The histone deacetylase Hda1 from Ustilago maydis is essential for teliospore development

Molecular Microbiology

Volumn 46, Issue 4, 2002, Pages 1169-1182

  Reichmann, Michael ^a,c   Jamnischek, Alexander ^b   Weinzierl, Gerhard ^b   Ladendorf, Oliver ^b   Huber, Sieglinde ^b   Kahmann, Regine ^b   Kämper, Jörg ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c Bayrische Landesanstalt für Bodenkunde und Pflanzenzüchtung ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE;

ARTICLE; BACTERIAL STRAIN; CELL PROLIFERATION; CONTROLLED STUDY; DEREGULATION; DEVELOPMENTAL STAGE; FUNGAL DEVELOPMENT; FUNGAL STRAIN; FUNGUS ISOLATION; GENE DELETION; MATING; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PATHOGENICITY; PRIORITY JOURNAL; PROBABILITY; PROTEIN EXPRESSION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SPOROGENESIS; TELIOSPORE; USTILAGO MAYDIS;

CLONING, MOLECULAR; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENETIC COMPLEMENTATION TEST; HISTONE DEACETYLASES; MACROMOLECULAR SUBSTANCES; MOLECULAR WEIGHT; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SPORES, FUNGAL; TRANSCRIPTION FACTORS; USTILAGO; ZEA MAYS;

BACTERIA (MICROORGANISMS); FUNGI; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; USTILAGO; USTILAGO MAYDIS; ZEA MAYS;

EID: 0036434908     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2002.03238.x     Document Type: Article

References (72)

1. Baidyaroy, D., Brosch, G., Ahn, J.H., Graessle, S., Wegener, S., Tonukari, N.J., et al. (2001) A gene related to yeast HOS2 histone deacetylase affects extracellular depolymerase expression and virulence in a plant pathogenic fungus. Plant Cell 13: 1609-1624.
2. Banuett, F. (1995) Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu Rev Genet 29: 179-208.
3. 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.
4. Banuett, F., and Herskowitz, I. (1996) Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122: 2965-2976.
5. Barrett, K.J., Gold, S.E., and Kronstad, J.W. (1993) Identification and complementation of a mutation to constitutive filamentous growth in Ustilago maydis. Mol Plant Microbe Interact 6: 274-283.
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. Bauchwitz, R., and Holloman, W.K. (1990) Isolation of the REC2 gene controlling recombination in Ustilago maydis. Gene 96: 285-288.
8. Bernstein, B.E., Tong, J.K., and Schreiber, S.L. (2000) Genomewide studies of histone deacetylase function in yeast. Proc Natl Acad Sci USA 97: 13708-13713.
9. Bohlmann, R. (1996) Isolierung und Charakterisierung von Filamentspezifisch Exprimierten Genen aus Ustilago maydis. PhD-thesis, Fakultät für Biologie, Ludwig-Maximilian-Universität, München.
10. Bohlmann, R., Schauwecker, F., Basse, C., and Kahmann, R. (1994) Genetic regulation of mating and dimorphism in Ustilago maydis. In Advances in Molecular Genetics of Plant-Microbe Interactions, Vol. 3. Daniels, M.J., (ed.) Dordrecht: Kluwer Academic Publishers, pp. 239-245.
11. Bölker, M., Urban, M., and Kahmann, R. (1992) The a mating type locus of Ustilago maydis specifies cell signaling components. Cell 68: 441-450.
12. Brachmann, A. (2001) Die Frühe Infektionsphase von Ustilago maydis: Genregulation durch das bE/bW-Heterodimer. PhD-thesis, Faculty for Biology, Ludwig-Maximilian-University, Munich.
13. 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.
14. Burke, D., Dawson, D., and Stearns, T. (2000) Methods in Yeast Genetics. Cold Spring Harbour: Cold Spring Harbour Laboratory Press.
15. Clancy, M.J. (1998) Meiosis: Step-by-step through sporulation. Curr Biol 8: R461-R463.
16. Dürrenberger, F., Wong, K., and Kronstad, J.W. (1998) Identification of a cAMP-dependent protein kinase catalytic subunit required for virulence and morphogenesis in Ustilago maydis. Proc Natl Acad Sci USA 95: 5684-5689.
17. Dürrenberger, F., Laidlaw, R.D., and Kronstad, J.W. (2001) The hgl1 gene is required for dimorphism and teliospore formation in the fungal pathogen Ustilago maydis. Mol Microbiol 41: 337-348.
18. Gold, S., Duncan, G., Barrett, K., and Kronstad, J. (1994) cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev 8: 2805-2816.
19. Gold, S.E., Brogdon, S.M., Mayorga, M.E., and Kronstad, J.W. (1997) The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. Plant Cell 9: 1585-1594.
20. Graessle, S., Loidl, P., and Brosch, G. (2001) Histone acetylation: Plants and fungi as model systems for the investigation of histone deacetylases. Cell Mol Life Sci 58: 704-720.
21. Grunstein, M. (1997) Histone acetylation in chromatin structure and transcription. Nature 389: 349-352.
22. 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.
23. Hassig, C.A., Tong, J.K., Fleischer, T.C., Owa, T., Grable, P.G., Ayer, D.E., and Schreiber, S.L. (1998) A role for histone deacetylase activity in HDAC1-mediated transcriptional repression. Proc Natl Acad Sci USA 95: 3519-3524.
24. 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.
25. Holliday, R. (1961) Induced mitotic crossing-over in Ustilago maydis. Genet Res Camb 2: 231-248.
26. Holliday, R. (1974) Ustilago maydis. In Handbook of Genetics, Vol. 1 King, R.C., (ed.). New York, USA: Plenum Press, pp. 575-595.
27. Hong, L., Schroth, G.P., Matthews, H.R., Yau, P., and Bradbury, E.M. (1993) Studies of the DNA binding properties of histone H4 amino terminus. Thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 'tail' to DNA. J Biol Chem 268: 305-314.
28. Huber, S.M.F.E., Lottspeich, F., and Kämper, J. (2002) A gene with similarity to dioxygenases is specifically expressed in teliospores of Ustilago maydis. Mol Gen Genom 267:757-771.
29. Johnson, C.A., and Turner, B.M. (1999) Histone deacetylases: Complex transducers of nuclear signals. Semin Cell Dev Biol 10: 179-188.
30. Kadosh, D., and Struhl, K. (1998a) Histone deacetylase activity of Rpd3 is important for transcriptional repression in vivo. Genes Dev 12: 797-805.
31. Kadosh, D., and Struhl, K. (1998b) Targeted recruitment of the Sin3-Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo. Mol Cell Biol 18: 5121-5127.
32. Kahmann, R., Steinberg, G., Basse, C., and Kämper, J., (eds). (2000) Ustilago Maydis, the Causative Agent of Corn Smut Disease. Dodrecht: Kluwer Academic Publishers.
33. 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.
34. Keon, J.P., White, G.A., and 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.
35. Keon, J.P., Broomfield, P.L., White, G.A., and Hargreaves, J.A. (1994) A mutant form of the succinate dehydrogenase iron-sulphur protein subunit confers resistance to carboxin in the maize smut pathogen Ustilago maydis. Biochem Soc Trans 22: 234-237.
36. +, a histone deacetylase gene ofSchizosaccharomyces pombe, is required for the meiotic cell cycle and resistance to trichostatin A. FEBS Lett 436: 193-196.
37. 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.
38. Krüger, J., Loubradou, G., Wanner, G., Regenfelder, E., Feldbürgge, M., and Kahmann, R. (2000) Activation of the cAMP pathway in Ustilago maydis reduces fungal proliferation and teliospore formation in plant tumors. Mol Plant Microbe Interact 13: 1034-1040.
39. Lamb, T.M., and Mitchell, A.P. (2001) Coupling of Saccharomyces cerevisiae early meiotic gene expression to DNA replication depends upon RPD3 and SIN3. Genetics 157: 545-556.
40. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
41. Luger, K., and Richmond, T.J. (1998) The histone tails of the nucleosome. Curr Opin Genet Dev 8: 140-146.
42. Minucci, S., and Pelicci, P.G. (1999) Retinoid receptors in health and disease: Co-regulators and the chromatin connection. Semin Cell Dev Biol 10: 215-225.
43. Mumberg, D., Müller, R., and Funk, M. (1994) Regulatable promoters of Saccharomyces cerevisiae: Comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res 22: 5767-5768.
44. Mumberg, D., Müller, R., and Funk, M. (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156: 119-122.
45. Pazin, M.J., and Kadonaga, J.T. (1997) What's up and down with histone deacetylation and transcription? Cell 89: 325-328.
46. Perez-Martin, J., and Johnson, A.D. (1998) Mutations in chromatin components suppress a defect of Gcn5 protein in Saccharomyces cerevisiae. Mol Cell Biol 18: 1049-1054.
47. 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.
48. Regenfelder, E., Spellig, T., Hartmann, A., Lauenstein, S., Bolker, M., and Kahmann, R. (1997) G proteins in Ustilago maydis: Transmission of multiple signals? EMBO J 16: 1934-1942.
49. Reinke, H., Gregory, P.D., and Hörz, W. (2001) A transient histone hyperacetylation signal marks nucleosomes for remodeling at the PHO8 promoter in vivo. Mol Cell 7: 529-538.
50. Romeis, T., Brachmann, A., Kahmann, R., and Kämper, J. (2000) Identification of a target gene for the bE/bW homeodomain protein complex in Ustilago maydis. Mol Microbiol 37: 54-66.
51. Rossi, V., Hartings, H., and Motto, M. (1998) Identification and characterisation of an RPD3 homologue from maize (Zea mays L.) that is able to complement an rpd3 null mutant of Saccharomyces cerevisiae. Mol Gen Genet 258: 288-296.
52. Rundlett, S.E., Carmen, A.A., Suka, N., Turner, B.M., and Grunstein, M. (1998) Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3. Nature 392: 831-835.
53. Sambrook, J., Frisch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
54. 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.
55. Schiestl, R.H., and Gietz, R.D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet 16: 339-346.
56. 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.
57. 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.
58. Snetselaar, K.M., and Mims, C.W. (1994) Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol Res 98: 347-355.
59. 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.
60. Spellig, T., Bottin, A., and Kahmann, R. (1996) Green fluo-rescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol Gen Genet 252: 503-509.
61. Srikantha, T., Tsai, L., Daniels, K., Klar, A.J., and Soll, D.R. (2001) The histone deacetylase genes HDA1 and RPD3 play distinct roles in regulation of high-frequency phenotypic switching in Candida albicans. J Bacteriol 183: 4614-4625.
62. Struhl, K. (1998) Histone acetylation and transcriptional regulatory mechanisms. Genes Dev 12: 599-606.
63. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997) The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
64. Torreblanca, J., Stumpferl, S., and Basse, C. (2002) Histone deacetylase Hda1 acts as a repressor of the Ustilago maydis biotrophic marker gene Mig1. Fungal Genet Biol (in press).
65. Urban, M., Kahmann, R., and Bölker, M. (1996a) The biallelic a mating type locus of Ustilago maydis: Remnants of an additional pheromone gene indicate evolution from a multiallelic ancestor. Mol Gen Genet 250: 414-420.
66. Urban, M., Kahmann, R., and Bölker, M. (1996b) Identification of the pheromone response element in Ustilago maydis. Mol Gen Genet 251: 31-37.
67. Verdone, L., Wu, J., van Riper, K., Kacherovsky, N., Vogelauer, M., Young, E.T., et al. (2002) Hyperacetylation of chromatin at the ADH2 promoter allows Adr1 to bind in repressed conditions. EMBO J 21: 1101-1111.
68. Vidal, M., and Gaber, R.F. (1991) RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae. Mol Cell Biol 11: 6317-6327.
69. Wade, P.A., Pruss, D., and Wolffe, A.P. (1997) Histone acetylation: Chromatin in action. Trends Biochem Sci 22: 128-132.
70. 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.
71. Yang, M.M., Inouye, C., Zeng, Y., Bearss, D., and Seto, E. (1996) Transcriptional repression by YY1 is mediated by interaction with a mammalian homolog of the yeast global regulator RPD3. Proc Natl Acad Sci USA 93: 12845-12850.
72. Zhang, Y., LeRoy, G., Seelig, H.P., Lane, W.S., and Reinberg, D. (1998) The dermatomyositis-specific auto-antigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95: 279-289.