The Ustilago maydis b mating type locus controls hyphal proliferation and expression of secreted virulence factors in planta

Molecular Microbiology

Volumn 75, Issue 1, 2010, Pages 208-220

  Wahl, Ramon ^a   Zahiri, Alexander ^a   Kämper, Jörg ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROLINE; SERINE; VIRULENCE FACTOR;

ALLELE; ARTICLE; CELL SYNCHRONIZATION; CONTROLLED STUDY; CYTOKINESIS; DNA DETERMINATION; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS HYPHAE; GENE CONTROL; GENE LOCUS; GENE MUTATION; MATING; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SEXUAL DEVELOPMENT; TEMPERATURE SENSITIVITY; USTILAGO MAYDIS;

AMINO ACID SUBSTITUTION; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENES, MATING TYPE, FUNGAL; HYPHAE; MUTATION, MISSENSE; PLANT DISEASES; USTILAGO; VIRULENCE FACTORS;

FUNGI; USTILAGO MAYDIS;

EID: 72949119538     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06984.x     Document Type: Article

References (49)

1. Banuett, F. 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. Bendtsen, J.D., Jensen, L.J., Blom, N., von Heijne, G. Brunak, S. (2004) Feature based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 17 : 349 356.
3. Birch, P.R., Rehmany, A.P., Pritchard, L., Kamoun, S. Beynon, J.L. (2006) Trafficking arms: oomycete effectors enter host plant cells. Trends Microbiol 14 : 8 11.
4. Bohlmann, R., Schauwecker, F., Basse, C. Kahmann, R. (1994) Genetic regulation of mating and dimorphism in Ustilago maydis. Adv Mol Genet Plant-Microbe Interact 3 : 239 245.
5. Bölker, M., Urban, M. Kahmann, R. (1992) The a mating type locus of U. maydis specifies cell signaling components. Cell 68 : 441 450.
6. Bölker, M., Genin, S., Lehmler, C. Kahmann, R. (1995) Genetic regulation of mating, and dimorphism in Ustilago maydis. Can J Bot 73 : 320 325.
7. Brachmann, A. (2001) Die frühe Infektionsphase von Ustilago Maydis: Genregulation durch das bE/bW Heterodimer. PhD Thesis. Munich: Ludwig-Maximilian-University.
8. Brachmann, A., Weinzierl, G., Kämper, J. Kahmann, R. (2001) Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42 : 1047 1063.
9. Brachmann, A., Schirawski, J., Müller, P. Kahmann, R. (2003) An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis. EMBO J 22 : 2199 2210.
10. Cánovas, D. Pérez-Martín, J. (2009) Sphingolipid biosynthesis is required for polar growth in the dimorphic phytopathogen Ustilago maydis. Fungal Genet Biol 46 : 190 200.
11. Catanzariti, A.M., Dodds, P.N., Lawrence, G.J., Ayliffe, M.A. Ellis, J.G. (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18 : 243 256.
12. Chisholm, S.T., Coaker, G., Day, B. Staskawicz, B.J. (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124 : 803 814.
13. Eichhorn, H., Lessing, F., Winterberg, B., Schirawski, J., Kämper, J., Müller, P. Kahmann, R. (2006) A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell 18 : 3332 3345.
14. Emanuelsson, O., Nielsen, H., Brunak, S. von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300 : 1005 1016.
15. Flor-Parra, I., Vranes, M., Kämper, J. Pérez-Martín, 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.
16. García-Muse, T., Steinberg, G. Pérez-Martín, J. (2003) Pheromone-induced G2 arrest in the phytopathogenic fungus Ustilago maydis. Eukaryot Cell 2 : 494 500.
17. Gillissen, B., Bergemann, J., Sandmann, C., Schroer, B., Bölker, M. Kahmann, R. (1992) A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68 : 647 657.
18. Goldberg, A.L. (2003) Protein degradation and protection against misfolded or damaged proteins [Review]. Nature 426 : 895 899.
19. Hartmann, H.A., Kahmann, R. 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. Kahmann, R. (1999) Environmental signals controlling sexual development of the corn Smut fungus Ustilago maydis through the transcriptional regulator Prf1. Plant Cell 11 : 1293 1306.
21. Holliday, R. (1974) Ustilago maydis. In Handbook of Genetics, Vol. 1. King, R.C. (ed.). New York : Plenum Press, pp. 575 595.
22. Kamoun, S. (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44 : 41 60.
23. Kamoun, S. (2007) Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol 10 : 358 365.
24. Kämper, J., Reichmann, M., Romeis, T., Bölker, M. Kahmann, R. (1995) Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81 : 73 83.
25. Kämper, J. (2004) A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol Genet Genomics 271 : 103 110.
26. Kämper, J., Kahmann, R., Bölker, M., Ma, L.J., Brefort, T., Saville, B.J., et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444 : 97 101.
27. Keon, J.P., White, G.A. Hargreaves, J.A. (1991) Isolation, characterization and sequence of a gene conferring resistance to the systemic fungicide carboxin from the maize smut pathogen, Ustilago maydis. Curr Genet 19 : 475 481.
28. Kronstad, J.W. (1997) Mating type in filamentous fungi. Annu Rev Genet 31 : 245 276.
29. Loubradou, G., Brachmann, A., Feldbrügge, M. Kahmann, R. (2001) A homologue of the transcriptional repressor Ssn6p antagonizes cAMP signalling in Ustilago maydis. Mol Microbiol 40 : 719 730.
30. Medicherla, B. Goldberg, A.L. (2008) Heat shock and oxygen radicals stimulate ubiquitin-dependent degradation mainly of newly synthesized proteins. J Cell Biol 182 : 663 673.
31. Morgan, W. Kamoun, S. (2007) RXLR effectors of plant pathogenic oomycetes. Curr Opin Microbiol 10 : 332 338.
32. Müller, O., Schreier, P.H. Uhrig, J.F. (2008) Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis. Mol Genet Genomics 279 : 27 39.
33. O'Connell, R.J. Panstruga, R. (2006) Tete a tete inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 171 : 699 718.
34. Quadbeck-Seeger, C., Wanner, G., Huber, S., Kahmann, R. 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.
35. Ridout, C.J., Skamnioti, P., Porritt, O., Sacristan, S., Jones, J.D. Brown, J.K. (2006) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18 : 2402 2414.
36. Romeis, T., Brachmann, A., Kahmann, R. Kämper, J. (2000) Identification of a target gene for the bE/bW homeodomain protein complex in Ustilago maydis. Mol Microbiol 37 : 54 66.
37. Sambrook, J., Frisch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbour, NY : Cold Spring Harbour Laboratory Press.
38. Schauwecker, F., Wanner, G. Kahmann, R. (1995) Filament-specific expression of a cellulase gene in the dimorphic fungus Ustilago maydis. Biol Chem Hoppe Seyler 376 : 617 625.
39. Scherer, M., Heimel, K., Starke, V. Kämper, J. (2006) The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18 : 2388 2401.
40. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schäfer, W., Martin, T., et al. (1990) The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60 : 295 306.
41. Snetselaar, K.M. Mims, C.W. (1992) Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia 84 : 193 203.
42. Spee, J.H., de Vos, W.M. Kuipers, O.P. (1993) Efficient random mutagenesis method with adjustable mutation frequency by use of PCR and dITP. Nucleic Acids Res 21 : 777 778.
43. Spellig, T., Bölker, M., Lottspeich, F., Frank, R.W. Kahmann, R. (1994) Pheromones trigger filamentous growth in Ustilago maydis. EMBO J 13 : 1620 1627.
44. Tsukuda, T., Carleton, S., Fotheringham, S. Holloman, W.K. (1988) Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol Cell Biol 8 : 3703 3709.
45. Urban, M., Kahmann, R. Bölker, M. (1996) Identification of the pheromone response element in Ustilago maydis. Mol General Genet 251 : 31 37.
46. Weinzierl, G. (2001) Isolierung und Charakterisierung von Komponenten der b-vermittelten Regulationskaskade in Ustilago maydis. Thesis, Philipps-University Marburg.
47. Wösten, H.A., Bohlmann, R., Eckerskorn, C., Lottspeich, F., Bölker, M. 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.
48. Zarnack, K., Eichhorn, H., Kahmann, R. Feldbrügge, M. (2008) Pheromone-regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Mol Microbiol 69 : 1041 1053.
49. Zheng, Y., Kief, J., Auffarth, K., Farfsing, J.W., Mahlert, M., Nieto, F. Basse, C.W. (2008) The Ustilago maydis Cys2His2-type zinc finger transcription factor Mzr1 regulates fungal gene expression during the biotrophic growth stage. Mol Microbiol 68 : 1450 1470.