Dissection of Filamentous Growth by Transposon Mutagenesis in Saccharomyces cerevisiae

INVESTIGATIONS

Dissection of Filamentous Growth by Transposon Mutagenesis in Saccharomyces cerevisiae

H. U. Mosch and G. R. Fink
Institute for Microbiology, Georg-August-University Gottingen, D-37077 Gottingen, Germany

Diploid Saccharomyces cerevisiae strains starved for nitrogen undergo a developmental transition from growth as single yeast form (YF) cells to a multicellular form consisting of filaments of pseudohyphal (PH) cells. Filamentous growth is regulated by an evolutionarily conserved signaling pathway that includes the small GTP-binding proteins Ras2p and Cdc42p, the protein kinases Ste20p, Ste11p and Ste7p, and the transcription factor Ste12p. Here, we designed a genetic screen for mutant strains defective for filamentous growth (dfg) to identify novel targets of the filamentation signaling pathway, and we thereby identified 16 different genes, CDC39, STE12, TEC1, WHI3, NAB1, DBR1, CDC55, SRV2, TPM1, SPA2, BNI1, DFG5, DFG9, DFG10, BUD8 and DFG16, mutations that block filamentous growth. Phenotypic analysis of dfg mutant strains genetically dissects filamentous growth into the cellular processes of signal transduction, bud site selection, cell morphogenesis and invasive growth. Epistasis tests between dfg mutant alleles and dominant activated alleles of the RAS2 and STE11 genes, RAS2(Val19) and STE11-4, respectively, identify putative targets for the filamentation signaling pathway. Several of the genes described here have homologues in filamentous fungi, where they also regulate fungal development.

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				N. Colomina, F. Ferrezuelo, H. Wang, M. Aldea, and E. Gari Whi3, a Developmental Regulator of Budding Yeast, Binds a Large Set of mRNAs Functionally Related to the Endoplasmic Reticulum J. Biol. Chem., October 17, 2008; 283(42): 28670 - 28679. [Abstract] [Full Text] [PDF]

				R. Froquet, N. Cherix, R. Birke, M. Benghezal, E. Cameroni, F. Letourneur, H.-U. Mosch, C. De Virgilio, and P. Cosson Control of Cellular Physiology by TM9 Proteins in Yeast and Dictyostelium J. Biol. Chem., March 14, 2008; 283(11): 6764 - 6772. [Abstract] [Full Text] [PDF]

				O. Valerius, M. Kleinschmidt, N. Rachfall, F. Schulze, S. Lopez Marin, M. Hoppert, K. Streckfuss-Bomeke, C. Fischer, and G. H. Braus The Saccharomyces Homolog of Mammalian RACK1, Cpc2/Asc1p, Is Required for FLO11-dependent Adhesive Growth and Dimorphism Mol. Cell. Proteomics, November 1, 2007; 6(11): 1968 - 1979. [Abstract] [Full Text] [PDF]

				A.-B. Krappmann, N. Taheri, M. Heinrich, and H.-U. Mosch Distinct Domains of Yeast Cortical Tag Proteins Bud8p and Bud9p Confer Polar Localization and Functionality Mol. Biol. Cell, September 1, 2007; 18(9): 3323 - 3339. [Abstract] [Full Text] [PDF]

				M. A. Juanes, E. Queralt, M. C. Bano, and J. C. Igual Rot1 plays an antagonistic role to Clb2 in actin cytoskeleton dynamics throughout the cell cycle J. Cell Sci., July 15, 2007; 120(14): 2390 - 2401. [Abstract] [Full Text] [PDF]

				S. Ohnuki, S. Nogami, H. Kanai, D. Hirata, Y. Nakatani, S. Morishita, and Y. Ohya Diversity of Ca2+-Induced Morphology Revealed by Morphological Phenotyping of Ca2+-Sensitive Mutants of Saccharomyces cerevisiae Eukaryot. Cell, May 1, 2007; 6(5): 817 - 830. [Abstract] [Full Text] [PDF]

				H.-O. Park and E. Bi Central Roles of Small GTPases in the Development of Cell Polarity in Yeast and Beyond Microbiol. Mol. Biol. Rev., March 1, 2007; 71(1): 48 - 96. [Abstract] [Full Text] [PDF]

				S. Chou, S. Lane, and H. Liu Regulation of Mating and Filamentation Genes by Two Distinct Ste12 Complexes in Saccharomyces cerevisiae. Mol. Cell. Biol., July 1, 2006; 26(13): 4794 - 4805. [Abstract] [Full Text] [PDF]

				C. Wu, G. Jansen, J. Zhang, D. Y. Thomas, and M. Whiteway Adaptor protein Ste50p links the Ste11p MEKK to the HOG pathway through plasma membrane association. Genes & Dev., March 15, 2006; 20(6): 734 - 746. [Abstract] [Full Text] [PDF]

				K. Rothfels, J. C. Tanny, E. Molnar, H. Friesen, C. Commisso, and J. Segall Components of the ESCRT Pathway, DFG16, and YGR122w Are Required for Rim101 To Act as a Corepressor with Nrg1 at the Negative Regulatory Element of the DIT1 Gene of Saccharomyces cerevisiae Mol. Cell. Biol., August 1, 2005; 25(15): 6772 - 6788. [Abstract] [Full Text] [PDF]

				E. S. Bensen, A. Clemente-Blanco, K. R. Finley, J. Correa-Bordes, and J. Berman The Mitotic Cyclins Clb2p and Clb4p Affect Morphogenesis in Candida albicans Mol. Biol. Cell, July 1, 2005; 16(7): 3387 - 3400. [Abstract] [Full Text] [PDF]

				K. J. Barwell, J. H. Boysen, W. Xu, and A. P. Mitchell Relationship of DFG16 to the Rim101p pH Response Pathway in Saccharomyces cerevisiae and Candida albicans Eukaryot. Cell, May 1, 2005; 4(5): 890 - 899. [Abstract] [Full Text] [PDF]

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				Z. Cheng and T. M. Menees RNA Branching and Debranching in the Yeast Retrovirus-like Element Ty1 Science, January 9, 2004; 303(5655): 240 - 243. [Abstract] [Full Text] [PDF]

				T. J. Kottom, J. R. Kohler, C. F. Thomas Jr., G. R. Fink, and A. H. Limper Lung Epithelial Cells and Extracellular Matrix Components Induce Expression of Pneumocystis carinii STE20, a Gene Complementing the Mating and Pseudohyphal Growth Defects of ste20 Mutant Yeast Infect. Immun., November 1, 2003; 71(11): 6463 - 6471. [Abstract] [Full Text] [PDF]

				A. Breitkreutz, L. Boucher, B.-J. Breitkreutz, M. Sultan, I. Jurisica, and M. Tyers Phenotypic and Transcriptional Plasticity Directed by a Yeast Mitogen-Activated Protein Kinase Network Genetics, November 1, 2003; 165(3): 997 - 1015. [Abstract] [Full Text] [PDF]

				G. H. Braus, O. Grundmann, S. Bruckner, and H.-U. Mosch Amino Acid Starvation and Gcn4p Regulate Adhesive Growth and FLO11 Gene Expression in Saccharomyces cerevisiae Mol. Biol. Cell, October 1, 2003; 14(10): 4272 - 4284. [Abstract] [Full Text] [PDF]

				E. Spreghini, D. A. Davis, R. Subaran, M. Kim, and A. P. Mitchell Roles of Candida albicans Dfg5p and Dcw1p Cell Surface Proteins in Growth and Hypha Formation Eukaryot. Cell, August 1, 2003; 2(4): 746 - 755. [Abstract] [Full Text] [PDF]

				G. G. Toby, W. Gherraby, T. R. Coleman, and E. A. Golemis A Novel RING Finger Protein, Human Enhancer of Invasion 10, Alters Mitotic Progression through Regulation of Cyclin B Levels Mol. Cell. Biol., March 15, 2003; 23(6): 2109 - 2122. [Abstract] [Full Text] [PDF]

				T. Kohler, S. Wesche, N. Taheri, G. H. Braus, and H.-U. Mosch Dual Role of the Saccharomyces cerevisiae TEA/ATTS Family Transcription Factor Tec1p in Regulation of Gene Expression and Cellular Development Eukaryot. Cell, October 1, 2002; 1(5): 673 - 686. [Abstract] [Full Text] [PDF]

				P. J. Cullen and G. F. Sprague Jr. The Roles of Bud-Site-Selection Proteins during Haploid Invasive Growth in Yeast Mol. Biol. Cell, September 1, 2002; 13(9): 2990 - 3004. [Abstract] [Full Text] [PDF]

				S. Hohmann Osmotic Stress Signaling and Osmoadaptation in Yeasts Microbiol. Mol. Biol. Rev., June 1, 2002; 66(2): 300 - 372. [Abstract] [Full Text] [PDF]

				H.-S. Hwang and K. Song IBD2 Encodes a Novel Component of the Bub2p-Dependent Spindle Checkpoint in the Budding Yeast Saccharomyces cerevisiae Genetics, June 1, 2002; 161(2): 595 - 609. [Abstract] [Full Text] [PDF]

				D. M. Leslie, B. Grill, M. P. Rout, R. W. Wozniak, and J. D. Aitchison Kap121p-Mediated Nuclear Import Is Required for Mating and Cellular Differentiation in Yeast Mol. Cell. Biol., April 15, 2002; 22(8): 2544 - 2555. [Abstract] [Full Text] [PDF]

				S. P. Palecek, A. S. Parikh, and S. J. Kron Sensing, signalling and integrating physical processes during Saccharomyces cerevisiae invasive and filamentous growth Microbiology, April 1, 2002; 148(4): 893 - 907. [Full Text] [PDF]

				L. R. Schenkman, C. Caruso, N. Page, and J. R. Pringle The role of cell cycle-regulated expression in the localization of spatial landmark proteins in yeast J. Cell Biol., March 4, 2002; 156(5): 829 - 841. [Abstract] [Full Text] [PDF]

				E. Gari, T. Volpe, H. Wang, C. Gallego, B. Futcher, and M. Aldea Whi3 binds the mRNA of the G1 cyclin CLN3 to modulate cell fate in budding yeast Genes & Dev., November 1, 2001; 15(21): 2803 - 2808. [Abstract] [Full Text] [PDF]

				S.-H. Ahn, B. T. Tobe, J. N. F. Gerald, S. L. Anderson, A. Acurio, and S. J. Kron Enhanced Cell Polarity in Mutants of the Budding Yeast Cyclin-dependent Kinase Cdc28p Mol. Biol. Cell, November 1, 2001; 12(11): 3589 - 3600. [Abstract] [Full Text] [PDF]

				S. Lane, S. Zhou, T. Pan, Q. Dai, and H. Liu The Basic Helix-Loop-Helix Transcription Factor Cph2 Regulates Hyphal Development in Candida albicans Partly via Tec1 Mol. Cell. Biol., October 1, 2001; 21(19): 6418 - 6428. [Abstract] [Full Text] [PDF]

				B. L. Drees, B. Sundin, E. Brazeau, J. P. Caviston, G.-C. Chen, W. Guo, K. G. Kozminski, M. W. Lau, J. J. Moskow, A. Tong, et al. A protein interaction map for cell polarity development J. Cell Biol., August 6, 2001; 154(3): 549 - 576. [Abstract] [Full Text] [PDF]