The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Global Approaches to Identify Genes Involved during Infection Structure Formation in Rice Blast Fungus, Magnaporthe grisea

  • Park, Woo-Bong (Agrochem R＆D Center, LG Life Science Research Park)
  • Published : 2003.02.01
Download PDF
⟨ Previous Next ⟩

Abstract

The ascomycete Magnaporthe grisea is a pathogen of rice blast and is known to form specialized infection structures called appressoria for successful infection into host cells. To understand the molecular mechanism underlying infection process, appressorium-related genes were identified through global approaches including EST sequencing, differential hybridization, and sup-pression subtractive hybridization. EST database was generated on >2,000 cDNA clones randomly selected from appressorium stage cDNA library. Large number of ESTs showed homology to known proteins possibly involved in infection-related cellular development (attachment, germination, appressorium formation, and colonization) of rice blast fungus. The 1051 ESTs showing significant homology to known genes were assigned to 11 functional categories. Differential hybridization and suppression subtractive hybridization were applied to identify genes showing an appressorium stage specific expression pattern. A number of genes were selected as up-regulated during appressorium formation compared with the vegetative growing stage. Clones from various cDNA libraries constructed in different developmental stages were arrayed on slide glass for further expression profiling study. functional characterization of genes identified from these global approaches may lead to a better understand-ing of the infection process of this devastating plant disease, and the development of novel ways to protect host plant.

Keywords

References

  1. Adams, M. D., Dubnick, M., Kerlavage, A. R, Moreno, R, Kelley, J. M., Utterback, T. R., Nagle, J. W., Fields, C. and Venter, J. C. 1992. Sequence identification of 2,375 human brain genes. Nature 355:632-634 https://doi.org/10.1038/355632a0
  2. Alexander, N. J., Hohn, T. M. and McCormick, S. P. 1998. The TRIll gene of Fusarium sporotrichioides encodes a cytochrome P-450 monooxygenase required for C-15 hydroxylation in trichothecene biosynthesis. Appl. Environ. Microbiol. 64:221-225
  3. Balhadere, P. V., Foster, A. J. and Talbot, N. J. 1999. Identification of pathogenicity mutants of the rice blast fungus Magnaporthe grisea by insertional mutagenesis. Mol. PlantMicrobe Interact. 12:129-142 https://doi.org/10.1094/MPMI.1999.12.2.129
  4. Balhadere, P. V. and Talbot, N. J. (2001) PDEl encodes a P-type ATPase involved in appressorium-mediated plant infection by the rice blast fungus Magnaporthe grisea. Plant Cell 13:1987-2004 https://doi.org/10.1105/tpc.13.9.1987
  5. Basse, C. W., Stumpferl, S. and Kahmann, R. 2000. Characterization of a Ustilago maydis gene specifically induced during the biotrophic phase: evidence for negative as well as positive regulation. Mol. Cell. Biol. 20:329-339 https://doi.org/10.1128/MCB.20.1.329-339.2000
  6. Bell, A. A. and Wheeler, M. H. 1986. Biosynthesis and functions of fungal melanins. Annu. Rev. Phytopathol. 24:411-451 https://doi.org/10.1146/annurev.py.24.090186.002211
  7. Bhari, S. M., Staples, R. C., Freve, P. and Yoder, O. C. 1989. Characterization of an infection structure-specific gene from the rust fungus Uromyces appendiculatus. Gene 81:237-243 https://doi.org/10.1016/0378-1119(89)90184-4
  8. Birch, P. R. J., Avrova, A. O., Duncan, J. M., Lyon, G. D. and Toth, R L. 1999. Isolation of potato genes that are induced during an early stage of the hypersensitive response to Phytophthora infestans. Mol. Plant-Microbe Interact. 12:356-61 https://doi.org/10.1094/MPMI.1999.12.4.356
  9. Choi, W. and Dean, R. A. 1997. The adenylate cyclase gene MACI of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9:1973-1983 https://doi.org/10.1105/tpc.9.11.1973
  10. Chumley, F. G. and Valent, B. 1990. Genetic analysis of melanindeficient, non-pathogenic mutants of Magnaporthe grisea. Mol. Plant-Microbe Interact. 3: 135-143 https://doi.org/10.1094/MPMI-3-135
  11. Cohen, J. 1997. The genomics gamble. Science 275:767-772 https://doi.org/10.1126/science.275.5301.767
  12. Dean, R. A. 1997. Signal pathways and appressorium morphogenesis. Annu. Rev. Phytopathol. 35:211-234 https://doi.org/10.1146/annurev.phyto.35.1.211
  13. Deising, H., Nicholson, R. L., Haug, M., Howard, R. J. and Mengden, K. 1992. Adhesion pad formation and the involvement of cutinase and esterases in the attachment of uredospores to the host cuticle. Plant Cell 4: 1101-1111 https://doi.org/10.1105/tpc.4.9.1101
  14. Deising, H., Rauscher, M., Haug, M. and Heiler, S. 1995. Differentiation and cell wall degrading enzymes in the obligately biotrophic rust fungus Uromyces viciae-fabae. Can. J. Bot. 73:S624-S631 https://doi.org/10.1139/b95-304
  15. DeZwaan, T. M., Carroll, A. M., Valent, B. and Sweigard, J. A. 1999. Magnaporthe grisea Pthl1p is a novel plasma membrane protein that mediates appressorium formation differentiation in response to inductive substrate cues. Plant Cell 11: 2013-2030 https://doi.org/10.1105/tpc.11.10.2013
  16. Diatchenko, L., Lau, Y. F., Campbell, A. P., Chenchik, A., Moqadam, F., et al. 1996. Suppression subtractive hybridization: a method for generating differentially regulated or tissuespecific cDNA probes and libraries. Proc. Natl. Acad. Sci. USA 93:6025-30 https://doi.org/10.1073/pnas.93.12.6025
  17. Dickman, M. B. and Yarden, O. 1999. Serine/threonine protein kinases and phosphatases in filamentous fungi. Fungal Genet. BioI. 26:99-117 https://doi.org/10.1006/fgbi.1999.1118
  18. Dixon, K. P., Xu, J. R., Smimoff, 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 https://doi.org/10.1105/tpc.11.10.2045
  19. Ewing, B. and Green, P. 1998. Base-calling of automated sequencer traces using phred. ll. Error probabilities. Genome Res. 8: 186-194 https://doi.org/10.1101/gr.8.3.186
  20. Fang, E. G. 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 https://doi.org/10.1094/MPMI.2000.13.11.1214
  21. Gilbert, R. D., Johnson, A. M. and Dean, R. A. 1996. Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol. Mol. Plant Pathol. 48:335-346 https://doi.org/10.1006/pmpp.1996.0027
  22. Gold, S. E., Garcia-Pedrajas, M. D. and Martinez-Espinoza, A. D. 2001. New (and used) approaches to the study of fungal pathogenicity. Annu. Rev. Phytopathol. 39:337-365 https://doi.org/10.1146/annurev.phyto.39.1.337
  23. Gordon, D., Abajian, C. and Green, P. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8:175-185 https://doi.org/10.1101/gr.8.3.175
  24. Hahn, M. and Mendgen, K. 1997. Characterization of in plantainduced rust genes isolated from a haustorium-specific cDNA library. Mol. Plant-Microbe Interact. 10:427-437 https://doi.org/10.1094/MPMI.1997.10.4.427
  25. Hahn, M., Neef, U., Struck, C, Gottfert, M. and Mendgen, K. 1997. A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol. PlantMicrobe Interact. 10:438-445 https://doi.org/10.1094/MPMI.1997.10.4.438
  26. Hamer, J. E. and Talbot, N. J. 1998. Infection-related development in the rice blast fungus Magnaporthe grisea. Curro Opin. Microbiol. 1:693-697 https://doi.org/10.1016/S1369-5274(98)80117-3
  27. Higa, A., Hidaka, T., Minai, Y, Matsuoka, Y. and Haga, M. 2001. Active oxygen radicals induce peroxidase activity in rice blade tissues. Biosci. Biotechnol. Biochem. 65: 1852-1855 https://doi.org/10.1271/bbb.65.1852
  28. Howard, R. J. and Ferrari, M. A. 1989. Role of melanin in appressorium formation. Exp. Mycol. 13:403-418 https://doi.org/10.1016/0147-5975(89)90036-4
  29. 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 https://doi.org/10.1073/pnas.88.24.11281
  30. Howard, R. J. and Valent, B. 1996. Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu. Rev. Microbiol. 50:491-512 https://doi.org/10.1146/annurev.micro.50.1.491
  31. Hwang, C. S., Flaishman, M. A. and Kolattukudy, P. E. 1995. Cloning of a gene expressed during appressorium formation by Colletotrichum gloeosporioides and a marked decrease in virulence by disruption of this gene. Plant Cell 7: 183-193 https://doi.org/10.1105/tpc.7.2.183
  32. de Jong, J. C, McCormack, B. J., Smimoff, N. and Talbot, N. J. 1997. Glycerol generates turgor in rice blast. Nature 389:244-245 https://doi.org/10.1038/38418
  33. Judelson, H. S. and Michelmore, R. W. 1990. Highly abundant and stage-specific mRNAs in the obligate pathogen Bremia lactucae. Mol. Plant-Microbe Interact. 3:225-232 https://doi.org/10.1094/MPMI-3-225
  34. Justesen, A., Somerville, S., Christiansen, S. and Giese, H. 1996. Isolation and characterization of two novel genes expressed in germinating conidia of the obligate biotroph Erysiphe graminis' f. sp. hordei. Gene 170: 131-135 https://doi.org/10.1016/0378-1119(95)00875-6
  35. Kamakura, T., Xiao, J., Choi, W., Kochi, T., Yamaguchi, S., Teraoka, T. and Yamaguchi, I. 1999. cDNA subtractive cloning of genes expressed during early stage of appressorium formation by Magnaporthe grisea. Biosci. Biotechnol. Biochem. 63:1407-1413 https://doi.org/10.1271/bbb.63.1407
  36. Kamakura, T., Yamaguchi, S., Saitoh, K., Teraoka, T. and Yamaguchi, I. 2002. A novel gene, CBP1, encoding a putative extracellular chitin binding protein, may play an important role in the hydrophobic surface sensing of Magnaporthe grisea during appressorium formation. Mol. Plant-Microbe Interact. 15:437-444 https://doi.org/10.1094/MPMI.2002.15.5.437
  37. Kamoun, S., Hraber, P., Sorbal, B., Nuss, D. and Govers, F. 1999. Initial assessment of gene diversity for the oomycete pathogen Phytophthora infestans based on expressed sequences. Fungal Genet. BioI. 28:94-106 https://doi.org/10.1006/fgbi.1999.1166
  38. Keon, J., Bailey, A. and Hargreaves, J. 2000. A group of expressed cDNA sequences from the wheat fungal leaf blotch pathogen, Mycophaerella graminicola (Septoria triticii. Fungal Genet. Biol. 29: 118-133 https://doi.org/10.1006/fgbi.2000.1186
  39. Kim, S., Ahn, I-P. and Lee, Y-H. 2001. Analysis of genes expressed during rice-Magnaporthe grisea interactions. Mol. Plant-Microbe Interact. 14: 340-1346
  40. Kruger, W. M., Pritsch, C, Chao, S. and Muehlbauer, G. J. 2002. Functional and comparative bioinformatic analysis of expressed genes from wheat spikes infected with Fusarium graminearum. Mol. Plant-Microbe Interact. 15:445-455 https://doi.org/10.1094/MPMI.2002.15.5.445
  41. Lee, S.-C and Lee, Y.-H. 1998. Calcium/calmodulin-dependent signaling for appressorium formation in the plant pathogenic fungus Magnaporthe grisea. Mol. Cells 8:698-704
  42. Lee, Y.-H. and Dean, R. A. 1993. cAMP regulates infection structure formation in the plant pathogenic fungus Magnaporthe grisea. Plant Cell 5:693-700 https://doi.org/10.1105/tpc.5.6.693
  43. Lee, Y-H. and Dean, R. A. 1993. Stage-specific gene expression during infection structure formation of Magnaporthe grisea. Exp. Mycol. 17:215-222 https://doi.org/10.1006/emyc.1993.1020
  44. Lee, Y.-H. and Dean, R. A. 1994. Hydrophobicity of contact surface induces appressorium formation of Magnaporthe grisea. FEMS Microbiol. Lett. 115:71-76 https://doi.org/10.1111/j.1574-6968.1994.tb06616.x
  45. Liu, S. and Dean, R. A. 1997. G protein alpha subunit genes control growth, development and pathogenicity of Magnaporthe grisea. Mol. Plant-Microbe Interact. 10:1075-1086 https://doi.org/10.1094/MPMI.1997.10.9.1075
  46. Liu, Z. and Kolattukudy, P. K. 1999. Early expression of calrnodulin gene that precedes appressorium formation in Magnaporthe grisea is inhibited by self-inhibitors and requires surface attachment. J. Bacterial. 181:3571-3577
  47. Liu, Z., Szabo, L. J. and Bushnell, W. R. 1993. Molecular cloning and analysis of abundant and stage-specific mRNAs from Puccinia graminis. Mol. Plant-Microbe Interact. 6:84-91 https://doi.org/10.1094/MPMI-6-084
  48. Maeda, T., Wurgler-Murphy, S. and Saito, H. 1994. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369:242-245 https://doi.org/10.1038/369242a0
  49. McCafferty, H. R. K. and Talbot, N. J. 1998. Identification of three ubiquitin genes of the rice blast fungus Magnaporthe grisea, one of which is highly expressed during initial stages of plant colonization. Curro Genet. 33:352-361 https://doi.org/10.1007/s002940050347
  50. Mesterhazy, A, Bartok, T, Mirocha, C. G. and Komoroczy, R. 1999. Nature of wheat resistance to Fusarium head blight and the role of deoxynivalenol for breeding. Plant Breed. 118:97-110 https://doi.org/10.1046/j.1439-0523.1999.118002097.x
  51. Mitchell, T. K. and Dean, R. A 1995. The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenicity by the rice blast pathogen Magnaporthe grisea. Plant Cell 7: 1869-1878 https://doi.org/10.1105/tpc.7.11.1869
  52. Money, N. P. 1997. Mechanism linking cellular pigmentation and pathogenicity in rice blast disease. Fungal Genet. Bioi. 22:151-152 https://doi.org/10.1006/fgbi.1997.1017
  53. Motoyama, T., Imanishi, K. and Yamaguchi, I. 1998. cDNA cloning, expression, and mutagenesis of scytalone dehydratase needed for pathogenicity of the rice blast fungus, Pyricularia oryzae. Biosci. Biotechnol. Biochem. 62:564-566 https://doi.org/10.1271/bbb.62.564
  54. Nurnberger, T. and Scheel, D. 2001. Signal transmission in the plant immune response. Trends in Plant Science 6:372-379 https://doi.org/10.1016/S1360-1385(01)02019-2
  55. Ono, E., Wong, H. L., Kawasaki, T, Hasegawa, M., Kodama, O. and Shimamoto, K. 200 I. Essential role of the small GTPase Rae in disease resistance of rice. Proc. Natl. Acad. Sci. USA 98:759-764 https://doi.org/10.1073/pnas.021273498
  56. Ou, S. H. 1985. Rice Diseases, 2nd ed. (Kew, Surrey, UK: Commonwealth Mycological Institute)
  57. Pieterse, C. M. J., Risseeuw, E. P. and Davidse, L. C. 1991. An in planta-induced gene of Phytophthora infestans codes for ubiquitin. Plant Mol. Bioi. 17:799-811 https://doi.org/10.1007/BF00037062
  58. Pieterse, C. M. J., Verbakel, H. M., Spaans, J. H., Davidse, L. C. and Govers, F. 1993. Increased expression of the calmodulin gene of the late blight fungus Phytophthora infestans during pathogenesis on potato. Mol. Plant-Microbe Interact. 6: 164-172 https://doi.org/10.1094/MPMI-6-164
  59. Qutob, D., Hraber, P. T., Sobral, B. W. S. and Gijzen, M. 2000. Comparative analysis of expressed sequences in Phytophthora sojae. Plant Physiol. 123:243-253 https://doi.org/10.1104/pp.123.1.243
  60. Rauyaree, P., Choi, W., Fang, E., Blackmon, B. and Dean, R. A 2001. Genes expressed during early stages of rice infection with the rice blast fungus Magnaporthe grisea. Mol. Plant Pathol' 2:347-354 https://doi.org/10.1046/j.1464-6722.2001.00085.x
  61. Shi, Z., Christian, D. and Leung, H. 1998. Interactions between spore morphogenetic mutations affect cell types, sporulation, and pathogenesis in Magnaporthe grisea. Mol. Plant-Microbe Interact. II: 199-207
  62. Soanes, D. M., Skinner, W., Keon, J., Hargreaves, J. and Talbot, N. J. 2002. Genomics of phytopathogenic fungi and the development of bioinformatic resources. Mol. Plant-Microbe Interact. 15:421-427 https://doi.org/10.1094/MPMI.2002.15.5.421
  63. Sweigard, J. A, Carroll, A M., FarraH, L., Chumley, F. G. and Valent, B. 1998. Magnaporthe grisea pathogenicity genes obtained through insertional mutagenesis. Mol. Plant-Microbe Interact. 11:404-412 https://doi.org/10.1094/MPMI.1998.11.5.404
  64. Sweigard, J. A, Chumley, F. G. and Valent, B. 1992. Disruption of a Magnaporthe grisea cutinase gene. Mol. Gen. Genet. 232: 183-190
  65. Talbot, N. J., Ebbole, D. J. and Hamer, J. E. 1993. Identification and characterization of MPGi, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575-1590 https://doi.org/10.1105/tpc.5.11.1575
  66. Talbot, N. J., Kershaw, M. J., Wakley, G. E., de Vries, O. M. H., Wessel, J. G. et al. 1996. MPGi encodes a fungal hydrophobin involved in surface interactions during infectionrelated development of Magnaporthe grisea. Plant Cell 8:985-999 https://doi.org/10.1105/tpc.8.6.985
  67. Thines, E., Weber, R. 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 https://doi.org/10.1105/tpc.12.9.1703
  68. Thomas, S. W., Rasmussen, S. W., Glaring, M. A, Rouster, J. A, Christiansen, S. K. and Oliver, R. P. 2001 Gene identification in the obligate fungal pathogen Blumeria graminis by expressed sequence tag analysis. Fungal Genet. Bioi. 33: 195-211 https://doi.org/10.1006/fgbi.2001.1281
  69. 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 https://doi.org/10.1093/emboj/18.3.512
  70. Vidal-Cros, A, Viviani, F., Labesse, G., Boccara, M. and Gaudry, M. 1994 Polyhydroxynaphthalene reductase involved in melanin biosynthesis in Magnaporthe grisea: purification, cDNA cloning and sequencing. Eur. J. Biochem. 219:985-992 https://doi.org/10.1111/j.1432-1033.1994.tb18581.x
  71. Weber, R. W. S., Wakley, G. E., Thines, E. and Talbot, N. J. 2001. the vacuole as central element of the lytic system and sink for lipid droplets in maturing appressoria of Magnaporthe grisea. Protoplasma 216: 101-112 https://doi.org/10.1007/BF02680137
  72. White, O. and Kerlavage, A. R. 1996. TDB: New databases for biological discovery. Methods Enrymol. 266:27-40 https://doi.org/10.1016/S0076-6879(96)66004-2
  73. Wubben, J. P., Joosten, M. H. A J. and De Wit, P. J. G. M. 1994. Expression and localization of two in planta induced extracellular proteins of the fungal tomato pathogen Cladosporium fulvum. Mol. Plant-Microbe Interact. 7:516-524 https://doi.org/10.1094/MPMI-7-0516
  74. Xiao, J. Z., Ohshima, A., Kamakura, T, Ishyama, T and Yamaguchi, I. 1994. Extracelluar glycoproteins associated with cellular differentiation in Magnaporthe grisea. Mol. Plant-Microbe Interact. 7:639-644 https://doi.org/10.1094/MPMI-7-0639
  75. Xiong, L., Lee, M-W., Qi, M. and Yang, Y. 2001. Identification of defense-related rice genes by suppression subtractive hybridization and differential screening. Mol. Plant-Microbe interact. 14:685-692 https://doi.org/10.1094/MPMI.2001.14.5.685
  76. Xoconostle-Cazares, B., Specht, C. A, Robbins, P. W., Liu, Y, Leon, C. and Ruiz-Herrera, J. 1997. Umchs5, a gene coding for a class IV chitin synthase in Ustilago maydis. Fungal Genet. BioI. 22: 199-208 https://doi.org/10.1006/fgbi.1997.1014
  77. Xu, J.-R. 2001. MAP kinases in fungal pathogens. Fungal Genet. Bioi. 31:137-152
  78. 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 Develop. 10:2696-2706 https://doi.org/10.1101/gad.10.21.2696
  79. Xu, J.-R., Staiger, C. J. and Hamer, J. E. 1998. Inactivation of the mitogen-activated protein kinase Mpsl from the rice blast fungus prevents penetration of host cell but allows activation of plant defense responses. Proc. Natl. Acad. Sci. USA 95: 12713-12718 https://doi.org/10.1073/pnas.95.21.12713
  80. Xue, C, Park, G., Choi, W., 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 Cell14:2107-2119 https://doi.org/10.1105/tpc.003426
  81. Xuei, X, Bhairi, S., Staples, R. C. and Yoder, O. C. 1992. Characterization of INF56, a gene expressed during infection structure development of Uromyces appendiculatus. Gene 110:49-55 https://doi.org/10.1016/0378-1119(92)90443-S
  82. Yang, G., Rose, M. S., Turgeon, B. G. and Yoder, O. C. 1996. A polyketide synthase is required for fungal virulence and production of the polyketide T-toxin. Plant Cell 8:2139-2150 https://doi.org/10.1105/tpc.8.11.2139
  83. Yoder, O. C. and Turgeon, B. G. 2001. Fungal genomics and pathogenicity. Curro Opinion Plant Biol. 4:315-321 https://doi.org/10.1016/S1369-5266(00)00179-5

Cited by

  1. Identification of Genes Expressed during Conidial Germination of the Pepper Anthracnose Pathogen, Colletotrichum acutatum vol.23, pp.1, 2013, https://doi.org/10.5352/JLS.2013.23.1.8