Appressorienbildung von Ustilago maydis auf hydrophoben Oberflächen: Regulation durch Membranproteine

Ustilago maydis ist der Erreger des Maisbeulenbrandes. Die pathogene Entwicklung wird durch Fusion kompatibler Zellen und der Bildung eines dikaryotischen Filaments initiiert. Auf der Pflanzenoberfläche bildet U. maydis Appressorien aus, die das Eindringen des Pilzes in die Pflanze ermöglichen. Die...

Ausführliche Beschreibung

Gespeichert in:
1. Verfasser: Lanver, Daniel
Beteiligte: Kahmann, Regine (Prof. Dr.) (BetreuerIn (Doktorarbeit))
Format: Dissertation
Sprache:Deutsch
Veröffentlicht: Philipps-Universität Marburg 2011
Biologie
Ausgabe:http://dx.doi.org/10.17192/z2011.0126
Schlagworte:
Online Zugang:PDF-Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!

1. Pagni, M., Ioannidis, V., Cerutti, L., Zahn-Zabal, M., Jongeneel, C.V., and Falquet, L. (2004). MyHits: a new interactive resource for protein annotation and domain identification. Nucleic Acids Res 32, W332-335.


2. Seet, B.T., and Pawson, T. (2004). MAPK signaling: Sho business. Curr Biol 14, R708- 710.


3. 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.


4. Tong, A.H., Drees, B., Nardelli, G., Bader, G.D., Brannetti, B., Castagnoli, L., Evangelista, M., Ferracuti, S., Nelson, B., Paoluzi, S., Quondam, M., Zucconi, A., Hogue, C.W., Fields, S., Boone, C., and Cesareni, G. (2002). A combined experimental and computational strategy to define protein interaction networks for peptide recognition modules. Science 295, 321-324.


5. Keyse, S.M. (2000). Protein phosphatases and the regulation of mitogen-activated protein kinase signalling. Curr Opin Cell Biol 12, 186-192.


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


7. Brachmann, A., König, J., Julius, C., and Feldbrügge, M. (2004). A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics 272, 216-226.


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


9. 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.


10. Singh, P.K., and Hollingsworth, M.A. (2006). Cell surface-associated mucins in signal transduction. Trends Cell Biol 16, 467-476.


11. Rahn, J.J., Shen, Q., Mah, B.K., and Hugh, J.C. (2004). MUC1 initiates a calcium signal after ligation by intercellular adhesion molecule-1. J Biol Chem 279, 29386- 29390.


12. Vadaie, N., Dionne, H., Akajagbor, D.S., Nickerson, S.R., Krysan, D.J., and Cullen, P.J. (2008). Cleavage of the signaling mucin Msb2 by the aspartyl protease Yps1 is required for MAPK activation in yeast. J Cell Biol 181, 1073-1081.


13. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. (1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10, 1-6.


14. Cserzo, M., Wallin, E., Simon, I., von Heijne, G., and Elofsson, A. (1997). Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng 10, 673-676.


15. Xu, J.R., and Hamer, J.E. (1996). MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10, 2696-2706.


16. Roberts, R.L., and Fink, G.R. (1994). Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev 8, 2974-2985.


17. Kars, I., Krooshof, G.H., Wagemakers, L., Joosten, R., Benen, J.A., and van Kan, J.A. (2005). Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Plant J 43, 213-225.


18. Wreschner, D.H., McGuckin, M.A., Williams, S.J., Baruch, A., Yoeli, M., Ziv, R., Okun, L., Zaretsky, J., Smorodinsky, N., Keydar, I., Neophytou, P., Stacey, M., Lin, H.H., and Gordon, S. (2002). Generation of ligand-receptor alliances by "SEA" module-mediated cleavage of membrane-associated mucin proteins. Protein Sci 11, 698-706.


19. Klis, F.M., Mol, P., Hellingwerf, K., and Brul, S. (2002). Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol Rev 26, 239-256.


20. Talbot, N.J., Kershaw, M.J., Wakley, G.E., De Vries, O., Wessels, J., and Hamer, J.E. (1996). MPG1 Encodes a Fungal Hydrophobin Involved in Surface Interactions during Infection-Related Development of Magnaporthe grisea. Plant Cell 8, 985- 999.


21. Sambrook, J., Frisch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, New York.


22. Braun, E.J., and Howard, R.J. (1994). Adhesion of fungal spores and germlings to host plant surfaces. Protoplasma 181, 202-212.


23. Nicholson, R.L., and Epstein, L. (1991). Adhesion of fungi to the plant surface: prerequisite for pathogenesis. In The Fungal Spore and Disease Initiation in Plants and Animals, ed. Cole G.T., Hoch H.C., Plenum Publishing Corporation, New York, 3-23.


24. Epstein, L., and Nicholson, R.N. (1997). Adhesion of spores and hyphae to plant surfaces. In The Mycota V, Plant Relationships, ed. Carroll G.C., Tudzynski P., Springer Verlag, Berlin, 11-25.


25. Amyloids--a functional coat for microorganisms. Nat Rev Microbiol 3, 333-341.


26. Brewster, J.L., de Valoir, T., Dwyer, N.D., Winter, E., and Gustin, M.C. (1993). An osmosensing signal transduction pathway in yeast. Science 259, 1760-1763.


27. Kamakura, T., Yamaguchi, S., Saitoh, K., Teraoka, T., and Yamaguchi, I. (2002). A novel gene, CBP1, encoding a putative extracellular chitin-binding protein, may play an important role in the hydrophobic surface sensing of Magnaporthe grisea during appressorium differentiation. Mol Plant Microbe Interact 15, 437-444.


28. Commenil, P., Belingheri, L., and Dehorter, B. (1998). Antilipase antibodies prevent infection of tomato leaves by Botrytis cinerea. Physiol Mol Plant Pathol 52, 1-14.


29. Wynn, W.K. (1976). Appressorium formation over stomates by the bean rust fungus: response to the surface contact stimulus. Phytopathology 66, 136-146.


30. Broomfield, P.L., and Hargreaves, J.A. (1992). A single amino-acid change in the iron- sulphur protein subunit of succinate dehydrogenase confers resistance to carboxin in Ustilago maydis. Curr Genet 22, 117-121.


31. Pandey, P., Kharbanda, S., and Kufe, D. (1995). Association of the DF3/MUC1 breast cancer antigen with Grb2 and the Sos/Ras exchange protein. Cancer Res 55, 4000- 4003.


32. Frank, A.B. (1883). Über einige neue und weniger bekannte Pflanzenkrankheiten. Ber Deutsch Bot Gesell 1, 29-34.


33. Epstein, L., Laccetti, L.B., Staples, R.C., and Hoch, H.C. (1987). Cell-substratum adhesive protein involved in surface contact responses of the bean rust fungus. Physiol Mol Plant Pathol 30, 373-388.


34. Carpita, N.C., Defernez, M., Findlay, K., Wells, B., Shoue, D.A., Catchpole, G., Wilson, R.H., and McCann, M.C. (2001). Cell wall architecture of the elongating maize coleoptile. Plant Physiol 127, 551-565.


35. Gilbert, R.D., Johnson, A.M., and Dean, R.A. (1996). Chemical signals responsible for appressorium formation in the rice blast fungus. Physiol Mol Plant Pathol 48, 335- 346.


36. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.


37. Pain, N.A., Green, J.R., Jones, G.L., and O'Connell, R.J. (1996). Composition and organisation of extracellular matrices around germ tubes and appressoria of Colletotrichum lindemuthianum. Protoplasma 190, 119-130.


38. Christensen, J.J. (1963). Corn smut induced by Ustilago maydis. Amer Phytopathol Soc Monogr 2.


39. Mey, G., Held, K., Scheffer, J., Tenberge, K.B., and Tudzynski, P. (2002). CPMK2, an SLT2-homologous mitogen-activated protein (MAP) kinase, is essential for pathogenesis of Claviceps purpurea on rye: evidence for a second conserved pathogenesis-related MAP kinase cascade in phytopathogenic fungi. Mol Microbiol 46, 305-318.


40. Southern, E.M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98, 503-517.


41. Schirawski, J., Bohnert, H.U., Steinberg, G., Snetselaar, K., Adamikowa, L., and Kahmann, R. (2005). Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 17, 3532-3543.


42. Soto, P., Zhang, J., and Carraway, K.L. (2006). Enzymatic cleavage as a processing step in the maturation of Muc4/sialomucin complex. J Cell Biochem 97, 1267-1274.


43. Extracellular glycoprotein(s) associated with cellular differentiation in Magnaporthe grisea. Mol Plant Microbe Interact 7, 639-644.


44. Extracellular proteins associated with induction of differentiation in bean rust uredospore germlings. Phytopathology 75, 1073-1076.


45. 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.


46. Pothiratana, C. (2007). Functional characterization of the homeodomain transcription factor Hdp1 in Ustilago maydis. Dissertation, Philipps-Universität Marburg, Marburg. Regulation der Appressorienbildung in Ustilago maydis


47. 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.


48. Chen, R.E., and Thorner, J. (2007). Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1773, 1311-1340.


49. Rowell, J.B., and DeVay, J.E. (1954). Genetics of Ustilago zea in relation to basic problems of its pathogenicity. Phytopatholgy 44, 356-362.


50. Regenfelder, E., Spellig, T., Hartmann, A., Lauenstein, S., Bölker, M., and Kahmann, R. (1997). G proteins in Ustilago maydis: Transmission of multiple signals? EMBO J 16, 1934-1942.


51. 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.


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


53. Müller, O., Schreier, P.H., and Uhrig, J.F. (2008). Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis. Mol Genet Genomics 279, 27-39.


54. 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.


55. Correa, A., Staples, R.C., and Hoch, H.C. (1996). Inhibition of thigmostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma 194, 91- 102.


56. Cook, J.G., Bardwell, L., and Thorner, J. (1997). Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous-growth signalling pathway. Nature 390, 85-88.


57. Smith, D.G., Garcia-Pedrajas, M.D., Gold, S.E., and Perlin, M.H. (2003). Isolation and characterization from pathogenic fungi of genes encoding ammonium permeases and their roles in dimorphism. Mol Microbiol 50, 259-275.


58. 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.


59. Ospina-Giraldo, M.D., Mullins, E., and Kang, S. (2003). Loss of function of the Fusarium oxysporum SNF1 gene reduces virulence on cabbage and Arabidopsis. Curr Genet 44, 49-57.


60. Xu, J.R. (2000). Map kinases in fungal pathogens. Fungal Genet Biol 31, 137-152.


61. Kim, S., Ahn, I.P., Rho, H.S., and Lee, Y.H. (2005). MHP1, a Magnaporthe grisea hydrophobin gene, is required for fungal development and plant colonization. Mol Microbiol 57, 1224-1237.


62. Posas, F., and Saito, H. (1997). Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276, 1702-1705.


63. 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.


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


65. Reiser, V., Salah, S.M., and Ammerer, G. (2000). Polarized localization of yeast Pbs2 depends on osmostress, the membrane protein Sho1 and Cdc42. Nat Cell Biol 2, 620-627.


66. Ruiz-Roldan, M.C., Maier, F.J., and Schafer, W. (2001). PTK1, a mitogen-activated- protein kinase gene, is required for conidiation, appressorium formation, and pathogenicity of Pyrenophora teres on barley. Mol Plant Microbe Interact 14, 116- 125.


67. Regulation der Appressorienbildung in Ustilago maydis


68. Norice, C.T., Smith, F.J., Jr., Solis, N., Filler, S.G., and Mitchell, A.P. (2007). Requirement for Candida albicans Sun41 in biofilm formation and virulence. Eukaryot Cell 6, 2046-2055.


69. Rogers, L.M., Kim, Y.K., Guo, W., Gonzalez-Candelas, L., Li, D., and Kolattukudy, P.E. (2000). Requirement for either a host-or pectin-induced pectate lyase for infection of Pisum sativum by Nectria hematococca. Proc Natl Acad Sci U S A 97, 9813-9818.


70. Regulation der Appressorienbildung in Ustilago maydis Zarrinpar, A., Bhattacharyya, R.P., Nittler, M.P., and Lim, W.A. (2004). Sho1 and Pbs2 act as coscaffolds linking components in the yeast high osmolarity MAP kinase pathway. Mol Cell 14, 825-832.


71. Cullen, P.J. (2007). Signaling mucins: the new kids on the MAPK block. Crit Rev Eukaryot Gene Expr 17, 241-257.


72. Müller, P. (2003). Signalweiterleitung in Ustilago maydis: Die Kpp4/Fuz7/Kpp2-MAPK- Kaskade kontrolliert Pheromonantwort und pathogene Entwicklung. Dissertation, Philipps-Universität Marburg, Marburg.


73. Terhune, B.T., and Hoch, H.C. (1993). Substrate hydrophobicity and adhesion of Uromyces urediospores and germlings. Exp Mycol 17, 241-252.


74. Tucker, S.L., and Talbot, N.J. (2001). Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol 39, 385-417.


75. Choi, W., and Dean, R.A. (1997). The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9, 1973-1983.


76. Zheng, L., Campbell, M., Murphy, J., Lam, S., and Xu, J.R. (2000). The BMP1 gene is essential for pathogenicity in the gray mold fungus Botrytis cinerea. Mol Plant Microbe Interact 13, 724-732.


77. Mitchell, T.K., and Dean, R.A. (1995). The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7, 1869-1878.


78. Sgarlata, C., and Perez-Martin, J. (2005). The cdc25 phosphatase is essential for the G2/M phase transition in the basidiomycete yeast Ustilago maydis. Mol Microbiol 58, 1482-1496.


79. Tonukari, N.J., Scott-Craig, J.S., and Walton, J.D. (2000). The Cochliobolus carbonum SNF1 gene is required for cell wall-degrading enzyme expression and virulence on maize. Plant Cell 12, 237-248.


80. The Colletotrichum lagenarium MAP kinase gene CMK1 regulates diverse aspects of fungal pathogenesis. Mol Plant Microbe Interact 13, 374-383.


81. Staples, R.C. (1985). The development of infection structures by the rusts and other fungi. Microbiol Sci 2, 193-194, 197-198.


82. 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.


83. Perez-Nadales, E., and Di Pietro, A. (2011). The Membrane Mucin Msb2 Regulates Invasive Growth and Plant Infection in Fusarium oxysporum. Plant Cell (in press).


84. Fernandez-Alvarez, A., Elias-Villalobos, A., and Ibeas, J.I. (2009). The O- mannosyltransferase PMT4 is essential for normal appressorium formation and penetration in Ustilago maydis. Plant Cell 21, 3397-3412.


85. Roman, E., Nombela, C., and Pla, J. (2005). The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candida albicans. Mol Cell Biol 25, 10611-10627.


86. Pitoniak, A., Birkaya, B., Dionne, H.M., Vadaie, N., and Cullen, P.J. (2009). The signaling mucins Msb2 and Hkr1 differentially regulate the filamentation mitogen- activated protein kinase pathway and contribute to a multimodal response. Mol Biol Cell 20, 3101-3114.


87. Giesbert, S., Lepping, H.B., Tenberge, K.B., and Tudzynski, P. (1998). The Xylanolytic System of Claviceps purpurea: Cytological Evidence for Secretion of Xylanases in Infected Rye Tissue and Molecular Characterization of Two Xylanase Genes. Phytopathology 88, 1020-1030.


88. Dupres, V., Alsteens, D., Wilk, S., Hansen, B., Heinisch, J.J., and Dufrene, Y.F. (2009). The yeast Wsc1 cell surface sensor behaves like a nanospring in vivo. Nat Chem Biol 5, 857-862.


89. Oh, Y., Donofrio, N., Pan, H., Coughlan, S., Brown, D.E., Meng, S., Mitchell, T., and Dean, R.A. (2008). Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae. Genome Biol 9, R85.


90. Powell, A.L., van Kan, J., ten Have, A., Visser, J., Greve, L.C., Bennett, A.B., and Labavitch, J.M. (2000). Transgenic expression of pear PGIP in tomato limits fungal colonization. Mol Plant Microbe Interact 13, 942-950.


91. Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland. J Biol Chem 276, 13057-13064.


92. Vranes, M. (2006). Transkriptom-Analyse der frühen Infektionsphase von Ustilago maydis: Identifikation neuer pathogenitätsrelevanter Gene. Dissertation, Philipps- Universität Marburg, Marburg.


93. Tatebayashi, K., Tanaka, K., Yang, H.Y., Yamamoto, K., Matsushita, Y., Tomida, T., Imai, M., and Saito, H. (2007). Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J 26, 3521-3533. ten Have, A., Mulder, W., Visser, J., and van Kan, J.A. (1998). The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol Plant Microbe Interact 11, 1009-1016.


94. Xue, C., Park, G., Choi, W., Zheng, L., Dean, R.A., and Xu, J.R. (2002). Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus. Plant Cell 14, 2107-2119.


95. Mims, C.W., and Richardson, E.A. (1989). Ultrastructure of appressorium development by basidiospore germlings of the rust fungus Gymnosporangium juniperi- virginianae. Protoplasma 148, 111-119.


96. 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.


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


98. Snetselaar, K.M., Bölker, M., and Kahmann, R. (1996). Ustilago maydis mating hyphae orient their growth toward pheromone sources. Fungal Genet Biol 20, 299-312. Regulation der Appressorienbildung in Ustilago maydis


99. Raitt, D.C., Posas, F., and Saito, H. (2000). Yeast Cdc42 GTPase and Ste20 PAK-like kinase regulate Sho1-dependent activation of the Hog1 MAPK pathway. EMBO J 19, 4623-4631.


100. Mendgen, K., and Deising, H. (1993). Infection structures of fungal plant pathogens – a cytological and physiological evaluation. New Phytol 124, 193-213.


101. Julenius, K., Molgaard, A., Gupta, R., and Brunak, S. (2005). Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15, 153-164.


102. Snetselaar, K.M., and Mims, C.W. (1994). Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol Res 98, 347-355.


103. Snetselaar, K.M. (1993). Microscopic observation of Ustilago maydis mating interactions. Exp Mycol 17, 345-355.


104. Snetselaar, K.M., and Mims, C.W. (1993). Infection of maize stigmas by Ustilago maydis: Light and electron microscopy. Phytopathology 83, 843.


105. 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.


106. Flemming, H.C., and Wingender, J. (2010). The biofilm matrix. Nat Rev Microbiol 8, 623-633.


107. Zhao, X., Kim, Y., Park, G., and Xu, J.R. (2005). A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell 17, 1317-1329.


108. Puhalla, J.E. (1968). Compatibility reactions on solid medium and interstrain inhibition in Ustilago maydis. Genetics 60, 461-474.


109. O'Rourke, S.M., and Herskowitz, I. (2002). A third osmosensing branch in Saccharomyces cerevisiae requires the Msb2 protein and functions in parallel with the Sho1 branch. Mol Cell Biol 22, 4739-4749.


110. Cullen, P.J., Schultz, J., Horecka, J., Stevenson, B.J., Jigami, Y., and Sprague, G.F., Jr. (2000). Defects in protein glycosylation cause SHO1-dependent activation of a STE12 signaling pathway in yeast. Genetics 155, 1005-1018.


111. Nelson, B., Parsons, A.B., Evangelista, M., Schaefer, K., Kennedy, K., Ritchie, S., Petryshen, T.L., and Boone, C. (2004). Fus1p interacts with components of the Hog1p mitogen-activated protein kinase and Cdc42p morphogenesis signaling pathways to control cell fusion during yeast mating. Genetics 166, 67-77.


112. Tatebayashi, K., Yamamoto, K., Tanaka, K., Tomida, T., Maruoka, T., Kasukawa, E., and Saito, H. (2006). Adaptor functions of Cdc42, Ste50, and Sho1 in the yeast osmoregulatory HOG MAPK pathway. EMBO J 25, 3033-3044.


113. 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.


114. 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.


115. 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.


116. Müller, 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.


117. Skamnioti, P., and Gurr, S.J. (2007). Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19, 2674-2689.


118. Stagljar, I., Korostensky, C., Johnsson, N., and te Heesen, S. (1998). A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo. Proc Natl Acad Sci U S A 95, 5187-5192.


119. Zhao, X., Mehrabi, R., and Xu, J.R. (2007). Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6, 1701-1714.


120. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95, 14863- 14868.


121. Yang, H.Y., Tatebayashi, K., Yamamoto, K., and Saito, H. (2009). Glycosylation defects activate filamentous growth Kss1 MAPK and inhibit osmoregulatory Hog1 MAPK. Embo J 28, 1380-1391.


122. Roman, E., Cottier, F., Ernst, J.F., and Pla, J. (2009). Msb2 signaling mucin controls activation of Cek1 mitogen-activated protein kinase in Candida albicans. Eukaryot Cell 8, 1235-1249.


123. 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.


124. Verna, J., Lodder, A., Lee, K., Vagts, A., and Ballester, R. (1997). A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 94, 13804-13809.


125. Müller, P., Weinzierl, G., Brachmann, A., Feldbrügge, 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.


126. 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 U S A 95, 5857-5864.


127. Mösch, H.U., Roberts, R.L., and Fink, G.R. (1996). Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 93, 5352-5356.


128. 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.


129. Cohen, S.N., Chang, A.C., and Hsu, L. (1972). Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A 69, 2110-2114.


130. Peter, M., Neiman, A.M., Park, H.O., van Lohuizen, M., and Herskowitz, I. (1996). Functional analysis of the interaction between the small GTP binding protein Cdc42 and the Ste20 protein kinase in yeast. EMBO J 15, 7046-7059.


131. Yee, A.R., and Kronstad, J.W. (1993). Construction of chimeric alleles with altered specificity at the b incompatibility locus of Ustilago maydis. Proc Natl Acad Sci U S A 90, 664-668.


132. 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.