Inhibitory phosphorylation of a mitotic cyclin-dependent kinase regulates the morphogenesis, cell size and virulence of the smut fungus Ustilago maydis

Journal of Cell Science

Volumn 118, Issue 16, 2005, Pages 3607-3622

  Sgarlata, Cecilia ^a   Pérez Martín, José ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Cell cycle; Inhibitory phosphorylation; Phytopathogenic fungus; Ustilago maydis; Wee1 like kinases

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; PROTEIN SUBUNIT; UNCLASSIFIED DRUG; WEE1 KINASE;

ARTICLE; CELL CYCLE; CELL CYCLE G2 PHASE; CELL GROWTH; CELL SIZE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; FUNGAL CELL; FUNGAL MORPHOLOGY; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS MUTANT; GENE OVEREXPRESSION; INHIBITION KINETICS; MITOSIS; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PLANT FUNGUS INTERACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SMUT (PLANT DISEASE); USTILAGO MAYDIS;

CATALYTIC DOMAIN; CDC2 PROTEIN KINASE; CELL CYCLE PROTEINS; CELL ENLARGEMENT; CYCLIN B; ENZYME ACTIVATION; FEEDBACK, BIOCHEMICAL; FUNGAL PROTEINS; G2 PHASE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, CDC; MITOSIS; MORPHOGENESIS; NUCLEAR PROTEINS; PHOSPHORYLATION; PLANT DISEASES; PROTEIN-TYROSINE KINASES; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES POMBE PROTEINS; USTILAGO;

EUKARYOTA; FUNGI; USTILAGO MAYDIS;

EID: 24944511673     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02499     Document Type: Article

References (63)

1. Aligue, R., Wu, L. and Russell, P. (1997). Regulation of Schizosaccharomyces pombe Wee1 tyrosine kinase. J. Biol. Chem. 272, 13320-13325.
2. 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.
3. Banuett, F. and Herskowitz, I. (1996). Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122, 2965-2976.
4. Banuett, F. and Herskowitz, I. (2002). Bud morphogenesis and the actin and microtubule cytoskeletons during budding in the corn smut fungus, Ustilago maydis. Fungal Genet. Biol. 37, 149-170.
5. Basse, C. W. and Steinberg, G. (2004). Ustilago maydis, model system for analysis of the molecular basis of fungal pathogenicity. Mol. Plant Pathol. 5, 83-92.
6. 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.
7. Bölker, M., Böhnert, H. U., Braun, K. H., Görl, J. and Kahmann, R. (1995a). Tagging pathogenicity genes in Ustilago maydis by restriction enzyme-mediated integration (REMI). Mol. Gen. Genet. 248, 547-552.
8. Bölker, M., Genin, S., Lehmler, C. and Kahmann, R. (1995b). Genetic regulation of mating and dimorphism in Ustilago maydis. Can. J. Bot. 73, 320-325.
9. CDC28 in response to G1 and G2 cyclins. EMBO J. 12, 3417-3426.
10. Bottin, A., Kämper, J. and Kahmann, R. (1996). Isolation of a carbon source-regulated gene from Ustilago maydis. Mol. Gen. Genet. 253, 342-352.
11. Brachmann, A. (2001). Die frühe infektionsphase von Ustilago maydis: Genregulation dutch das bW/bE-Heterodimer. PhD Dissertation, Ludwig-Maximilians-Universität, München.
12. Brachmann, A., Weinzierl, G, Kämper, J. and Kahmann, R. (2001). Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol. Microbiol. 42, 1047-1063.
13. Brachmann, A., Schirawski, J., Mülller, P. and Kahmann, R. (2003). An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis. EMBO J. 9, 2199-2210.
14. Barral, Y., Parra, M., Bidlingmaier, S. and Snyder, M. (1999). Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev. 13, 176-187.
15. Carroll, C. W., Altman, R., Schieltz, D., Yates, J. R. and Kellog, D. (1998). The septins are required for the mitosis-specific activation of the Gin4 kinase. J. Cell Biol. 143, 709-717.
16. Castillo-Lluva, S., García-Muse, T. and Pérez-Martín, J. (2004). A member of the Fizzy-related family of APC activators is required at different stages of plant infection by Ustilago maydis. J. Cell Sci. 117, 4143-4156.
17. Cerutti, L. and Simanis, V. (2000). Controlling the end of the cell cycle. Curr. Opin. Genet. Dev. 10, 65-69.
18. De Souza, C. P., Ye, X. S. and Osmani, S. A. (1999). Checkpoint defects leading to premature mitosis also cause endoreplication of DNA in Aspergillus nidulans. Mol. Biol. Cell 10, 3661-3674.
19. Devault, A., Fesquet, D., Cavadore, J. C., Garrrigues, A. M., Labbé, J. C., Lorca, T., Picard, A., Philippe, M. and Dorée, M. (1992). Cyclin A potentiates maturation-promoting factor activation in the early Xenopus embryo via inhibition of the tyrosine kinase that phosphorylates Cdc2. J. Cell Biol. 118, 1109-1120.
20. Fantes, P. A. (1977). Control of cell size and cycle time in Schizosaccharomyces pombe. J. Cell Sci. 24, 51-67.
21. wee1 mitotic inhibitor is a tyrosine/serine kinase. Nature 349, 808-811.
22. Fleig, U. N. and Gould, K. L. (1991). Regulation of Cdc2 activity in Schizosaccharomyces pombe: the role of phosphorylation. Semin. Cell Biol. 2, 195-204.
23. García-Muse, T., Steinberg, G. and Pérez-Martín, J. (2003). Pheromone-induced G2 arrest in the phytopathogenic fungus Ustilago maydis. Eukaryot. Cell 2, 494-500.
24. García-Muse, T., Steinberg, G. and Pérez-Martín, J. (2004). Characterization of B-type cyclins in the smut fungus Ustilago maydis: roles in morphogenesis and pathogenicity. J. Cell Sci. 117, 487-506.
25. Garrido, E. and Pérez-Martín, J. (2003). The crk1 gene encodes an Ime2-related protein that is required for morphogenesis in the plant pathogen Ustilago maydis. Mol. Microbiol. 47, 729-743.
26. Garrido, E., Voß, U., Müller, P., Castillo-Lluva, S., Kahmann, R. and Pérez-Martín, J. (2004). The induction of sexual development and virulence in the smut fungus Ustilago maydis depends on Crk1, a novel MAPK protein. Genes Dev. 18, 3117-3130.
27. cdc2. Cell 67, 197-211.
28. + protein kinase regulates entry into mitosis. Nature 342, 39-45.
29. Gillissen, B., Bergemann, J., Sandmann, C., Schrör, B., Bölker, M. and Kahmann, R. (1992). A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68, 647-657.
30. Hanks, S. K. (1991). Eukaryotic protein kinases. Curr. Opin. Struct. Biol. 1, 369-383.
31. Harris, S. D. (1997). The duplication cycle in Aspergillus nidulans. Fungal Genet. Biol. 22, 1-12.
32. Harris, S. D. and Kraus, P. R. (1998). Regulation of septum formation in Aspergillus nidulans by a DNA damage checkpoint pathway. Genetics 148, 1055-1067.
33. Harvey, S. L. and Kellogg, D. R. (2003). Conservation of mechanisms controlling entry into mitosis: budding yeast Wee1 delays entry into mitosis and is required for cell size control. Curr. Biol. 13, 264-275.
34. Holliday, R. (1974). Ustilago maydis. In Handbook of Genetics (ed. R. C. King), pp. 575-595. New York, USA: Plenum Press.
35. Jorgensen, P., Nishikawa, J. L., Breitkreutz, B. J. and Tyers, M. (2002). Systematic identification of pathways that couple cell growth and cell division in yeast. Science 297, 395-400.
36. Kahmann, R., Steinberg, G., Basse, C., Feldbrügge, M. and Kämper, J. (2000). Ustilago maydis, the causative agent of corn smut disease. In Fungal Pathology (ed. J. W. Kronstad), pp. 347-371. Dodrecht, The Netherlands: Kluwer Academic Publishers.
37. Kellogg, D. R. (2003). Wee1-dependent mechanisms required for coordination of cell growth and cell division. J. Cell Sci. 116, 4883-4890.
38. Kraus, P. R. and Harris, S. D. (2001). The Aspergillus nidulans snt genes are required for the regulation of septum formation and cell cycle checkpoints. Genetics 159, 557-569.
39. La Valle, R. and Wittenberg, C. (2001). A role for the Swe1 checkpoint kinase during filamentous growth of Saccharomyces cerevisiae. Genetics 158, 549-562.
40. Lew, D. J. (2000). Cell cycle checkpoints that ensure coordination between nuclear and cytoplasmic events in Saccharomyces cerevisiae. Curr. Opin. Genet. Dev. 10, 47-53.
41. Lew, D. J. and Reed, S. I. (1995). Cell cycle checkpoints monitors cell morphogenesis in budding yeast. J. Cell Biol. 129, 739-749.
42. Lew, D. J. and Kornbluth, S. (1996). Regulatory roles of cyclin dependent kinase phosphorylation in cell cycle control. Curr. Opin. Cell Biol. 8, 795-804.
43. Longtine, M. S., Fares, H. and Pringle, J. R. (1998). Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function. J. Cell Biol. 143, 719-736.
44. Lundgren, K., Walworth, N., Booher, R., Dembski, M., Kirschner, M. and Beach, D. (1991). Mik1 and Wee1 cooperate in the inhibitory tyrosine phosphorylation of Cdc2. Cell 64, 1111-1122.
45. Martínez-Anaya, C., Dickinson, R. J. and Sudbery, P. E. (2003). In yeast, the pseudohyphal phenotype induced by isoamyl alcohol results from the operation of the morphogenesis checkpoint. J. Cell Sci. 116, 3423-3431.
46. McGowan, C. and Russell, P. (1995). Cell cycle regulation of human Wee1. EMBO J. 14, 2166-2175.
47. cdc2 kinase in fission yeast. EMBO J. 10, 4301-4309.
48. Nurse, P. (1975). Genetic control of cell size at cell division in yeast. Nature 256, 547-551.
49. cdc2 on tyrosine 15. Proc. Natl. Acad. Sci. USA 89, 2917-2921.
50. Rey, A. L., Herald, H. A. and Lew, D. J. (1996). Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol. Biol. Cell 7, 1657-1666.
51. Rua, D., Tobe, B. T. and Kron, S. J. (2001). Cell cycle control of yeast filamentous growth. Curr. Opin. Microbiol., 4, 720-727.
52. Rupes, I. (2002). Checking cell size in yeast. Trends Genet. 18, 479-485.
53. + functions as an inducer in the mitotic control of fission yeast. Cell 45, 145-153.
54. +, a gene encoding a protein kinase homolog. Cell 49, 559-567.
55. Sherman, F., Fink, G. R. and Hicks, J. B. (1986). Laboratory Course Manual For Methods In Yeast Genetics. Cold Spring Harbor, NY. Cold Spring Harbor Laboratory Press.
56. Sia, R. A., Herald, H. A. and Lew, D. J. (1996). Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol. Biol. Cell 11, 1657-1666.
57. Snetselaar, K. M. and McCann, M. C. (1997). Using microdensitometry to correlate cell morphology with the nuclear cycle in Ustilago maydis. Mycologia 89, 689-697.
58. Spellig, T., Bottin, A. and Kahmann, R. (1996). Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol. Gen. Genet. 252, 503-509.
59. Steinberg, G., Wedlich-Söldner, R., Brill, M. and Schulz, I. (2001). Microtubules in the fungal pathogen Ustilago maydis are highly dynamic and determine cell polarity. J. Cell Sci. 114, 609-622.
60. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple alignment aided by quality analysis tools. Nucleic Acid Res. 25, 4876-4882.
61. Tsukuda, T., Carleton, S., Fotheringham, S. and Holloman, W. K. (1988). Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol. Cell. Biol. 8, 3703-3709.
62. Watanabe, N., Broome, M. and Hunter, T. (1995). Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J. 14, 1878-1891.
63. Wolkow, T. D., Harris, S. D. and Hamer, J. E. (1996). Cytokinesis in Aspergillus nidulansis controlled by cell size, nuclear positioning and mitosis. J. Cell Sci. 109, 2179-2188.