The Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signaling pathways to coordinate the cell cycle and pathogenic development

Plant Cell

Volumn 22, Issue 8, 2010, Pages 2908-2922

  Heimel, Kai ^a,b   Scherer, Mario ^b,c   Schuler, David ^a   Kämper, Jörg ^a,b  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c QIAGEN GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

USTILAGO MAYDIS;

EID: 77957780985     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.076265     Document Type: Article

References (74)

1. Banuett, F., and Herskowitz, I. (1989). Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc. Natl. Acad. Sci. USA 86: 5878-5882.
2. Böhmer, C., Ripp, C., and Bölker, M. (2009). The germinal centre kinase Don3 triggers the dynamic rearrangement of higher-order septin structures during cytokinesis in Ustilago maydis. Mol. Microbiol. 74: 1484-1496.
3. Bölker, M., Böhnert, H.U., Braun, K.H., Görl, J., and Kahmann, R. (1995b). Tagging pathogenicity genes in Ustilago maydis by restriction enzyme-mediated integration (REMI). Mol. Gen. Genet. 248: 547-552.
4. Bölker, M., Genin, S., Lehmler, C., and Kahmann, R. (1995a). Genetic regulation of mating, and dimorphism in Ustilago maydis. Can. J. Bot. 73: 320-325.
5. Bölker, M., Urban, M., and Kahmann, R. (1992). The a mating type locus of U. maydis specifies cell signaling components. Cell 68: 441-450.
6. 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.
7. Brefort, T., Doehlemann, G., Mendoza-Mendoza, A., Reissmann, S., Djamei, A., and Kahmann, R. (2009). Ustilago maydis as a pathogen. Annu. Rev. Phytopathol. 47: 423-445.
8. Breter, H.J., Ferguson, J., Peterson, T.A., and Reed, S.I. (1983). Isolation and transcriptional characterization of three genes which function at start, the controlling event of the Saccharomyces cerevisiae cell division cycle: CDC36, CDC37, and CDC39. Mol. Cell. Biol. 3: 881-891.
9. Brown, A.J., and Casselton, L.A. (2001). Mating in mushrooms: Increasing the chances but prolonging the affair. Trends Genet. 17: 393-400.
10. Day, P.R., Anagnostakis, S.L., and Puhalla, J.E. (1971). Pathogenicity resulting from mutation at the b locus of Ustilago maydis. Proc. Natl. Acad. Sci. USA 68: 533-535.
11. Di Stasio, M., Brefort, T., Mendoza-Mendoza, A., Munch, K., and Kahmann, R. (2009). The dual specificity phosphatase Rok1 negatively regulates mating and pathogenicity in Ustilago maydis. Mol. Microbiol. 73: 73-88.
12. Don, J., and Stelzer, G. (2002). The expanding family of CREB/CREM transcription factors that are involved with spermatogenesis. Mol. Cell. Endocrinol. 187: 115-124.
13. Eichhorn, H., Lessing, F., Winterberg, B., Schirawski, J., Kämper, J., Müller, P., and Kahmann, R. (2006). A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell 18: 3332-3345.
14. Ekena, J.L., Stanton, B.C., Schiebe-Owens, J.A., and Hull, C.M. (2008). Sexual development in Cryptococcus neoformans requires CLP1, a target of the homeodomain transcription factors Sxi1alpha and Sxi2a. Eukaryot. Cell 7: 49-57.
15. Ellenberger, T., Fass, D., Arnaud, M., and Harrison, S.C. (1994). Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Genes Dev. 8: 970-980.
16. Feldbrügge, M., Zarnack, K., Vollmeister, E., Baumann, S., Koepke, J., König, J., Münsterkötter, M., and Mannhaupt, G. (2008). The posttranscriptional machinery of Ustilago maydis. Fungal Genet. Biol. 45(Suppl 1): S40-S46.
17. Flor-Parra, I., Vranes, M., Kämper, J., and Perez-Martin, J. (2006). Biz1, a zinc finger protein required for plant invasion by Ustilago maydis, regulates the levels of a mitotic cyclin. Plant Cell 18: 2369-2387.
18. Foulkes, N.S., Mellstrom, B., Benusiglio, E., and Sassone-Corsi, P. (1992). Developmental switch of CREM function during spermatogenesis: from antagonist to activator. Nature 355: 80-84.
19. Garcia-Muse, T., Steinberg, G., and Perez-Martin, J. (2003). Pheromone-induced G2 arrest in the phytopathogenic fungus Ustilago maydis. Eukaryot. Cell 2: 494-500.
20. Grandel, A., Romeis, T., and Kämper, J. (2000). Regulation of pathogenic development in the corn smut fungus Ustilago maydis. Mol. Plant Pathol. 1: 61-66.
21. 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.
22. Hartwell, L.H., Culotti, J., and Reid, B. (1970). Genetic control of the cell-division cycle in yeast. I. Detection of mutants. Proc. Natl. Acad. Sci. USA 66: 352-359.
23. Heimel, K., Scherer, M., Vranes, M., Wahl, R., Pothiratana, C., Schuler, D., Vincon, V., Finkernagel, V., Flor-Parra, I., and Kämper, J. (2010). The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PLoS Pathog. 6: e1001035.
24. Ho, E.C., Cahill, M.J., and Saville, B.J. (2007). Gene discovery and transcript analyses in the corn smut pathogen Ustilago maydis: Expressed sequence tag and genome sequence comparison. BMC Genomics 8: 334.
25. Holliday, R. (1961). The genetics of Ustilago maydis. Genet. Res. Camb. 2: 204-230.
26. Hu, C.D., Chinenov, Y., and Kerppola, T.K. (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9: 789-798.
27. Hu, C.D., Grinberg, A.V., and Kerppola, T.K. (2006). Visualization of protein interactions in living cells using bimolecular fluorescence complementation (BiFC) analysis. In Current Protocols of Cell Biology, J.S. Bonifacino, M. Dasso, J.B. Harford, J. Lippincott-Schwartz, and K.M. Yamada, eds (New York: Wiley), Unit 21.3.
28. Hurst, H.C. (1995). Transcription factors 1: bZIP proteins. Protein Profile 2: 101-168.
29. Husberg, C., Murphy, P., Martin, E., and Kolsto, A.B. (2001). Two domains of the human bZIP transcription factor TCF11 are necessary for transactivation. J. Biol. Chem. 276: 17641-17652.
30. Inada, K., Morimoto, Y., Arima, T., Murata, Y., and Kamada, T. (2001). The clp1 gene of the mushroom Coprinus cinereus is essential for A-regulated sexual development. Genetics 157: 133-140.
31. Kaffarnik, F., Müller, P., Leibundgut, M., Kahmann, R., and Feldbrügge, M. (2003). PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J. 22: 5817-5826.
32. Kämper, J. (2004). A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol. Genet. Genomics 271: 103-110.
33. Kämper, J., et al. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
34. Kerppola, T.K. (2006). Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat. Protoc. 1: 1278-1286.
35. Kothe, E. (2001). Mating-type genes for basidiomycete strain improvement in mushroom farming. Appl. Microbiol. Biotechnol. 56: 602-612.
36. Kües, U. (2000). Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol. Mol. Biol. Rev. 64: 316-353.
37. Leong, D.T., Gupta, A., Bai, H.F., Wan, G., Yoong, L.F., Too, H.P., Chew, F.T., and Hutmacher, D.W. (2007). Absolute quantification of gene expression in biomaterials research using real-time PCR. Biomaterials 28: 203-210.
38. Li, C., and Wong, W.H. (2001). Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc. Natl. Acad. Sci. USA 98: 31-36.
39. Li, C., and Wong, W.H. (2003). DNA-chip analyzer (dChip). In The Analysis of Gene Expression Data: Methods and Software, G. Parmigiani, E.S. Garrett, R. Irizarry, and S.L. Zeger, eds (New York: Springer), pp. 120-141.
40. Luca, F.C., Mody, M., Kurischko, C., Roof, D.M., Giddings, T.H., and Winey, M. (2001). Saccharomyces cerevisiae Mob1p is required for cytokinesis and mitotic exit. Mol. Cell. Biol. 21: 6972-6983.
41. Luca, F.C., and Winey, M. (1998). MOB1, an essential yeast gene required for completion of mitosis and maintenance of ploidy. Mol. Biol. Cell 9: 29-46.
42. Maerz, S., Dettmann, A., Ziv, C., Liu, Y., Valerius, O., Yarden, O., and Seiler, S. (2009). Two NDR kinase-MOB complexes function as distinct modules during septum formation and tip extension in Neurospora crassa. Mol. Microbiol. 74: 707-723.
43. Mendoza-Mendoza, A., Eskova, A., Weise, C., Czajkowski, R., and Kahmann, R. (2009). Hap2 regulates the pheromone response transcription factor Prf1 in Ustilago maydis. Mol. Microbiol., in press.
44. Mielnichuk, N., Sgarlata, C., and Perez-Martin, J. (2009). A role for the DNA-damage checkpoint kinase Chk1 in the virulence program of the fungus Ustilago maydis. J. Cell Sci. 122: 4130-4140.
45. 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.
46. Müller, P., Leibbrandt, A., Teunissen, H., Cubasch, S., Aichinger, C., and Kahmann, R. (2004). The Gbeta-subunit-encoding gene bpp1 controls cyclic-AMP signaling in Ustilago maydis. Eukaryot. Cell 3: 806-814.
47. Müller, P., Weinzierl, G., Brachmann, A., Feldbrügge, M., and Kahmann, R. (2003). Mating and pathogenic development of the Smut fungus Ustilago maydis are regulated by one mitogen-activated protein kinase cascade. Eukaryot. Cell 2: 1187-1199.
48. Orlando, D.A., Lin, C.Y., Bernard, A., Wang, J.Y., Socolar, J.E., Iversen, E.S., Hartemink, A.J., and Haase, S.B. (2008). Global control of cell-cycle transcription by coupled CDK and network oscillators. Nature 453: 944-947.
49. Perez-Martin, J., Castillo-Lluva, S., Sgarlata, C., Flor-Parra, I., Mielnichuk, N., Torreblanca, J., and Carbo, N. (2006). Pathocycles: Ustilago maydis as a model to study the relationships between cell cycle and virulence in pathogenic fungi. Mol. Genet. Genomics 276: 211-229.
50. Puhalla, J.E. (1970). Genetic studies on the b incompatibility locus of Ustilago maydis. Genet. Res. Camb. 16: 229-232.
51. Quadbeck-Seeger, C., Wanner, G., Huber, S., Kahmann, R., and Kämper, J. (2000). A protein with similarity to the human retinoblastoma binding protein 2 acts specifically as a repressor for genes regulated by the b mating type locus in Ustilago maydis. Mol. Microbiol. 38: 154-166.
52. Raper, J.R. (1966). Genetics of Sexuality in Higher Fungi. (New York: The Ronald Press).
53. Reed, S.I. (1980). The selection of S. cerevisiae mutants defective in the start event of cell division. Genetics 95: 561-577.
54. Romeis, T., Kämper, J., and Kahmann, R. (1997). Single-chain fusions of two unrelated homeodomain proteins trigger pathogenicity in Ustilago maydis. Proc. Natl. Acad. Sci. USA 94: 1230-1234.
55. Rowell, J.B. (1955). Functional role of compatibility factors and an in vitro test for sexual incompatibility with haploid lines of Ustilago zea. Phytopathology 45: 370-374.
56. Rowell, J.B., and DeVay, J.E. (1954). Genetics of Ustilago zea in relation to basic problems of its pathogenicity. Phytopathology 44: 356-362.
57. Sambrook, J., Frisch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
58. Saunders, D.G., Aves, S.J., and Talbot, N.J. (2010). Cell cycle-mediated regulation of plant infection by the rice blast fungus. Plant Cell 22: 497-507.
59. Scherer, M., Heimel, K., Starke, V., and Kämper, J. (2006). The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18: 2388-2401.
60. Schultz, J., Milpetz, F., Bork, P., and Ponting, C.P. (1998). SMART, a simple modular architecture research tool: Identification of signaling domains. Proc. Natl. Acad. Sci. USA 95: 5857-5864.
61. 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.
62. Skibbe, D.S., Doehlemann, G., Fernandes, J., and Walbot, V. (2010). Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328: 89-92.
63. 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.
64. Song, Y., Cheon, S.A., Lee, K.E., Lee, S.Y., Lee, B.K., Oh, D.B., Kang, H.A., and Kim, J.Y. (2008). Role of the RAM network in cell polarity and hyphal morphogenesis in Candida albicans. Mol. Biol. Cell 19: 5456-5477.
65. Soulard, A., Lechler, T., Spiridonov, V., Shevchenko, A., Li, R., and Winsor, B. (2002). Saccharomyces cerevisiae Bzz1p is implicated with type I myosins in actin patch polarization and is able to recruit actin-polymerizing machinery in vitro. Mol. Cell. Biol. 22: 7889-7906.
66. Spellig, T., Bölker, M., Lottspeich, F., Frank, R.W., and Kahmann, R. (1994). Pheromones trigger filamentous growth in Ustilago maydis. EMBO J. 13: 1620-1627.
67. Swiezynski, K.M., and Day, P.R. (1960a). Migration of nuclei in Coprinus lagopus. Genet. Res. 1: 129-139.
68. Swiezynski, K.M., and Day, P.R. (1960b). Heterokaryon formation in Coprinus lagopus. Genet. Res. 1: 114-128.
69. Thomas, M.J., and Seto, E. (1999). Unlocking the mechanisms of transcription factor YY1: Are chromatin modifying enzymes the key? Gene 236: 197-208.
70. Toone, W.M., Johnson, A.L., Banks, G.R., Toyn, J.H., Stuart, D., Wittenberg, C., and Johnston, L.H. (1995). Rme1, a negative regulator of meiosis, is also a positive activator of G1 cyclin gene expression. EMBO J. 14: 5824-5832.
71. Urban, M., Kahmann, R., and Bölker, M. (1996). Identification of the pheromone response element in Ustilago maydis. Mol. Gen. Genet. 251: 31-37.
72. Wahl, R., Zahiri, A., and Kamper, J. (2010). The Ustilago maydis b mating type locus controls hyphal proliferation and expression of secreted virulence factors in planta. Mol. Microbiol. 75: 208-220.
73. Weiss, E.L., Kurischko, C., Zhang, C., Shokat, K., Drubin, D.G., and Luca, F.C. (2002). The Saccharomyces cerevisiae Mob2p-Cbk1p kinase complex promotes polarized growth and acts with the mitotic exit network to facilitate daughter cell-specific localization of Ace2p transcription factor. J. Cell Biol. 158: 885-900.
74. Zarnack, K., Eichhorn, H., Kahmann, R., and Feldbrügge, M. (2008). Pheromone-regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Mol. Microbiol. 69: 1041-1053.