Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea

Plant Cell

Volumn 11, Issue 10, 1999, Pages 2045-2058

  Dixon, Katherine P ^a   Xu, Jin Rong ^b   Smirnoff, Nicholas ^a   Talbot, Nicholas J ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b JEALOTT S HILL RESEARCH STATION   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINITOL; FUNGAL GENETICS; GLYCEROL; MYCOSIS; PLANT DISEASE; SIGNAL TRANSDUCTION; STRESS TOLERANCE;

MAGNAPORTHE GRISEA;

EID: 0033213665     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.11.10.2045     Document Type: Article

References (60)

1. Adachi, K., and Hamer, J.E. (1998). Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grisea. Plant Cell 10, 1361-1373.
2. Albertyn, J., Hohmann, S., Thevelein, J.M., and Prior, B.A. (1994). GPD1, which encodes glycerol-3-phcsphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae and its expression is regulated by the high-osmolarity glycerol response pathway. Mol. Cell. Biol. 14, 4135-4144.
3. Alspaugh, J.A., Perfect, J.R., and Heitman, J. (1997). Cryptococcus neoformans mating and virulence are regulated by the G-protein a sub-unit GPA1 and cAMP. Genes Dev. 11, 3206-3217.
4. Altschul, S.F., Gish, W., Miller, W., Myers, C.W., and Lipman, D.L. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
5. Banuett, F. (1998). Signaling in the yeasts: An informational cascade with links to the filamentous fungi. Microbiol. Mol. Biol. Rev. 62, 249-275.
6. Banuett, F., and Herskowitz, I. (1996). Discrete developmental stages during teliospore formation in the maize smut fungus Ustilago maydis. Development 122, 2965-2976.
7. Beckerman, J.L., Naider, F., and Ebbole, D.J. (1997). Inhibition of pathogenicity of the rice blast fungus by Saccharomyces cerevisiae α-factor. Science 276, 1116-1119.
8. Blomberg, A., and Adler, L. (1992). Physiology of osmotolerance in fungi. Adv. Microb. Physiol. 33, 145-212.
9. Bourett, T.M., and Howard, R.J. (1990). In vitro development of penetration structures in the rice blast fungus Magnaporthe grisea. Can. J. Bot. 68, 329-342.
10. Bourett, T.M., and Howard, R.J. (1992). Actin in penetration pegs of the rice blast fungus Magnaporthe grisea. Protoplasma 168, 20-26.
11. Brewster, J.L., and Gustin, M.C. (1994). Positioning of cell growth and division after osmotic stress requires a MAP kinase pathway. Yeast 10, 425-439.
12. Brewster, J.L., de Valoir, T., Dwyer, N.D., Winter, E., and Gustin, M.C. (1993). An osmosensing signal transduction pathway in yeast. Science 259, 1760-1763.
13. Carroll, A.M., Sweigard, J.A., and Valent, B. (1994). Improved vectors for selecting resistance to hygrornycin. Fungal Genet. Newsl. 41, 22.
14. Chida, T., and Sisler, H.D. (1987). Restoration of appressorial penetration ability by melanin precursors in Pyricularia oryzae treated with antipenetrants and in melanin-ceficient mutants. J. Pestic. Sci. 12, 49-55.
15. Choi, W., and Dean, R.A. (1997). The acenylate cyclase gene MAC1 of Magnaporthe grisea control appressorium formation and other aspects of growth and development. Plant Cell 9, 1973-1983.
16. Chumley, F.G., and Valent, B. (1990). Genetic analysis of melanin deficient, nonpathogenic mutants of Magnaporthe grisea. Mol. Plant-Microbe Interact. 3, 135-143.
17. Crawford, M.S., Chumley, F.G., Weaver, C.G., and Valent, B. (1986). Characterization of the heterokaryotic and vegetative diploid phases of Magnaporthe grisea. Genetics 114, 1111-1129.
18. de Jong, J.C., McCormack, B.J., Smirnoff, N., and Talbot, N.J. (1997). Glycerol generates turgor in rice blast. Nature 389, 244-245.
19. Feinberg, A.P., and Vogelstein, B. (1983). A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6-13.
20. Gao, S.J., and Nuss, D.L. (1996). Distinct roles for two G protein α sub-units in fungal virulence, morphology, and reproduction revealed by targeted gene disruption. Proc. Natl. Acad. Sci. USA 93, 14122-14127.
21. Gietz, R.D., and Schiestl, R.H. (1995). Transforming yeast with DNA. Methods Mol. Cell. Biol. 5, 255-269.
22. Gold, S., Duncan, G., Barren, K., and Kronstad, J. (1994). cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev. 8, 2805-2816.
23. Gustin, M.C., Albertyn, J., Alexander, M., and Davenport, K. (1998). MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62, 1264-1300.
24. Hall, J.P., Cherkasova, V., Elion, E., Gustin, M.C., and Winter, E. (1996). The osmoregulatory pathway represses mating pathway activity in Saccharomyces cerevisiae - Isolation of a fus3 mutant that is insensitive to the repression mechanism. Mol. Cell Biol. 16, 6715-6723.
25. Hamer, J.E., Howard, R.J., Chumley, F.G., and Valent, B. (1988). A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239, 288-290.
26. Han, J., Lee, J.D., Bibbs, L., and Ulevitch, R.J. (1994). A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265, 303-311.
27. Han, S.J., Choi, K.Y., Brey, P.T., and Lee, W.J. (1998). Molecular cloning and characterization of a Drosophila p38 mitogen-activated protein kinase. J. Biol. Chem. 273, 369-374.
28. Herskowitz, I. (1995). MAP kinase pathways in yeast: For mating and more. Cell 80, 187-197.
29. Hirayama, T., Maeda, T., Saito, H., and Shonozaki, K. (1995). Cloning and characterization of seven cDNAs for hyperosmolarity-responsiveness (HOR) genes of Saccharomyces cerevisiae. Mol. Gen. Genet. 249, 127-138.
30. Howard, R.J., and Ferrari, M.A. (1989). Role of melanin in appressorium formation. Exp. Mycol. 13, 403-418.
31. 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.
32. 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.
33. Hwang, B.Y., Kim, K.D., and Kim, Y.B. (1989). Carbohydrate composition and acid invertase activity in rice leaves infected with Pyricularia oryzae. J. Phytopathol. 125, 124-132.
34. Johnson, L.N., Noble, M.E., and Owen, D.J. (1996). Active and inactive protein kinases: Structural basis for regulation. Cell 85, 149-158.
35. Kumar, S., McLaughlin, M.M., McDonnell, P.C., Lee, J.C., Livi, G.P., and Young, R.R. (1995). Human mitogen-activated protein kinase CSBP1, but not CSSP2, complements a HOG1 deletion in yeast. J. Biol. Chem. 270, 29043-29046.
36. 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.
37. Lewis, D.H., and Smith, D.C. (1967). Sugar alcohols (polyols) in fungi and green plants. I. Distribution, physiology and metabolism. New Phytol. 66, 143-184.
38. Liu, S., and Dean, R.A. (1997). G protein α subunit genes control growth, development and pathogenicity of Magnaporthe grisea. Mol. Plant-Microbe Interact. 10, 1075-1086.
39. Maeda, T., Wurgler-Murphy, S.M., and Saito, H. (1994). A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369, 242-245.
40. Maeda, T., Takekawa, M., and Saito, H. (1995). Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269, 554-558.
41. Millar, J.B.A., Buck, V., and Wilkinson, M.G. (1995). Pyp1 and Pyp2 PTPases dephosphorylate an osmosensing MAP kinase controlling cell size at division in fission yeast. Genes Dev. 9, 2117-2130.
42. 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 fungus Magnaporthe grisea. Plant Cell 7, 1869-1878.
43. Money, N.P. (1997). Mechanism linking cellular pigmentation and pathogenicity in rice blast disease. Fungal Genet. Biol. 22, 151-152.
44. Money, N.P., and Howard, R.J. (1996). Confirmation of a link between fungal pigmentation, turgor pressure, and pathogenicity using a new method of turgor measurement. Fungal Genet. Biol. 20, 217-227.
45. Norbeck, J., Pahlman, A.K., Akhtar, N., Blomberg, A., and Adler, L. (1996). Purification and characterization of two isoenzymes of DL-glycerol-3-phosphatase from Saccharomyces cerevisiae. Identification of the corresponding GPPI and GPP2 genes and evidence for osmotic regulation of Gpp2p expression by the osmosensing mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem. 271, 13875-13881.
46. O'Rourke, S.M., and Herskowitz, I. (1998). The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes Dev. 12, 2874-2886.
47. Popping, B., Gibbons, T., and Watson, M.D. (1996). The Pisum sativum MAP kinase homolog (PSMAPK) rescues the Saccharomyces cerevisiae hog1 deletion mutant under conditions of high osmotic stress. Plant Mol. Biol. 31, 355-363.
48. Posas, F., and Saito, H. (1998). Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. EMBO J. 17, 1385-1394.
49. Posas, F., Wurgler-Murphy, S.M., Maeda, T., Witten, E.A., Thai, T.C., and Saito, H. (1996). Yeast HOG1 MAP kinase is regulated by a multi-step phosphorelay mechanism in the SLN1-YPD1-SSK1 two-component osmosensor. Cell 86, 865-875.
50. Robinson, M.J., and Cobb, M.H. (1997). Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9, 180-186.
51. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
52. Sheikh-Hamad, D., DiMari, J., Suki, W.N., Safirstein, R., Watts, B.A., and Rouse, D. (1998). p38 kinase activity is essential for osmotic induction of mRNAs for HSP70 and transporter for organic solute betaine in Madin-Darby canine kidney cells. J. Biol. Chem. 273, 1832-1837.
53. Talbot, N.J. (1995). Having a blast: Exploring the pathogenicity of Magnaporthe grisea. Trends Microbiol. 3, 9-16.
54. Talbot, N.J., Ebbole, D.J., and Hamer, J.E. (1993). Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5, 1575-1590.
55. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
56. Valent, B., Farrall, L., and Chumley, F.G. (1991). Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics 127, 87-101.
57. Wong, B., Murray, J.S., Castellanos, M., and Croen, K.D. (1993). D-arabitol metabolism in Candida albicans: Studies of the biosynthetic pathway and the gene that encodes NAD-dependent D-arabitol dehydrogenase. J. Bacteriol. 175, 6314-6320.
58. 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.
59. 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.
60. 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.