nelson, G., Kozlova-Zwinderman, O., Collis, A.J., Knight, M.R., Fincham, J.R.S., Stanger, C.P., et al. (2004) Calcium measurement in living filamentous fungi expressing codon-optimized aequorin. Mol Microbiol 52 : 1225 1528.
55. 2+-ATPase, in the yeast Yarrowia lipolytica. Gene 206 : 107 116.
56. Pereira, G. Schiebel, E. (2005) Kin4 kinase delays mitotic exit in response to spindle alignment defects. Mol Cell 19 : 209 221.
57. Rao, J.P., Reena, G. Subramanyam, C. (1997) Calmodulin-dependent protein phosphorylation during conidial germination and growth of Neurospora crassa. Mycol Res 101 : 1484 1488.
58. Rappleye, C.A., Engle, J.T. Goldman, W.E. (2004) RNA interference in Histoplasma capsulatum demonstrates a roles for α-(1,3)-glucan in virulence. Mol Microbiol 53 : 153 165.
59. Rasmussen, C.D., Mean, R.L., Lu, K.P., May, G.S. Means, A.R. (1990) Characterization and expression of the unique calmodulin gene of Aspergillus nidulans. J Biol Chem 265 : 13767 13775.
60. Rasmussen, C., Garen, C., Brining, S., Kincaid, R.L., Means, R.L. Means, A.R. (1994) The calmodulin-dependent protein phosphatase catalytic subunit (calcineurin A) is an essential gene in Aspergillus nidulans. EMBO J 13 : 2545 2552.
61. Robert, I.N., Oliver, R.P., Punt, P.J. van den Hondel, C.A.M.J.J. (1989) Expression of the Escherichia coliβ-glucuronidase gene in industrial and phytopathogenic filamentous fungi. Curr Genet 15 : 177 180.
62. 2+ in the regulation of hyphal extension and branching in Fusarium graminearum A 3/5. Exp Mycol 15 : 263 272.
63. Roy, B.G. Datta, A. (1987) A calmodulin inhibitor blocks morphogenesis in Candida albicans. FEMS Microbiol Lett 41 : 327 329.
64. Sanders, D., Pelloux, J., Brownlee, C. Harper, J.F. (2002) Calcium at the crossroads of signaling. Plant Cell 14 : S401 S417.
65. 2+/calmodulin signaling pathway on morphological development of Candida albicans. Biol Pharm Bull 27 : 1281 1284.
66. Simao, R.C.G. Gomes, S.L. (2001) Structure, expression, and functional analysis of the gene coding for calmodulin in the chytridiomycete Blastocladiella emersonii. J Bacteriol 183 : 2280 2288.
67. Singh, U.P., Prithiviraj, B. Sarma, B.K. (2001) Effect of calcium and calmodulin modulators on the development of Erysiphe pisi on pea leaves. Microbiol Res 156 : 65 69.
68. Solomon, P.S., Rybak, K., Trengove, R.D. Oliver, R.P. (2006) Investigating the role of calcium/calmodulin-dependent protein kinases in Stagonospora nodorum. Mol Microbiol 62 : 367 381.
69. Soriani, F.M., Martins, V.P., Magnani, T., Tudella, V.G., Curtiz, C. Uyemura, S.A. (2005) A PMR1-like calcium ATPase of Aspergillus fumigatus: cloning, identification and functional expression in S. cerevisae. Yeast 22 : 813 824.
70. Steinbach, W.J., Cramer, R.A., Zachary Perfect, B., Jr, Asfaw, Y.G., Sauer, T.C., Najvar, L.K., et al. (2006) Calcineurin controls growth, morphology and pathogenicity in Aspergillus fumigatus. Eukaryot Cell 5 : 1091 1103.
71. Tanguay, P., Bozza, S. Breuil, C. (2006) Assessing RNAi frequency and efficiency in Ophiostoma floccosum and O. piceae. Fungal Genet Biol 43 : 804 812.
72. Tran, N., Cairns, M.K., Dawes, I.W. Arndt, G.M. (2003) Expressing functional siRNAs in mammalian cells using convergent transcription. BMC Biotechnol 3 : 21.
73. Uccelletti, D., Mancini, P., Farina, F., Morrone, S. Palleschi, C. (1999) Inactivation of the KlPMR1 gene of Kluyveromyces lactis results in defective cell wall morphogenesis. Microbiology 145 : 1079 1087.
74. Uhm, K.H., Ahn, I.P., Kim, S. Lee, Y.H. (2002) Calcium/calmodulin- dependent signaling for penetration development in Colletotrichum gloeosporioides. Biochem Cell Biol 93 : 82 87.
75. Urashima, A.S., Hashimoto, Y., Don, L.D., Kusaba, M., Tosa, Y., Nakayashiki, H. Mayama, S. (1999) Molecular analysis of the wheat blast population in Brazil with a homolog of retrotransposon MGR583. Annu Phytopathol Soc Jpn 65 : 429 436.
76. Viaud, M.C., Balhadere, P.V. Talbot, N.J. (2002) A Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection. Plant Cell 14 : 917 930.
77. Viaud, M., Simon, A.B., Brygoo, Y., Pradier, J.M. Lewis, C. (2003) Cyclophilin A and calcineurin function investigated by gene activation, cyclosporine A inhibition and cDNA arrays approaches in the phytophathogenic Botrytis cinerea. Mol Microbiol 50 : 1451 1465.
78. Warwar, V. Dickman, M.B. (1996) Effects of calcium and calmodulin on spore germination and appressorium development in Colletotrichum trifolii. Appl Environ Microbiol 62 : 74 79.
79. Yang, J., Kang, H.A., Ko, S.M., Chae, S.K., Ryu, D.D.Y. Kim, J.Y. (2001a) Cloning of the Aspergillus niger PMRA gene, a homologue of yeast PMR1, and characterization of a pmrA null mutant. FEMS Microbiol Lett 199 : 97 102.
80. Yang, Y.H., Cheng, P., Zhi, G. Liu, T. (2001b) Identification of a calcium/calmodulin-dependent protein kinase that phosphorylates the Neurospora circadian clock protein FREQUENCY. J Biol Chem 276 : 41064 41072.
81. 2+ channel component Mid1. Exp Cell Res 293 : 185 195.
82. Zelter, A., Bencina, M., Bowan, B.J., Yarden, O. Read, N.D. (2004) A comparative genomic analysis of the calcium signaling machinery in Neurospora crassa, Magnaporthe oryzae and Saccharomyces cerevisiae. Fungal Genet Biol 41 : 827 841.
83. Zhou, Z. Elledge, S.J. (1993) DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell 75 : 1119 1127.