Functional characterization of a seven-WD40 repeat protein Rak1 in Ustilago maydis

In dem pflanzenpathogenen Brandpilz Ustilago maydis wird die Paarungsreaktion zweier kompatibler Zellen durch ein Pheromon/Rezeptor System koordiniert. Der Pheromon Stimulus wird dabei über ein konserviertes MAP Kinase Modul übermittelt was zur Aktivierung von Prf1 führt, einem essentiellen Regul...

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1. Verfasser: Wang, Lei
Beteiligte: Kahmann, Regine (Prof. Dr. ) (BetreuerIn (Doktorarbeit))
Format: Dissertation
Sprache:Englisch
Veröffentlicht: Philipps-Universität Marburg 2011
Biologie
Ausgabe:http://dx.doi.org/10.17192/z2011.0115
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1. http://archiv.ub.uni-marburg.de/diss/z2007/0540


2. Arnold, K., Bordoli, L., Kopp, J. and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics, 22, 195-201.


3. Hermanto, U., Zong, C.S., Li, W.Q. and Wang, L.W. (2002) RACK1, an insulin-like growth factor I (IGF-I) receptor-interacting protein, modulates IGF-I-dependent integrin signaling and promotes cell spreading and contact extracellular matrix. Mol Cell Biol, 22, 2345-2365.


4. Garcia-Muse, T., Steinberg, G. and Perez-Martin, J. (2003) Pheromone-induced G 2 arrest in the phytopathogenic fungus Ustilago maydis. Eukaryot Cell, 2, 494- 500.


5. Kiely, P.A., O'Gorman, D., Luong, K., Ron, D. and O'Connor, R. (2006) Insulin-like growth factor I controls a mutually exclusive association of RACK1 with protein phosphatase 2A and beta 1 integrin to promote cell migration. Mol Cell Biol, 26, 4041-4051.


6. Martinez-Espinoza, A.D., Garcia-Pedrajas, M.D. and Gold, S.E. (2002) The Ustilaginales as plant pests and model systems. Fungal Genet Biol, 35, 1-20.


7. Kamper, J. (2004) A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol Genet Genomics, 271, 103-110. References 80


8. Brachmann, A., Konig, J., Julius, C. and Feldbrugge, M. (2004) A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics, 272, 216-226. References 77


9. 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.


10. Kamper, J., Reichmann, M., Romeis, T., Bolker, M. and Kahmann, R. (1995) Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell, 81, 73-83.


11. Steinberg, G. and Perez-Martin, J. (2008) Ustilago maydis, a new fungal model system for cell biology. Trends Cell Biol, 18, 61-67.


12. Liu, X., Nie, X., Ding, Y. and Chen, J. (2010) Asc1, a WD-repeat protein, is required for hyphal development and virulence in Candida albicans. Acta Biochim Biophys Sin, 42, 793-800.


13. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M., Tetko, I., Guldener, U., Mannhaupt, G., Munsterkotter, M. and Mewes, H.W. (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res, 32, 5539-5545.


14. Guo, J.J., Wang, S.C., Wang, J.B., Huang, W.D., Liang, J.S. and Chen, J.G. (2009) Dissection of the relationship between RACK1 and heterotrimeric G-proteins in Arabidopsis. Plant Cell Physiol, 50, 1681-1694.


15. Kronstad, J.W. and Leong, S.A. (1990) The b-mating-type locus of Ustilago maydis contains variable and constant regions. Genes Dev, 4, 1384-1395.


16. Gold, S., Duncan, G., Barrett, K. and Kronstad, J. (1994) cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev, 8, 2805- 2816.


17. 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.


18. Jorgensen, P., Nishikawa, J.L., Breitkreutz, B.-J. and Tyers, M. (2002) Systematic identification of pathways that couple cell growth and division in yeast. Science, 297, 395-400.


19. Steele, M.R., McCahill, A., Thompson, D.S., MacKenzie, C., Isaacs, N.W., Houslay, M.D. and Bolger, G.B. (2001) Identification of a surface on the beta-propeller protein RACK1 that interacts with the cAMP-specific phosphodiesterase PDE4D5. Cell Signal, 13, 507-513.


20. Banuett, F. and Herskowitz, I. (1994) 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.


21. Ceci, M., Gaviraghi, C., Gorrini, C., Sala, L.A., Offenhauser, N., Marchisio, P.C. and Biffo, S. (2003) Release of eIF6 (p27(BBP)) from the 60S subunit allows 80S ribosome assembly. Nature, 426, 579-584.


22. Armache, J.P., Jarasch, A., Anger, A.M., Villa, E., Becker, T., Bhushan, S., Jossinet, F., Habeck, M., Dindar, G., Franckenberg, S., Marquez, V., Mielke, T., Thomm, M., Berninghausen, O., Beatrix, B., Soding, J., Westhof, E., Wilson, D.N. and Beckmann, R. (2010) Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-angstrom resolution. Proc Natl Acad Sci U S A, 107, 19748-19753.


23. Berndt, P., Lanver, D. and Kahmann, R. (2010) The AGC Ser/Thr kinase Aga1 is essential for appressorium formation and maintenance of the actin cytoskeleton in the smut fungus Ustilago maydis. Mol Microbiol, 78, 1484-1499.


24. Yaka, R., Thornton, C., Vagts, A.J., Phamluong, K., Bonci, A. and Ron, D. (2002) NMDA receptor function is regulated by the inhibitory scaffolding protein, RACK1. Proc Natl Acad Sci U S A, 99, 5710-5715.


25. Sambrook, J., Fritsch, E.F. and Maniatis., T. (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, USA. References 84


26. Paul, S.K., Oowatari, Y. and Kawamukai, M. (2009) A large complex mediated by Moc1, Moc2 and Cpc2 regulates sexual differentiation in fission yeast. FEBS J, 276, 5076-5093.


27. 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. References 82


28. Molina, L. and Kahmann, R. (2007) An Ustilago maydis gene involved in H 2 O 2 detoxification is required for virulence. Plant Cell, 19, 2293-2309.


29. Kim, S.W., Joo, Y.J. and Kim, J. (2010) Asc1p, a ribosomal protein, plays a pivotal role in cellular adhesion and virulence in Candida albicans. Journal of Microbiology, 48, 842-848.


30. Gillissen, B., Bergemann, J., Sandmann, C., Schroeer, B., Bolker, M. and Kahmann, R. (1992) A two component regulatory system for self non-self recognition in Ustilago maydis. Cell, 68, 647-657.


31. Egan, J.D., Garcia-Pedrajas, M.D., Andrews, D.L. and Gold, S.E. (2009) Calcineurin is an antagonist to PKA protein phosphorylation required for postmating References 78 filamentation and virulence, while PP2A is required for viability in Ustilago maydis. Mol Plant-Microbe Interact, 22, 1293-1301.


32. Hoffmann, B., Wanke, C., LaPaglia, S.K. and Braus, G.H. (2000) c-Jun and RACK1 homologues regulate a control point for sexual development in Aspergillus nidulans. Mol Microbiol, 37, 28-41.


33. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Stat. Methodol, 57, 289-300.


34. Ron, D., Jiang, Z., Yao, L.N., Vagts, A., Diamond, I. and Gordon, A. (1999) Coordinated movement of RACK1 with activated beta IIPKC. J Biol Chem, 274, 27039-27046.


35. Shor, B., Calaycay, J., Rushbrook, J. and McLeod, M. (2003) Cpc2/RACK1 is a ribosome-associated protein that promotes efficient translation in Schizosaccharomyces pombe. J Biol Chem, 278, 49119-49128.


36. Kruger, 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.


37. Link, A.J., Eng, J., Schieltz, D.M., Carmack, E., Mize, G.J., Morris, D.R., Garvik, B.M. and Yates, J.R. (1999) Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol, 17, 676-682.


38. Hanahan, D. (1985) DNA Cloning: A Practical Approach (Glover, D.M., ed.). IRL Press, McLean, Virginia.


39. Pass, J.M., Gao, J.M., Jones, W.K., Wead, W.B., Wu, X., Zhang, J., Baines, C.P., Bolli, R., Zheng, Y.T., Joshua, I.G. and Ping, P.P. (2001) Enhanced PKC beta II References 83 translocation and PKC beta II-RACK1 interactions in PKC epsilon-induced heart failure: a role for RACK1. Am J Physiol Heart Circ Physiol, 281, H2500- H2510.


40. Klosterman, S.J., Perlin, M.H., Garcia-Pedrajas, M., Covert, S.F. and Gold, S.E. (2007) Genetics of morphogenesis and pathogenic development of Ustilago maydis. Fungal Genomics, 57, 1-47.


41. Banuett, F. (1995) Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu Rev Genet, 29, 179-208.


42. Palmer, D.A., Thompson, J.K., Li, L., Prat, A. and Wang, P. (2006) Gib2, a novel G - like/RACK1 homolog, functions as a G subunit in cAMP signaling and is essential in Cryptococcus neoformans. J Biol Chem, 281, 32596-32605.


43. 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.


44. 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.


45. Mendoza-Mendoza, A., Eskova, A., Weise, C., Czajkowski, R. and Kahmann, R. (2009b) Hap2 regulates the pheromone response transcription factor prf1 in Ustilago maydis. Mol Microbiol, 72, 683-698.


46. Laity, C., Giasson, L., Campbell, R. and Kronstad, J. (1995) Heterozygosity at the b- mating-type locus attenuates fusion in Ustilago maydis. Curr Genet, 27, 451- 459.


47. Durrenberger, 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 U S A, 95, 5684-5689.


48. Brachmann, A., Weinzierl, G., Kamper, J. and Kahmann, R. (2001) Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol, 42, 1047-1063.


49. Urban, M., Kahmann, R. and Bolker, M. (1996) Identification of the pheromone response element in Ustilago maydis. Mol Gen Genet, 251, 31-37.


50. Sengupta, J., Nilsson, J., Gursky, R., Spahn, C.M.T., Nissen, P. and Frank, J. (2004) Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM. Nat Struct Mol Biol, 11, 957-962.


51. 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.


52. Bottin, A., Kamper, J. and Kahmann, R. (1996) Isolation of a carbon source-regulated gene from Ustilago maydis. Mol Gen Genet, 253, 342-352.


53. Burke, D., Dawson, D. and Stearns, T. (2000) Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor Laboratory Press, New York.


54. Liu, Q.H. and Hofmann, P.A. (2003) Modulation of protein phosphatase 2a by adenosine A(1) receptors in cardiomyocytes: role for p38 MAPK. American Journal of Physiology-Heart and Circulatory Physiology, 285, H97-H103.


55. Zarnack, K., Eichhorn, H., Kahmann, R. and Feldbrugge, M. (2008) Pheromone- regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Mol Microbiol, 69, 1041-1053.


56. Mendoza-Mendoza, A., Berndt, P., Djamei, A., Weise, C., Linne, U., Marahiel, M., Vranes, M., Kamper, J. and Kahmann, R. (2009a) Physical-chemical plant- derived signals induce differentiation in Ustilago maydis. Mol Microbiol, 71, 895-911.


57. Rosdahl, J.A., Mourton, T.L. and Brady-Kalnay, S.M. (2002) Protein kinase C delta (PKC delta) is required for protein tyrosine phosphatase mu (PTP mu)- dependent neurite outgrowth. Mol Cell Neurosci, 19, 292-306.


58. Rodriguez, M.M., Ron, D., Touhara, K., Chen, C.H. and Mochly-Rosen, D. (1999) RACK1, a protein kinase C anchoring protein, coordinates the binding of activated protein kinase C and select pleckstrin homology domains in vitro. Biochemistry, 38, 13787-13794.


59. Koehler, J.A. and Moran, M.F. (2001) RACK1, a protein kinase C scaffolding protein, interacts with the PH domain of p120(GAP). Biochem Biophys Res Commun, 283, 888-895.


60. Chang, B.Y., Conroy, K.B., Machleder, E.M. and Cartwright, C.A. (1998) RACK1, a receptor for activated C kinase and a homolog of the beta subunit of G proteins, inhibits activity of Src tyrosine kinases and growth of NIH 3T3 cells. Mol Cell Biol, 18, 3245-3256.


61. Liliental, J. and Chang, D.D. (1998) Rack1, a receptor for activated protein kinase C, interacts with integrin beta subunit. J Biol Chem, 273, 2379-2383.


62. Onishi, I., Lin, P.J.C., Diering, G.H., Williams, W.P. and Numata, M. (2007) RACK1 associates with NHE5 in focal adhesions and positively regulates the transporter activity. Cell Signal, 19, 194-203.


63. Okano, K., Schnaper, H.W., Bomsztyk, K. and Hayashida, T. (2006) RACK1 binds to Smad3 to modulate transforming growth factor-beta 1-stimulated alpha 2(I) collagen transcription in renal tubular epithelial cells. J Biol Chem, 281, 26196- 26204.


64. Liu, Y.V., Baek, J.H., Zhang, H., Diez, R., Cole, R.N. and Semenza, G.L. (2007) RACK1 competes with HSP90 for binding to HIF-1 alpha and is required for O- 2-independent and HSP90 inhibitor-induced degradation of HIF-1 alpha. Mol Cell, 25, 207-217.


65. Mamidipudi, V. and Cartwright, C. (2006) Rack1 induces apoptosis of human colon cells by suppressing SRC tyrosine kinase activity in the intrinsic and Akt pathways. Gastroenterology, 130, A131-A131.


66. Isacson, C.K., Lu, Q., Karas, R.H. and Cox, D.H. (2007) RACK1 is a BKCa channel binding protein. Am J Physiol Cell Physiol, 292, C1459-C1466.


67. Chen, S.H., Dell, E.J., Lin, F., Sai, J.Q. and Hamm, H.E. (2004) RACK1 regulates specific functions of G beta gamma. J Biol Chem, 279, 17861-17868.


68. Vomastek, T., Iwanicki, M.P., Schaeffer, H.J., Tarcsafalvi, A., Parsons, J.T. and Weber, M.J. (2007) RACK1 targets the extracellular signal-regulated kinase/mitogen- activated protein kinase pathway to link integrin engagement with focal adhesion disassembly and cell motility. Mol Cell Biol, 27, 8296-8305.


69. Xu, Y.Z., Wang, N.F., Ling, F., Li, P.Z. and Gao, Y. (2009) Receptor for activated C- kinase 1, a novel binding partner of adiponectin receptor 1. Biochem Biophys Res Commun, 378, 95-98.


70. Ikebuchi, Y., Takada, T., Ito, K., Yoshikado, T., Anzai, N., Kanai, Y. and Suzuki, H. (2009) Receptor for activated C-kinase 1 regulates the cellular localization and function of ABCB4. Hepatol Res, 39, 1091-1107.


71. Croze, E., Usacheva, A., Asarnow, D., Minshall, R.D., Perez, H.D. and Colamonici, O. (2000) Receptor for activated C-kinase (RACK-1), a WD motif-containing protein, specifically associates with the human type IIFN receptor. J Immunol, 165, 5127-5132.


72. Lopez-Bergami, P., Habelhah, H., Bhoumik, A., Zhang, W.Z., Wang, L.H. and Ronai, Z. (2005) Receptor for RACK1 mediates activation of JNK by protein kinase C. Mol Cell, 19, 578-579.


73. Ludin, K., Hilti, N. and Schweingruber, M. (1995) Schizosaccharomyces pombe rds1, an adenine-repressible gene regulated by glucose, ammonium, phosphate, carbon dioxide and temperature. Molecular and General Genetics MGG, 248, 439-445.


74. Herzog, F., Primorac, I., Dube, P., Lenart, P., Sander, B., Mechtler, K., Stark, H. and Peters, J.-M. (2009) Structure of the anaphase-promoting complex/cyclosome interacting with a mitoticcheckpoint complex. Science, 323, 1477-1481.


75. Halic, M., Becker, T., Pool, M.R., Spahn, C.M.T., Grassucci, R.A., Frank, J. and Beckmann, R. (2004) Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature, 427, 808-814.


76. Supplementary data


77. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schafer, 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.


78. Müller, F., Krüger, D., Sattlegger, E., Hoffmann, B., Ballario, P., Kanaan, M. and Barthelmess, I. (1995) The cpc-2 gene of Neurospora crassa encodes a protein entirely composed of WD-repeat segments that is involved in general amino acid control and female fertility. Molecular and General Genetics MGG, 248, 162- 173.


79. Garrido, E. and Perez-Martin, 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.


80. Data CD: The data CD contains the following two files: Supplementary Table 1 Functional enrichment of genes up-regulated in FB1Δrak1.


81. 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.


82. Durrenberger, 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.


83. Garrido, E., Voss, U., Muller, P., Castillo-Lluva, S., Kahmann, R. and Perez-Martin, 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.


84. Chang, B.Y., Chiang, M.L. and Cartwright, C.A. (2001) The interaction of Src and RACK1 is enhanced by activation of protein kinase C and tyrosine phosphorylation of RACK1. J Biol Chem, 276, 20346-20356.


85. Muller, P., Aichinger, C., Feldbrugge, M. and Kahmann, R. (1999) The MAP kinase Kpp2 regulates mating and pathogenic development in Ustilago maydis. Mol Microbiol, 34, 1007-1017.


86. Rothberg, K.G., Burdette, D.L., Pfannstiel, J., Jetton, N., Singh, R. and Ruben, L. (2006) The RACK1 homologue from Trypanosoma brucei is required for the onset and progression of cytokinesis. J Biol Chem, 281, 9781-9790.


87. Zeller, C.E., Parnell, S.C. and Dohlman, H.G. (2007) The RACK1 ortholog Asc1 functions as a G-protein subunit coupled to glucose responsiveness in yeast. J Biol Chem, 282, 25168-25176.


88. McCahill, A., Warwicker, J., Bolger, G.B., Houslay, M.D. and Yarwood, S.J. (2002) The RACK1 scaffold protein: A dynamic cog in cell response mechanisms. Mol Pharmacol, 62, 1261-1273.


89. Regmi, S., Rothberg, K.G., Hubbard, J.G. and Ruben, L. (2008) The RACK1 signal anchor protein from Trypanosoma brucei associates with eukaryotic elongation factor 1A: a role for translational control in cytokinesis. Mol Microbiol, 70, 724- 745.


90. Yarwood, S.J., Steele, M.R., Scotland, G., Houslay, M.D. and Bolger, G.B. (1999) The RACK1 signaling scaffold protein selectively interacts with the cAMP-specific phosphodiesterase PDE4D5 isoform. J Biol Chem, 274, 14909-14917.


91. Rigas, A.C., Ozanne, D.M., Neal, D.E. and Robson, C.N. (2003) The scaffolding protein RACK1 interacts with androgen receptor and promotes cross-talk through a protein kinase C signaling pathway. J Biol Chem, 278, 46087-46093.


92. Dell, E.J., Connor, J., Chen, S., Stebbins, E.G., Skiba, N.P., Mochly-Rosen, D. and Hamm, H.E. (2002) The subunit of heterotrimeric G proteins interacts with RACK1 and two other WD repeat proteins. J Biol Chem, 277, 49888-49895.


93. Heimel, K., Scherer, M., Vranes, M., Wahl, R., Pothiratana, C., Schuler, D., Vincon, V., Finkernagel, F., Flor-Parra, I. and Kamper, J. (2010b) The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PLoS Pathog, 6, e1001035.


94. Mayorga, M.E. and Gold, S.E. (2001) The ubc2 gene of Ustilago maydis encodes a putative novel adaptor protein required for filamentous growth, pheromone response and virulence. Mol Microbiol, 41, 1365-1379.


95. Abramovitch, R.B., Yang, G. and Kronstad, J.W. (2002) The ukb1 gene encodes a putative protein kinase required for bud site selection and pathogenicity in Ustilago maydis. Fungal Genet Biol, 37, 98-108.


96. Khrunyk, Y., Munch, K., Schipper, K., Lupas, A.N. and Kahmann, R. (2010) The use of FLP-mediated recombination for the functional analysis of an effector gene family in the biotrophic smut fungus Ustilago maydis. New Phytol, 187, 957- 968.


97. 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.


98. Zahiri, A., Heimel, K., Wahl, R., Rath, M. and Kamper, J. (2010) The Ustilago maydis forkhead transcription factor Fox1 is involved in the regulation of genes required for the attenuation of plant defenses during pathogenic development. Mol Plant- Microbe Interact, 23, 1118-1129.


99. 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.


100. 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.


101. Usacheva, A., Tian, X.Y., Sandoval, R., Salvi, D., Levy, D. and Colamonici, O.R. (2003) The WD motif-containing protein RACK-1 functions as a scaffold protein within the type IIFN receptor-signalling complex. J Immunol, 171, 2989- 2994.


102. Hoffmann, B., Mosch, H.U., Sattlegger, E., Barthelmess, I.B., Hinnebusch, A. and Braus, G.H. (1999) The WD protein Cpc2p is required for repression of Gcn4 protein activity in yeast in the absence of amino-acid starvation. Mol Microbiol, 31, 807-822.


103. Klosterman, S.J., Martinez-Espinoza, A.D., Andrews, D.L., Seay, J.R. and Gold, S.E. (2008) Ubc2, an ortholog of the yeast Ste50p adaptor, possesses a basidiomycete-specific carboxy terminal extension essential for pathogenicity independent of pheromone response. Mol Plant-Microbe Interact, 21, 110-121.


104. 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.


105. Bolker, M. (2001) Ustilago maydis -a valuable model system for the study of fungal dimorphism and virulence. Microbiology, 147, 1395-1401.


106. Kahmann, R. and Kamper, J. (2004) Ustilago maydis: how its biology relates to pathogenic development. New Phytol, 164, 31-42.


107. Gerbasi, V.R., Weaver, C.M., Hill, S., Friedman, D.B. and Link, A.J. (2004) Yeast Asc1p and mammalian RACK1 are functionally orthologous core 40S ribosomal proteins that repress gene expression. Mol Cell Biol, 24, 8276-8287.


108. Ikner, A. and Shiozaki, K. (2005) Yeast signaling pathways in the oxidative stress response. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, 569, 13-27.


109. Weinzierl, G., Leveleki, L., Hassel, A., Kost, G., Wanner, G. and Bolker, M. (2002) Regulation of cell separation in the dimorphic fungus Ustilago maydis. Mol Microbiol, 45, 219-231. References 85


110. Kuroha, K., Akamatsu, M., Dimitrova, L., Ito, T., Kato, Y., Shirahige, K. and Inada, T. (2010) Receptor for activated C kinase 1 stimulates nascent polypeptide- dependent translation arrest. EMBO Rep, 11, 956-961. References 81


111. Lesage, G., Shapiro, J., Specht, C.A., Sdicu, A.M., Menard, P., Hussein, S., Tong, A.H.Y., Boone, C. and Bussey, H. (2005) An interactional network of genes involved in chitin synthesis in Saccharomyces cerevisiae. BMC Genet, 6, -.


112. Ron, D., Chen, C.H., Caldwell, J., Jamieson, L., Orr, E. and Mochlyrosen, D. (1994) Cloning of an intracellular receptor for protein kinase C: A homolog of the subunit of G proteins. Proc Natl Acad Sci U S A, 91, 839-843.


113. Holliday, R. (1974) Molecular aspects of genetic exchange and gene conversion. Genetics, 78, 273-287.


114. Baum, S., Bittins, M., Frey, S. and Seedorf, M. (2004) Asc1p, a WD40-domain containing adaptor protein, is required for the interaction of the RNA-binding protein Scp160p with polysomes. Biochem J, 380, 823-830.


115. Silverstein, A.M., Barrow, C.A., Davis, A.J. and Mumby, M.C. (2002) Actions of PP2A on the MAP kinase pathway and apoptosis are mediated by distinct regulatory subunits. Proc Natl Acad Sci U S A, 99, 4221-4226.


116. Nilsson, J., Sengupta, J., Frank, J. and Nissen, P. (2004) Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep, 5, 1137-1141.


117. Zhang, W.Z., Zong, C.S., Hermanto, U., Lopez-Bergami, P., Ronai, Z. and Wang, L.H. (2006) RACK1 recruits STAT3 specifically to insulin and insulin-like growth factor 1 receptors for activation, which is important for regulating anchorage- independent growth. Mol Cell Biol, 26, 413-424. Supplementary data 86


118. Letourneux, C., Rocher, G. and Porteu, F. (2006) B56-containing PP2A dephosphorylate ERK and their activity is controlled by the early gene IEX-1 and ERK. EMBO J, 25, 727-738.


119. Chen, D., Toone, W.M., Mata, J., Lyne, R., Burns, G., Kivinen, K., Brazma, A., Jones, N. and Bahler, J. (2003) Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell, 14, 214-229.


120. Hartmann, H.A., Kruger, J., Lottspeich, F. and Kahmann, R. (1999) Environmental signals controlling sexual development of the corn smut fungus Ustilago maydis through the transcriptional regulator Prf1. Plant Cell, 11, 1293-1305.


121. Fuchs, U., Hause, G., Schuchardt, I. and Steinberg, G. (2006) Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell, 18, 2066-2081.


122. Brachmann, A., Schirawski, J., Muller, P. and Kahmann, R. (2003) An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis. EMBO J, 22, 2199-2210.


123. Scherer, M., Heimel, K., Starke, V. and Kamper, J. (2006) The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell, 18, 2388-2401.


124. Muller, P., Katzenberger, J.D., Loubradou, G. and Kahmann, R. (2003a) Guanyl nucleotide exchange factor Sql2 and Ras2 regulate filamentous growth in Ustilago maydis. Eukaryot Cell, 2, 609-617.


125. Eichhorn, H., Lessing, F., Winterberg, B., Schirawski, J., Kamper, J., Muller, P. and Kahmann, R. (2006) A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell, 18, 3332-3345.


126. Zhang, W.Z., Cheng, G.Z., Gong, J.L., Hermanto, U., Zong, C.S., Chan, J., Cheng, J.Q. and Wang, L.H. (2008) RACK1 and CIS mediate the degradation of BimEL in cancer cells. J Biol Chem, 283, 16416-16426.


127. Ullah, H., Scappini, E.L., Moon, A.F., Williams, L.V., Armstrong, D.L. and Pedersen, L.C. (2008) Structure of a signal transduction regulator, RACK1, from Arabidopsis thaliana. Protein Sci, 17, 1771-1780.


128. Coyle, S.M., Gilbert, W.V. and Doudna, J.A. (2009) Direct link between RACK1 function and localization at the ribosome in vivo. Mol Cell Biol, 29, 1626-1634.


129. Fedler, M., Luh, K.S., Stelter, K., Nieto-Jacobo, F. and Basse, C.W. (2009) The a2 mating-type locus genes lga2 and rga2 direct uniparental mitochondrial DNA (mtDNA) inheritance and constrain mtDNA recombination during sexual development of Ustilago maydis. Genetics, 181, 847-860.


130. Nunez, A., Franco, A., Madrid, M., Soto, T., Vicente, J., Gacto, M. and Cansado, J. (2009) Role for RACK1 orthologue Cpc2 in the modulation of stress response in fission yeast. Mol Biol Cell, 20, 3996-4009.


131. Kaffarnik, F., Muller, P., Leibundgut, M., Kahmann, R. and Feldbrugge, M. (2003) PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J, 22, 5817-5826.


132. Matyskiela, M.E. and Morgan, D.O. (2009) Analysis of activator-binding sites on the APC/C supports a cooperative substrate-binding mechanism. Mol Cell, 34, 68- 80.


133. Lanver, D., Mendoza-Mendoza, A., Brachmann, A. and Kahmann, R. (2010) Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell, 22, 2085-2101.


134. Heimel, K., Scherer, M., Schuler, D. and Kamper, J. (2010a) The Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signaling pathways to coordinate the cell cycle and pathogenic development. Plant Cell, 22, 2908- 2922.


135. 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 U S A, 86, 5878-5882.


136. Muller, P., Weinzierl, G., Brachmann, A., Feldbrugge, M. and Kahmann, R. (2003b) Mating and pathogenic development of the smut fungus Ustilago maydis are regulated by one mitogen-activated protein kinase cascade. Eukaryot Cell, 2, 1187-1199.


137. Patterson, R.L., van Rossum, D.B., Barrow, R.K. and Snyder, S.H. (2004) RACK1 binds to inositol 1,4,5-trisphosphate receptors and mediates Ca 2+ release. Proceedings of the National Academy of Sciences of the United States of America, 101, 2328-2332.


138. Spellig, T., Bolker, M., Lottspeich, F., Frank, R.W. and Kahmann, R. (1994) Pheromones trigger filamentous growth in Ustilago maydis. EMBO J, 13, 1620- 1627.


139. Muller, P., Leibbrandt, A., Teunissen, H., Cubasch, S., Aichinger, C. and Kahmann, R. (2004) The G -subunit-encoding gene bpp1 controls cyclic-AMP signaling in Ustilago maydis. Eukaryot Cell, 3, 806-814.


140. Hoffman, C.S. (2007) Propping up our knowledge of G protein signaling pathways: diverse functions of putative noncanonical G subunits in fungi. 2007, pe3.


141. Hartmann, H.A., Kahmann, R. and Bolker, M. (1996) The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO J, 15, 1632-1641. References 79


142. Brefort, T., Muller, P. and Kahmann, R. (2005) The high-mobility-group domain transcription factor Rop1 is a direct regulator of prf1 in Ustilago maydis. Eukaryot Cell, 4, 379-391.


143. McLeod, M., Shor, B., Caporaso, A., Wang, W., Chen, H. and Hu, L. (2000) Cpc2, a fission yeast homologue of mammalian RACK1 protein, interacts with Ran1 (Pat1) kinase to regulate cell cycle progression and meiotic development. Mol Cell Biol, 20, 4016-4027.


144. Bolker, M., Genin, S., Lehmler, C. and Kahmann, R. (1995) Genetic regulation of mating and dimorphism in Ustilago maydis. Can J Bot, 73, S320-S325.


145. Bolker, M., Urban, M. and Kahmann, R. (1992) The a mating type locus of U. maydis specifies cell signaling components. Cell, 68, 441-450.


146. Hoffman, C. and Winston, F. (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene, 57, 267-272.


147. Feldbrugge, M., Kamper, J., Steinberg, G. and Kahmann, R. (2004) Regulation of mating and pathogenic development in Ustilago maydis. Curr Opin Microbiol, 7, 666-672.