An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis

EMBO Journal

Volumn 22, Issue 9, 2003, Pages 2199-2210

  Brachmann, Andreas ^a   Schirawski, Jan ^b   Müller, Philip ^b   Kahmann, Regine ^b  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NONE

Author keywords

Appressoria; MAP kinase; Pathogenic development; Phytopathogenic fungus; Ustilago maydis

Indexed keywords

DNA; FUNGAL ENZYME; MITOGEN ACTIVATED PROTEIN KINASE; PHEROMONE; RNA;

ARTICLE; ENZYME ACTIVITY; FUNGUS; GENE; GENE EXPRESSION REGULATION; INFECTION; KPP6 GENE; LIFE CYCLE; MATING; NONHUMAN; PATHOGENESIS; PLANT; PLANT DISEASE; PLASMID; PRIORITY JOURNAL; USTILAGO MAYDIS;

BASE SEQUENCE; DNA PRIMERS; MITOGEN-ACTIVATED PROTEIN KINASES; PHEROMONES; PLANTS; SEQUENCE DELETION; USTILAGO;

FUNGI; USTILAGO MAYDIS;

EID: 0037881816     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg198     Document Type: Article

References (59)

1. Andrews, D.L., Egan, J.D., Mayorga, M.E. and Gold, S.E. (2000) The Ustilago maydis ubc4 and ubc5 genes encode members of a MAP kinase cascade required for filamentous growth. Mol. Plant Microbe Interact., 13, 781-786.
2. Banks, G.R., Shelton, P.A., Kanuga, N., Holden, D.W. and Spanos, A. (1993) The Ustilago maydis nar1 gene encoding nitrate reductase activity: sequence and transcriptional regulation. Gene, 131, 68-78.
3. Banuett, F. and Herskowitz, I. (1989) Different a alleles are necessary for maintenance of filamentous growth but not for meiosis. Proc. Natl Acad. Sci. USA, 86, 5878-5882.
4. Banuett, F. and Herskowitz, I. (1994a) Morphological transitions in the life cycle of Ustilago maydis and their genetic control by the a and b loci. Exp. Mycol., 18, 247-266.
5. Banuett, F. and Herskowitz, I. (1994b) Identification of fuz7, a Ustilago maydis MEK/MAPKK homolog required for a-locus-dependent and -independent steps in the fungal life cycle. Genes Dev., 8, 1367-1378.
6. Banuett, F. and Herskowitz, I. (1996) Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development, 122, 2965-2976.
7. Bohlmann, R. (1996) Isolierung und Charakterisierung von filamentspezifisch exprimierten Genen aus Ustilago maydis. PhD thesis, Fakultät für Biologie, Ludwig-Maximilian-Universität, München, Germany.
8. Bohlmann, R., Schauwecker, F., Basse, C. and Kahmann, R. (1994) Genetic regulation of mating and dimorphism in Ustilago maydis. In Daniels, M.J. (ed.), Advances in Molecular Genetics of Plant-Microbe Interactions, Vol. 3. Kluwer, Dordrecht, The Netherlands, pp. 239-245.
9. Bölker, M., Urban, M. and Kahmann, R. (1992) The a mating type locus of U.maydis specifies cell signaling components. Cell, 68, 441-450.
10. Bölker, M., Genin, S., Lehmler, C. and Kahmann, R. (1995) Genetic regulation of mating and dimorphism in Ustilago maydis. Can. J. Bot., 73, 320-325.
11. Bottin, A, Kämper, J. and Kahmann, R. (1996) Isolation of a carbon source-regulated gene from Ustilago maydis. Mol. Gen. Genet., 253, 342-352.
12. Brachmann, A., Weinzierl, G., Kämper, J. and Kahmann, R. (2001) The bW/bE heterodimer regulates a distinct set of genes in Ustilago maydis. Mol. Microbiol., 42, 1047-1063.
13. Breitkreutz, A., Boucher, L. and Tyers, M. (2001) MAPK specificity in the yeast pheromone response independent of transcriptional activation. Curr. Biol., 11, 1266-1271.
14. Brundrett, M., Bougher, N., Dell, B., Grove, T. and Malajczuk, N. (1996) Working with Mycorrhizas in Forestry and Agriculture. Australian Centre for International Agricultural Research, Canberra, Australia, Monograph 32.
15. D'Souza, C.A. and Heitman, J. (2001) Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol. Rev., 25, 349-364.
16. Gilbert, M.S., Johnson, A. and Dean, R. (1996) Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol. Mol. Plant Pathol., 48, 335-346.
17. Gillissen, B., Bergemann, J., Sandmann, C., Schröer, B., Bölker, M. and Kahmann, R. (1992) A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell, 68, 647-657.
18. Guthrie, C. and Fink, G.R. (1991) Guide to Yeast Genetics and Molecular Biology. Academic Press, San Diego, CA.
19. Hartmann, H.A., Kahmann, R. and Bölker, M. (1996) The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO J., 15, 1632-1641.
20. Hartmann, H.A., Krüger, J., Lottspeich, F. and Kahmann, R. (1999) Environmental signals controlling sexual development of the com smut fungus Ustilago maydis through the transcriptional regulator Prf1. Plant Cell, 11, 1293-1306.
21. Hoffman, C.S. and Winston, F. (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of E.coli. Gene, 57, 267-272.
22. Holliday, R. (1974) Ustilago maydis. In King,R.C. (ed.), Handbook of Genetics, Vol. 1. Plenum Press, New York, NY, pp. 575-595.
23. Huber, S.M., Lottspeich, F. and Kämper, J. (2002) A gene that encodes a product with similarity to dioxygenases is highly expressed in teliospores of Ustilago maydis. Mol. Genet. Genomics, 267, 757-771.
24. Kahmann, R., Steinberg, G., Basse, C., Feldbrügge, M. and Kämper, J. (2000) Ustilago maydis, the causative agent of com smut disease. In Kronstad, J.W. (ed.), Fungal Pathology. Kluwer, Dordrecht, The Netherlands, pp. 347-371.
25. Kämper, J., Reichmann, M., Romeis,T., Bölker, M. and Kahmann, R. (1995) Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell, 81, 73-83.
26. Koppitz, M., Spellig, T., Kahmann, R. and Kessler, H. (1996) Lipoconjugates: structure-activity studies for pheromone analogues of Ustilago maydis with varied lipophilicity. Int. J. Pept. Protein Res., 48, 377-390.
27. Kronstad, J., De Maria, A., Funnell, D., Laidlaw, R.D., Lee, N., Moniz de Sá, M. and Ramesh, M. (1998) Signaling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathways. Arch. Microbiol., 170, 395-404.
28. Krüger, J., Loubradou, G., Regenfelder, E., Hartmann, A. and Kahmann, R. (1998) Crosstalk between cAMP and pheromone signalling pathways in Ustilago maydis. Mol. Gen. Genet., 260, 193-198.
29. Kültz, D. (1998) Phylogenetic and functional classification of mitogen- and stress-activated protein kinases. J. Mol. Evol., 46, 571-588.
30. Lee, K.S., Irie, K., Gotoh, Y., Watanabe, Y., Araki, H., Nishida, E., Matsumoto, K. and Levin, D.E. (1993) A yeast mitogen-activated protein kinase homolog (Mpk1) mediates signalling by protein kinase C. Mol. Cell. Biol., 13, 3067-3075.
31. Lee, Y.-H. and Dean, R. (1994) Hydrophobicity of contact surface induces appressorium formation in Magnaporthe grisea. FEMS Microbiol. Lett., 115, 71-76.
32. Lev, S., Sharon, A., Hadar,R., Ma,H. and Horwitz,B.A. (1999) A mitogen-activated protein kinase of the com leaf pathogen Cochliobolus heterostrophus is involved in conidiation, appressorium formation and pathogenicity: diverse roles for mitogen-activated protein kinase homologs in foliar pathogens. Proc. Natl Acad. Sci. USA, 96, 13542-13547.
33. Loubradou, G., Brachmann, A., Feldbrügge, M. and Kahmann, R. (2001) A homologue of the transcriptional repressor Ssn6p antagonizes cAMP signalling in Ustilago maydis. Mol. Microbiol., 40, 719-730.
34. Madhani, H.D. and Fink, G.R. (1997) Combinatorial control required for the specificity of yeast MAPK signaling. Science, 275, 1314-1317.
35. Madhani, H.D. and Fink, G.R. (1998) The riddle of MAP kinase signaling specificity. Trends Genet., 14, 151-155.
36. Madhani, H.D., Styles, C.A. and Fink, G.R. (1997) MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation. Cell, 91, 673-684.
37. Mayorga, M.E. and Gold, S.E. (1999) A MAP kinase encoded by the ubc3 gene of Ustilago maydis is required for filamentous growth and full virulence. Mol. Microbiol., 34, 485-497.
38. Müller, P., Aichinger, C., Feldbrügge, M. and Kahmann, R. (1999) The MAP kinase Kpp2 regulates mating and pathogenic development in Ustilago maydis. Mol. Microbiol., 34, 1007-1017.
39. Mumberg,D., Müller, R. and Funk, M. (1995) Yeast vectors for the controlled expression of heterologous protein in different genetic backgrounds, Gene, 156, 119-122.
40. Murata, Y., Fujii, M., Zolan, M.E. and Kamada, T. (1998) Molecular analysis of pcc1, a gene that leads to A-regulated sexual morphogenesis in Coprinus cinereus. Genetics, 149, 1753-1761.
41. Park, G., Xue, C., Zheng, L., Lam, S. and Xu, J.R. (2002) MST12 regulates infectious growth but not appressorium formation in the rice blast fungus Magnaporthe grisea. Mol. Plant Microbe Interact., 15, 183-192.
42. Romeis, T., Brachmann, A., Kahmann, R. and Kämper, J. (2000) Idenfification of a target gene for the bE/bW homeodomain protein complex in Ustilago maydis. Mol. Microbiol., 37, 54-66.
43. Sambrook, J., Frisch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Sanchez-Martinez, C. and Perez-Martin, J. (2001) Dimorphism in fungal pathogens: Candida albicans and Ustilago maydis - similar inputs, different outputs. Curr. Opin. Microbiol., 4, 214-221.
45. Schauwecker, F., Wanner, G. and Kahmann, R. (1995) Filament-specific expression of a cellulase gene in the dimorphic fungus Ustilago maydis. Biol. Chem. Hoppe Seyler, 376, 617-625.
46. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schäfer, W., Martin, T., Herskowitz, I. and Kahmann, R. (1990) The b alleles of U.maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell, 60, 295-306.
47. Snetselaar, K.M. and Mims, C.W. (1992) Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia, 84, 193-203.
48. Snetselaar, K.M. and Mims, C.W. (1993) Infection of maize stigmas by Ustilago maydis: light and electron microscopy. Phytopathology, 83, 843-850.
49. Snetselaar, K.M. and Mims, C.W. (1994) Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol. Res., 98, 347-355.
50. Sprague, J.R., Jr (1991) Assay of yeast mating reaction. Methods Enzymol., 194, 77-93.
51. Straube, A., Enard, W., Berner, A., Wedlich-Söldner, R., Kahmann, R. and Steinberg, G. (2001) A split motor domain in cytoplasmic dynein. EMBO J., 20, 5901-5100.
52. Takano, Y., Kikuchi, T., Kubo, Y., Hamer, J.E., Mise, K. and Furusawa, I. (2000) The Colletotrichum lagenarium MAP kinase gene CMK1 regulates diverse aspects of fungal pathogenesis. Mol. Plant Microbe Interact., 13, 374-383.
53. Urban, M., Kahmann, R. and Bölker, M. (1996) Identification of the pheromone response element in Ustilago maydis. Mol. Gen. Genet., 251, 31-37.
54. Wong, S., Butler, G. and Wolfe, K.H. (2002) Gene order evolution and paleopolyploidy in hemiascomycete yeasts. Proc. Natl Acad. Sci. USA, 99, 9272-9277.
55. Wösten, H.A., Bohlmann, R., Eckerskorn, C., Lottspeich, F., Bölker, M. and Kahmann, R. (1996) A novel class of small amphipathic peptides affect aerial hyphal growth and surface hydrophobicity in Ustilago maydis. EMBO J., 15, 4274-4281.
56. Xu, J.R. (2000) MAP kinases in fungal pathogens. Fungal Genet. Biol., 31, 137-152.
57. 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.
58. 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 defence responses. Proc. Natl Acad. Sci. USA, 95, 12713-12718.
59. Yanisch-Perron, C., Vieira, J. and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors. Gene, 33, 103-119.