Skip to main content
Log in

Comprehensive and quantitative analysis of yeast deletion mutants defective in apical and isotropic bud growth

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

To obtain a comprehensive understanding of the budding phase transition, 4,711 Saccharomyces cerevisiae haploid nonessential gene deletion mutants were screened with the image processing program CalMorph, and 35 mutants with a round bud and 173 mutants with an elongated bud were statistically identified. We classified round and elongated bud mutants based on factors thought to affect the duration of the apical bud growth phase. Two round bud mutants (arc18 and sac6) were found to be defective in apical actin patch localization. Several elongated bud mutants demonstrated a delay of cell cycle progression at the apical growth phase, suggesting that these mutants have a defect in the control of cell cycle progression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Adams A, Pringle J (1984) Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J Cell Biol 98:934–945

    Article  PubMed  CAS  Google Scholar 

  • Ashburner M, Ball C, Blake J, Botstein D, Butler H, Cherry J, Davis A, Dolinski K, Dwight S, Eppig J, Harris M, Hill D, Issel-Tarver L, Kasarskis A, Lewis S, Matese J, Richardson J, Ringwald M, Rubin G, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29

    Article  PubMed  CAS  Google Scholar 

  • Bidlingmaier S, Snyder M (2002) Large-scale identification of genes important for apical growth in Saccharomyces cerevisiae by directed allele replacement technology (DART) screening. Funct Integr Genomics 1:345–356

    Article  PubMed  CAS  Google Scholar 

  • Blacketer M, Madaule P, Myers A (1995) Mutational analysis of morphologic differentiation in Saccharomyces cerevisiae. Genetics 140:1259–1275

    PubMed  CAS  Google Scholar 

  • Box G, Cox D (1964) An analysis of transformations. J R Stat Soc 26:211–252

    Google Scholar 

  • Brachmann C, Davies A, Cost G, Caputo E, Li J, Hieter P, Boeke J (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115–132

    Article  PubMed  CAS  Google Scholar 

  • Drees B, Brown C, Barrell B, Bretscher A (1995) Tropomyosin is essential in yeast, yet the TPM1 and TPM2 products perform distinct functions. J Cell Biol 128:383–392

    Article  PubMed  CAS  Google Scholar 

  • Drubin D, Nelson W (1996) Origins of cell polarity. Cell 84:335–344

    Article  PubMed  CAS  Google Scholar 

  • Dwight S, Harris M, Dolinski K, Ball C, Binkley G, Christie K, Fisk D, Issel-Tarver L, Schroeder M, Sherlock G, Sethuraman A, Weng S, Botstein D, Cherry J (2002) Saccharomyces Genome Database (SGD) provides secondary gene annotation using the Gene Ontology (GO). Nucl Acids Res 30:69–72

    Article  PubMed  CAS  Google Scholar 

  • Geissler S, Siegers K, Schiebel E (1998) A novel protein complex promoting formation of functional alpha- and gamma-tubulin. EMBO J 17:952–966

    Article  PubMed  CAS  Google Scholar 

  • Giaever G, Chu A, Ni L, Connelly C, Riles L, Véronneau S, Dow S, Lucau-Danila A, Anderson K, André B, Arkin A, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian K, Flaherty P, Foury F, Garfinkel D, Gerstein M, Gotte D, Güldener U, Hegemann J, Hempel S, Herman Z, Jaramillo D, Kelly D, Kelly S, Kötter P, LaBonte D, Lamb D, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi S, Revuelta J, Roberts C, Rose M, Ross-Macdonald P, Scherens B, Schimmack G, Shafer B, Shoemaker D, Sookhai-Mahadeo S, Storms R, Strathern J, Valle G, Voet M, Volckaert G, Wang C, Ward T, Wilhelmy J, Winzeler E, Yang Y, Yen G, Youngman E, Yu K, Bussey H, Boeke J, Snyder M, Philippsen P, Davis R, Johnston M (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391

    Article  PubMed  CAS  Google Scholar 

  • Karaoglu D, Kelleher D, Gilmore R (1997) The highly conserved Stt3 protein is a subunit of the yeast oligosaccharyltransferase and forms a subcomplex with Ost3p and Ost4p. J Biol Chem 272:32513–32520

    Article  PubMed  CAS  Google Scholar 

  • Karpova T, Tatchell K, Cooper J (1995) Actin filaments in yeast are unstable in the absence of capping protein or fimbrin. J Cell Biol 131:1483–1493

    Article  PubMed  CAS  Google Scholar 

  • Lew D, Reed S (1993) Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J Cell Biol 120:1305–1320

    Article  PubMed  CAS  Google Scholar 

  • Lew D, Reed S (1995) Cell cycle control of morphogenesis in budding yeast. Curr Opin Genet Dev 5:17–23

    Article  PubMed  CAS  Google Scholar 

  • Machesky L, Atkinson S, Ampe C, Vandekerckhove J, Pollard T (1994) Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J Cell Biol 127:107–115

    Article  PubMed  CAS  Google Scholar 

  • Madden K, Snyder M (1998) Cell polarity and morphogenesis in budding yeast. Annu Rev Microbiol 52:687–744

    Article  PubMed  CAS  Google Scholar 

  • Mösch H, Fink G (1997) Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. Genetics 145:671–684

    PubMed  Google Scholar 

  • Nakayama K, Nagasu T, Shimma Y, Kuromitsu J, Jigami Y (1992) OCH1 encodes a novel membrane bound mannosyltransferase: outer chain elongation of asparagine-linked oligosaccharides. EMBO J 11:2511–2519

    PubMed  CAS  Google Scholar 

  • Ohnuki S, Nogami S, Kanai H, Hirata D, Nakatani Y, Morishita S, Ohya Y (2007) Diversity of Ca2 + -induced morphology revealed by morphological phenotyping of Ca2 + -sensitive mutants of Saccharomyces cerevisiae. Eukaryot Cell 6:817–830

    Article  PubMed  CAS  Google Scholar 

  • Ohtani M, Saka A, Sano F, Ohya Y, Morishita S (2004) Development of image processing program for yeast cell morphology. J Bioinform Comput Biol 1:695–709

    Article  PubMed  Google Scholar 

  • Ohya Y, Sese J, Yukawa M, Sano F, Nakatani Y, Saito T, Saka A, Fukuda T, Ishihara S, Oka S, Suzuki G, Watanabe M, Hirata A, Ohtani M, Sawai H, Fraysse N, Latgé J, François J, Aebi M, Tanaka S, Muramatsu S, Araki H, Sonoike K, Nogami S, Morishita S (2005) High-dimensional and large-scale phenotyping of yeast mutants. Proc Natl Acad Sci USA 102:19015–19020

    Article  PubMed  CAS  Google Scholar 

  • Pruyne D, Bretscher A (2000a) Polarization of cell growth in yeast. J Cell Sci 113(Pt 4):571–585

    PubMed  CAS  Google Scholar 

  • Pruyne D, Bretscher A (2000b) Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J Cell Sci 113(Pt 3):365–375

    PubMed  CAS  Google Scholar 

  • Pruyne D, Gao L, Bi E, Bretscher A (2004) Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol Biol Cell 15:4971–4989

    Article  PubMed  CAS  Google Scholar 

  • Roemer T, Vallier L, Sheu Y, Snyder M (1998) The Spa2-related protein, Sph1p, is important for polarized growth in yeast. J Cell Sci 111(Pt 4):479–494

    PubMed  CAS  Google Scholar 

  • Rua D, Tobe B, Kron S (2001) Cell cycle control of yeast filamentous growth. Curr Opin Microbiol 4:720–727

    Article  PubMed  CAS  Google Scholar 

  • Saito T, Ohtani M, Sawai H, Sano F, Saka A, Watanabe D, Yukawa M, Ohya Y, Morishita S (2004) SCMD: Saccharomyces cerevisiae Morphological Database. Nucleic Acids Res 32:D319–D322

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, USA

  • Sheu Y, Santos B, Fortin N, Costigan C, Snyder M (1998) Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol Cell Biol 18:4053–4069

    PubMed  CAS  Google Scholar 

  • Sheu Y, Barral Y, Snyder M (2000) Polarized growth controls cell shape and bipolar bud site selection in Saccharomyces cerevisiae. Mol Cell Biol 20:5235–5247

    Article  PubMed  CAS  Google Scholar 

  • Snyder M, Gehrung S, Page B (1991) Studies concerning the temporal and genetic control of cell polarity in Saccharomyces cerevisiae. J Cell Biol 114:515–532

    Article  PubMed  CAS  Google Scholar 

  • Surana U, Robitsch H, Price C, Schuster T, Fitch I, Futcher A, Nasmyth K (1991) The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell 65:145–161

    Article  PubMed  CAS  Google Scholar 

  • Tjandra H, Compton J, Kellogg D (1998) Control of mitotic events by the Cdc42 GTPase, the Clb2 cyclin and a member of the PAK kinase family. Curr Biol 8:991–1000

    Article  PubMed  CAS  Google Scholar 

  • Winter D, Choe E, Li R (1999) Genetic dissection of the budding yeast Arp2/3 complex: a comparison of the in vivo and structural roles of individual subunits. Proc Natl Acad Sci USA 96:7288–7293

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank S. Ohnuki for assistance with the statistical analysis. This work was supported by the New Energy and Industrial Technology Development Organization (NEDO), by a grant for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and by the Institute for Bioinformatics and Research and Development of the Japan Science and Technology Corporation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yoshikazu Ohya.

Additional information

Communicated by P. Sunnerhagen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Watanabe, M., Watanabe, D., Nogami, S. et al. Comprehensive and quantitative analysis of yeast deletion mutants defective in apical and isotropic bud growth. Curr Genet 55, 365–380 (2009). https://doi.org/10.1007/s00294-009-0251-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-009-0251-0

Keywords

Navigation