Genome‐wide survey of non‐essential genes required for slowed DNA synthesis‐induced filamentous growth in yeast

We recently discovered that slowed DNA synthesis induces filamentous differentiation in S. cerevisiae. We screened the BY yeast deletion strains and identified four classes of non‐essential genes that are required for both slowed DNA‐induced filamentous growth and classic forms of filamentous growth: (a) genes encoding regulators of the actin cytoskeleton and cell polarity, ABP1, CAP2 and HUF1 (= YOR300W), in addition to the previously known BNI1, BUD2, PEA2, SPA2 and TPM1; (b) genes that are likely involved in cell wall biosynthesis, ECM25, GAS1 and PRS3; (c) genes encoding possible regulators of protein secretion, SEC66, RPL21A and RPL34B; (d) genes encoding factors for normal mitochondrial function, IML1 and UGO1. These results showed that pseudohyphal formation involves not the only previously known regulation of the actin cytoskeleton/cell polarity but also regulation of cell wall synthesis, protein secretion and mitochondrial function. Identification of multiple classes of genes that are required for both slowed DNA synthesis‐induced and classic forms of filamentous growth confirms that slowed DNA synthesis‐induced filamentous growth is bone fide filamentous differentiation. Copyright © 2005 John Wiley & Sons, Ltd.

[1]  A. Tong,et al.  Interaction between a Ras and a Rho GTPase couples selection of a growth site to the development of cell polarity in yeast. , 2003, Molecular biology of the cell.

[2]  G. Fink,et al.  Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. , 1994, Genes & development.

[3]  H. Bussey,et al.  Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae. , 1997, Genetics.

[4]  A. Ohta,et al.  Isolation and Characterization of EPD1, an Essential Gene for Pseudohyphal Growth of a Dimorphic Yeast,Candida maltosa , 1998, Journal of bacteriology.

[5]  R. Schekman,et al.  Binding of Secretory Precursor Polypeptides to a Translocon Subcomplex Is Regulated by BiP , 1997, Cell.

[6]  Gerald R. Fink,et al.  Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: Regulation by starvation and RAS , 1992, Cell.

[7]  Thierry Fontaine,et al.  Glycosylphosphatidylinositol-anchored Glucanosyltransferases Play an Active Role in the Biosynthesis of the Fungal Cell Wall* , 2000, The Journal of Biological Chemistry.

[8]  G. Fink,et al.  SOK2 may regulate cyclic AMP-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription , 1995, Molecular and cellular biology.

[9]  Christopher Minkyu Kang,et al.  Induction of S. cerevisiae filamentous differentiation by slowed DNA synthesis involves Mec1, Rad53 and Swe1 checkpoint proteins. , 2003, Molecular biology of the cell.

[10]  J. Bonifacino,et al.  Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. , 2002, Molecular biology of the cell.

[11]  David Botstein,et al.  Homology of a yeast actin-binding protein to signal transduction proteins and myosin-I , 1990, Nature.

[12]  M. Snyder,et al.  Polarized Growth Controls Cell Shape and Bipolar Bud Site Selection in Saccharomyces cerevisiae , 2000, Molecular and Cellular Biology.

[13]  G. Fink,et al.  Elements of the yeast pheromone response pathway required for filamentous growth of diploids. , 1993, Science.

[14]  M. Uhl,et al.  Haploinsufficiency‐based large‐scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C.albicans , 2003, The EMBO journal.

[15]  A. Hinnen,et al.  Functional analysis of 150 deletion mutants in Saccharomyces cerevisiae by a systematic approach , 1999, Molecular and General Genetics MGG.

[16]  A. Bretscher,et al.  Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. , 1998, The Journal of cell biology.

[17]  Christophe Fleury,et al.  Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia , 1997, Nature Genetics.

[18]  A. Bretscher,et al.  Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton , 1989, Cell.

[19]  W. Lo,et al.  The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. , 1998, Molecular biology of the cell.

[20]  J. Heitman,et al.  Characterization of alcohol-induced filamentous growth in Saccharomyces cerevisiae. , 2000, Molecular biology of the cell.

[21]  P. Walter,et al.  Mutants in three novel complementation groups inhibit membrane protein insertion into and soluble protein translocation across the endoplasmic reticulum membrane of Saccharomyces cerevisiae , 1992, The Journal of cell biology.

[22]  M. Snyder,et al.  A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. , 2001, Molecular biology of the cell.

[23]  R. Jensen,et al.  UGO1 Encodes an Outer Membrane Protein Required for Mitochondrial Fusion , 2001, The Journal of cell biology.

[24]  Ronald W. Davis,et al.  Functional profiling of the Saccharomyces cerevisiae genome , 2002, Nature.

[25]  A. T. Carter,et al.  Phosphoribosylpyrophosphate synthetase (PRS): A new gene family in Saccharomyces cerevisiae , 1994, Yeast.

[26]  J. Warner,et al.  Autoregulation in the Biosynthesis of Ribosomes , 2003, Molecular and Cellular Biology.

[27]  J. Heitman,et al.  Yeast pseudohyphal growth is regulated by GPA2, a G protein α homolog , 1997 .

[28]  G. Fink,et al.  Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. , 1997, Genetics.

[29]  John R. Pringle,et al.  Bni1p, a Yeast Formin Linking Cdc42p and the Actin Cytoskeleton During Polarized Morphogenesis , 1997, Science.

[30]  S. Kron,et al.  Cell cycle control of yeast filamentous growth. , 2001, Current opinion in microbiology.

[31]  Y. Jiang Transcriptional cosuppression of yeast Ty1 retrotransposons. , 2002, Genes & development.

[32]  J. Dickinson,et al.  'Fusel' alcohols induce hyphal-like extensions and pseudohyphal formation in yeasts. , 1996, Microbiology.

[33]  Young-Bum Kim,et al.  Uncoupling Protein-2 Negatively Regulates Insulin Secretion and Is a Major Link between Obesity, β Cell Dysfunction, and Type 2 Diabetes , 2001, Cell.

[34]  J. Dickinson,et al.  In yeast, the pseudohyphal phenotype induced by isoamyl alcohol results from the operation of the morphogenesis checkpoint , 2003, Journal of Cell Science.

[35]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[36]  Barry P. Young,et al.  Sec63p and Kar2p are required for the translocation of SRP‐dependent precursors into the yeast endoplasmic reticulum in vivo , 2001, The EMBO journal.

[37]  James G. McNally,et al.  Assembly and Function of the Actin Cytoskeleton of Yeast: Relationships between Cables and Patches , 1998, The Journal of cell biology.

[38]  I. Herskowitz,et al.  Putting the HO gene to work: practical uses for mating-type switching. , 1991, Methods in enzymology.

[39]  K. Tanaka,et al.  PRS3 encoding an essential subunit of yeast proteasomes homologous to mammalian proteasome subunit C5. , 1992, Biochemical and biophysical research communications.

[40]  W. Lo,et al.  FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin , 1996, Journal of bacteriology.

[41]  Hongyue Dai,et al.  Widespread aneuploidy revealed by DNA microarray expression profiling , 2000, Nature Genetics.

[42]  P. Radcliffe,et al.  The yeast PRS3 gene is required for cell integrity, cell cycle arrest upon nutrient deprivation, ion homeostasis and the proper organization of the actin cytoskeleton , 1999, Yeast.

[43]  M. Peter,et al.  Gic2p May Link Activated Cdc42p to Components Involved in Actin Polarization, Including Bni1p and Bud6p (Aip3p) , 2000, Molecular and Cellular Biology.