• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of mbcLink to Publisher's site
Mol Biol Cell. Sep 1994; 5(9): 1003–1022.
PMCID: PMC301123

Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae.

Abstract

Laboratory strains of Saccharomyces cerevisiae are dimorphic; in response to nitrogen starvation they switch from a yeast form (YF) to a filamentous pseudohyphal (PH) form. Time-lapse video microscopy of dividing cells reveals that YF and PH cells differ in their cell cycles and budding polarity. The YF cell cycle is controlled at the G1/S transition by the cell-size checkpoint Start. YF cells divide asymmetrically, producing small daughters from full-sized mothers. As a result, mothers and daughters bud asynchronously. Mothers bud immediately but daughters grow in G1 until they achieve a critical cell size. By contrast, PH cells divide symmetrically, restricting mitosis until the bud grows to the size of the mother. Thus, mother and daughter bud synchronously in the next cycle, without a G1 delay before Start. YF and PH cells also exhibit distinct bud-site selection patterns. YF cells are bipolar, producing their second and subsequent buds at either pole. PH cells are unipolar, producing their second and subsequent buds only from the end opposite the junction with their mother. We propose that in PH cells a G2 cell-size checkpoint delays mitosis until bud size reaches that of the mother cell. We conclude that yeast and PH forms are distinct cell types each with a unique cell cycle, budding pattern, and cell shape.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (5.0M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Adams AE, Pringle JR. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J Cell Biol. 1984 Mar;98(3):934–945. [PMC free article] [PubMed]
  • Adams AE, Pringle JR. Staining of actin with fluorochrome-conjugated phalloidin. Methods Enzymol. 1991;194:729–731. [PubMed]
  • Amon A, Surana U, Muroff I, Nasmyth K. Regulation of p34CDC28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae. Nature. 1992 Jan 23;355(6358):368–371. [PubMed]
  • Blacketer MJ, Koehler CM, Coats SG, Myers AM, Madaule P. Regulation of dimorphism in Saccharomyces cerevisiae: involvement of the novel protein kinase homolog Elm1p and protein phosphatase 2A. Mol Cell Biol. 1993 Sep;13(9):5567–5581. [PMC free article] [PubMed]
  • Booher RN, Deshaies RJ, Kirschner MW. Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J. 1993 Sep;12(9):3417–3426. [PMC free article] [PubMed]
  • Brandriss MC, Magasanik B. Genetics and physiology of proline utilization in Saccharomyces cerevisiae: enzyme induction by proline. J Bacteriol. 1979 Nov;140(2):498–503. [PMC free article] [PubMed]
  • Cabib E, Bowers B. Chitin and yeast budding. Localization of chitin in yeast bud scars. J Biol Chem. 1971 Jan 10;246(1):152–159. [PubMed]
  • Chang F, Herskowitz I. Identification of a gene necessary for cell cycle arrest by a negative growth factor of yeast: FAR1 is an inhibitor of a G1 cyclin, CLN2. Cell. 1990 Nov 30;63(5):999–1011. [PubMed]
  • Chant J, Pringle JR. Budding and cell polarity in Saccharomyces cerevisiae. Curr Opin Genet Dev. 1991 Oct;1(3):342–350. [PubMed]
  • Cross FR, Tinkelenberg AH. A potential positive feedback loop controlling CLN1 and CLN2 gene expression at the start of the yeast cell cycle. Cell. 1991 May 31;65(5):875–883. [PubMed]
  • Dirick L, Nasmyth K. Positive feedback in the activation of G1 cyclins in yeast. Nature. 1991 Jun 27;351(6329):754–757. [PubMed]
  • Elion EA, Grisafi PL, Fink GR. FUS3 encodes a cdc2+/CDC28-related kinase required for the transition from mitosis into conjugation. Cell. 1990 Feb 23;60(4):649–664. [PubMed]
  • Fantes P, Nurse P. Control of cell size at division in fission yeast by a growth-modulated size control over nuclear division. Exp Cell Res. 1977 Jul;107(2):377–386. [PubMed]
  • Feilotter H, Lingner C, Rowley R, Young PG. Regulation of the G2-mitosis transition. Biochem Cell Biol. 1992 Oct-Nov;70(10-11):954–971. [PubMed]
  • Forsburg SL, Nurse P. Cell cycle regulation in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Annu Rev Cell Biol. 1991;7:227–256. [PubMed]
  • Gimeno CJ, Fink GR. Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol Cell Biol. 1994 Mar;14(3):2100–2112. [PMC free article] [PubMed]
  • Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell. 1992 Mar 20;68(6):1077–1090. [PubMed]
  • Gould KL, Nurse P. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature. 1989 Nov 2;342(6245):39–45. [PubMed]
  • Grenson M, Mousset M, Wiame JM, Bechet J. Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. I. Evidence for a specific arginine-transporting system. Biochim Biophys Acta. 1966 Oct 31;127(2):325–338. [PubMed]
  • Hadwiger JA, Wittenberg C, Richardson HE, de Barros Lopes M, Reed SI. A family of cyclin homologs that control the G1 phase in yeast. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6255–6259. [PMC free article] [PubMed]
  • Hartwell LH, Culotti J, Pringle JR, Reid BJ. Genetic control of the cell division cycle in yeast. Science. 1974 Jan 11;183(4120):46–51. [PubMed]
  • Hartwell LH, Unger MW. Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division. J Cell Biol. 1977 Nov;75(2 Pt 1):422–435. [PMC free article] [PubMed]
  • Hoyt MA, Totis L, Roberts BT. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell. 1991 Aug 9;66(3):507–517. [PubMed]
  • Hutter KJ, Eipel HE. Microbial determinations by flow cytometry. J Gen Microbiol. 1979 Aug;113(2):369–375. [PubMed]
  • Johnston GC. Cell size and budding during starvation of the yeast Saccharomyces cerevisiae. J Bacteriol. 1977 Nov;132(2):738–739. [PMC free article] [PubMed]
  • Johnston GC, Singer RA. Growth and the cell cycle of the yeast Saccharomyces cerevisiae. I. Slowing S phase or nuclear division decreases the G1 cell cycle period. Exp Cell Res. 1983 Nov;149(1):1–13. [PubMed]
  • Johnston LH, Nasmyth KA. Saccharomyces cerevisiae cell cycle mutant cdc9 is defective in DNA ligase. Nature. 1978 Aug 31;274(5674):891–893. [PubMed]
  • Kilmartin JV, Wright B, Milstein C. Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J Cell Biol. 1982 Jun;93(3):576–582. [PMC free article] [PubMed]
  • Lew DJ, Reed SI. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J Cell Biol. 1993 Mar;120(6):1305–1320. [PMC free article] [PubMed]
  • Li R, Murray AW. Feedback control of mitosis in budding yeast. Cell. 1991 Aug 9;66(3):519–531. [PubMed]
  • Liu H, Styles CA, Fink GR. Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science. 1993 Dec 10;262(5140):1741–1744. [PubMed]
  • Ljungdahl PO, Gimeno CJ, Styles CA, Fink GR. SHR3: a novel component of the secretory pathway specifically required for localization of amino acid permeases in yeast. Cell. 1992 Oct 30;71(3):463–478. [PubMed]
  • Millar JB, McGowan CH, Lenaers G, Jones R, Russell P. p80cdc25 mitotic inducer is the tyrosine phosphatase that activates p34cdc2 kinase in fission yeast. EMBO J. 1991 Dec;10(13):4301–4309. [PMC free article] [PubMed]
  • Mortimer RK, Johnston JR. Genealogy of principal strains of the yeast genetic stock center. Genetics. 1986 May;113(1):35–43. [PMC free article] [PubMed]
  • Nasmyth K. Control of the yeast cell cycle by the Cdc28 protein kinase. Curr Opin Cell Biol. 1993 Apr;5(2):166–179. [PubMed]
  • Nurse P, Bissett Y. Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature. 1981 Aug 6;292(5823):558–560. [PubMed]
  • Nurse P, Thuriaux P. Regulatory genes controlling mitosis in the fission yeast Schizosaccharomyces pombe. Genetics. 1980 Nov;96(3):627–637. [PMC free article] [PubMed]
  • Nurse P, Thuriaux P, Nasmyth K. Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet. 1976 Jul 23;146(2):167–178. [PubMed]
  • Pardee AB. G1 events and regulation of cell proliferation. Science. 1989 Nov 3;246(4930):603–608. [PubMed]
  • Pringle JR, Preston RA, Adams AE, Stearns T, Drubin DG, Haarer BK, Jones EW. Fluorescence microscopy methods for yeast. Methods Cell Biol. 1989;31:357–435. [PubMed]
  • Richardson HE, Wittenberg C, Cross F, Reed SI. An essential G1 function for cyclin-like proteins in yeast. Cell. 1989 Dec 22;59(6):1127–1133. [PubMed]
  • Russell P, Moreno S, Reed SI. Conservation of mitotic controls in fission and budding yeasts. Cell. 1989 Apr 21;57(2):295–303. [PubMed]
  • Russell P, Nurse P. Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell. 1987 May 22;49(4):559–567. [PubMed]
  • Sherman F. Getting started with yeast. Methods Enzymol. 1991;194:3–21. [PubMed]
  • Siddiqui AH, Brandriss MC. A regulatory region responsible for proline-specific induction of the yeast PUT2 gene is adjacent to its TATA box. Mol Cell Biol. 1988 Nov;8(11):4634–4641. [PMC free article] [PubMed]
  • Sikorski RS, Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. [PMC free article] [PubMed]
  • Sorger PK, Murray AW. S-phase feedback control in budding yeast independent of tyrosine phosphorylation of p34cdc28. Nature. 1992 Jan 23;355(6358):365–368. [PubMed]
  • Surana U, Robitsch H, Price C, Schuster T, Fitch I, Futcher AB, Nasmyth K. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell. 1991 Apr 5;65(1):145–161. [PubMed]
  • Tyers M, Tokiwa G, Futcher B. Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. EMBO J. 1993 May;12(5):1955–1968. [PMC free article] [PubMed]
  • Wittenberg C, Sugimoto K, Reed SI. G1-specific cyclins of S. cerevisiae: cell cycle periodicity, regulation by mating pheromone, and association with the p34CDC28 protein kinase. Cell. 1990 Jul 27;62(2):225–237. [PubMed]
  • Wright R, Rine J. Transmission electron microscopy and immunocytochemical studies of yeast: analysis of HMG-CoA reductase overproduction by electron microscopy. Methods Cell Biol. 1989;31:473–512. [PubMed]

Articles from Molecular Biology of the Cell are provided here courtesy of American Society for Cell Biology

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...