Skip to main content
Molecular Biology of the Cell logoLink to Molecular Biology of the Cell
. 1992 Apr;3(4):429–444. doi: 10.1091/mbc.3.4.429

Actin- and tubulin-dependent functions during Saccharomyces cerevisiae mating projection formation.

E B Read 1, H H Okamura 1, D G Drubin 1
PMCID: PMC275593  PMID: 1498363

Abstract

Several conditional-lethal mutant alleles of the single-copy Saccharomyces cerevisiae beta-tubulin and actin genes were used to evaluate the roles of microtubules and actin filaments in the pheromone-induced extension of mating projections. Mutants defective in tubulin assembly form projections indistinguishable in appearance from those formed by wild-type cells. However, the tubulin mutants are unable to move their nuclei into the projections and to orient the spindle pole body associated with each nucleus toward the projection tip. Actin mutants are defective in spatial orientation of cell-surface growth required for formation of normal mating projections. Migration of nuclei into mating projections and Spa2p segregation to projection tips are also defective in actin mutants. Studies with abp1 null mutants showed that the function of the Abp1p actin-binding protein is either not required for projection formation or there are other proteins in yeast with similar functions. Our findings demonstrate that actin is required to restrict cell-surface growth to a defined region for pheromone-induced morphogenesis and suggest that nuclear position and orientation in mating projections depend on direct or indirect interaction of microtubules with actin filaments.

Full text

PDF
442

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams A. E., Botstein D., Drubin D. G. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature. 1991 Dec 5;354(6352):404–408. doi: 10.1038/354404a0. [DOI] [PubMed] [Google Scholar]
  2. Adams A. E., Johnson D. I., Longnecker R. M., Sloat B. F., Pringle J. R. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J Cell Biol. 1990 Jul;111(1):131–142. doi: 10.1083/jcb.111.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Adams A. E., Pringle J. R. 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. doi: 10.1083/jcb.98.3.934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Albrecht-Buehler G. Does the geometric design of centrioles imply their function? Cell Motil. 1981;1(2):237–245. doi: 10.1002/cm.970010206. [DOI] [PubMed] [Google Scholar]
  5. Baba M., Baba N., Ohsumi Y., Kanaya K., Osumi M. Three-dimensional analysis of morphogenesis induced by mating pheromone alpha factor in Saccharomyces cerevisiae. J Cell Sci. 1989 Oct;94(Pt 2):207–216. doi: 10.1242/jcs.94.2.207. [DOI] [PubMed] [Google Scholar]
  6. Barnes G., Drubin D. G., Stearns T. The cytoskeleton of Saccharomyces cerevisiae. Curr Opin Cell Biol. 1990 Feb;2(1):109–115. doi: 10.1016/s0955-0674(05)80040-7. [DOI] [PubMed] [Google Scholar]
  7. Byers B., Goetsch L. Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae. J Bacteriol. 1975 Oct;124(1):511–523. doi: 10.1128/jb.124.1.511-523.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cassimeris L. U., Wadsworth P., Salmon E. D. Dynamics of microtubule depolymerization in monocytes. J Cell Biol. 1986 Jun;102(6):2023–2032. doi: 10.1083/jcb.102.6.2023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cross F., Hartwell L. H., Jackson C., Konopka J. B. Conjugation in Saccharomyces cerevisiae. Annu Rev Cell Biol. 1988;4:429–457. doi: 10.1146/annurev.cb.04.110188.002241. [DOI] [PubMed] [Google Scholar]
  10. Delgado M. A., Conde J. Benomyl prevents nuclear fusion in Saccharomyces cerevisiae. Mol Gen Genet. 1984;193(1):188–189. doi: 10.1007/BF00327435. [DOI] [PubMed] [Google Scholar]
  11. Drubin D. G. Development of cell polarity in budding yeast. Cell. 1991 Jun 28;65(7):1093–1096. doi: 10.1016/0092-8674(91)90001-f. [DOI] [PubMed] [Google Scholar]
  12. Drubin D. G., Kirschner M. W. Tau protein function in living cells. J Cell Biol. 1986 Dec;103(6 Pt 2):2739–2746. doi: 10.1083/jcb.103.6.2739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Drubin D. G., Miller K. G., Botstein D. Yeast actin-binding proteins: evidence for a role in morphogenesis. J Cell Biol. 1988 Dec;107(6 Pt 2):2551–2561. doi: 10.1083/jcb.107.6.2551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Drubin D. G., Mulholland J., Zhu Z. M., Botstein D. Homology of a yeast actin-binding protein to signal transduction proteins and myosin-I. Nature. 1990 Jan 18;343(6255):288–290. doi: 10.1038/343288a0. [DOI] [PubMed] [Google Scholar]
  15. Gehrung S., Snyder M. The SPA2 gene of Saccharomyces cerevisiae is important for pheromone-induced morphogenesis and efficient mating. J Cell Biol. 1990 Oct;111(4):1451–1464. doi: 10.1083/jcb.111.4.1451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Harold F. M. To shape a cell: an inquiry into the causes of morphogenesis of microorganisms. Microbiol Rev. 1990 Dec;54(4):381–431. doi: 10.1128/mr.54.4.381-431.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hasek J., Rupes I., Svobodová J., Streiblová E. Tubulin and actin topology during zygote formation of Saccharomyces cerevisiae. J Gen Microbiol. 1987 Dec;133(12):3355–3363. doi: 10.1099/00221287-133-12-3355. [DOI] [PubMed] [Google Scholar]
  18. Herskowitz I. A regulatory hierarchy for cell specialization in yeast. Nature. 1989 Dec 14;342(6251):749–757. doi: 10.1038/342749a0. [DOI] [PubMed] [Google Scholar]
  19. Huffaker T. C., Thomas J. H., Botstein D. Diverse effects of beta-tubulin mutations on microtubule formation and function. J Cell Biol. 1988 Jun;106(6):1997–2010. doi: 10.1083/jcb.106.6.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jackson C. L., Hartwell L. H. Courtship in Saccharomyces cerevisiae: an early cell-cell interaction during mating. Mol Cell Biol. 1990 May;10(5):2202–2213. doi: 10.1128/mcb.10.5.2202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jackson C. L., Konopka J. B., Hartwell L. H. S. cerevisiae alpha pheromone receptors activate a novel signal transduction pathway for mating partner discrimination. Cell. 1991 Oct 18;67(2):389–402. doi: 10.1016/0092-8674(91)90190-a. [DOI] [PubMed] [Google Scholar]
  22. Jacobs C. W., Adams A. E., Szaniszlo P. J., Pringle J. R. Functions of microtubules in the Saccharomyces cerevisiae cell cycle. J Cell Biol. 1988 Oct;107(4):1409–1426. doi: 10.1083/jcb.107.4.1409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kilmartin J. V., Adams A. E. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J Cell Biol. 1984 Mar;98(3):922–933. doi: 10.1083/jcb.98.3.922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kobori H., Yamada N., Taki A., Osumi M. Actin is associated with the formation of the cell wall in reverting protoplasts of the fission yeast Schizosaccharomyces pombe. J Cell Sci. 1989 Dec;94(Pt 4):635–646. doi: 10.1242/jcs.94.4.635. [DOI] [PubMed] [Google Scholar]
  25. Kupfer A., Singer S. J. Cell biology of cytotoxic and helper T cell functions: immunofluorescence microscopic studies of single cells and cell couples. Annu Rev Immunol. 1989;7:309–337. doi: 10.1146/annurev.iy.07.040189.001521. [DOI] [PubMed] [Google Scholar]
  26. Lipke P. N., Taylor A., Ballou C. E. Morphogenic effects of alpha-factor on Saccharomyces cerevisiae a cells. J Bacteriol. 1976 Jul;127(1):610–618. doi: 10.1128/jb.127.1.610-618.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Liu H. P., Bretscher A. Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell. 1989 Apr 21;57(2):233–242. doi: 10.1016/0092-8674(89)90961-6. [DOI] [PubMed] [Google Scholar]
  28. Meluh P. B., Rose M. D. KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell. 1990 Mar 23;60(6):1029–1041. doi: 10.1016/0092-8674(90)90351-e. [DOI] [PubMed] [Google Scholar]
  29. Moore S. A. Comparison of dose-response curves for alpha factor-induced cell division arrest, agglutination, and projection formation of yeast cells. Implication for the mechanism of alpha factor action. J Biol Chem. 1983 Nov 25;258(22):13849–13856. [PubMed] [Google Scholar]
  30. Novick P., Botstein D. Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell. 1985 Feb;40(2):405–416. doi: 10.1016/0092-8674(85)90154-0. [DOI] [PubMed] [Google Scholar]
  31. Pringle J. R., Preston R. A., Adams A. E., Stearns T., Drubin D. G., Haarer B. K., Jones E. W. Fluorescence microscopy methods for yeast. Methods Cell Biol. 1989;31:357–435. doi: 10.1016/s0091-679x(08)61620-9. [DOI] [PubMed] [Google Scholar]
  32. Rose M. D., Fink G. R. KAR1, a gene required for function of both intranuclear and extranuclear microtubules in yeast. Cell. 1987 Mar 27;48(6):1047–1060. doi: 10.1016/0092-8674(87)90712-4. [DOI] [PubMed] [Google Scholar]
  33. Schulze E., Kirschner M. Microtubule dynamics in interphase cells. J Cell Biol. 1986 Mar;102(3):1020–1031. doi: 10.1083/jcb.102.3.1020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Snyder M., Gehrung S., Page B. D. Studies concerning the temporal and genetic control of cell polarity in Saccharomyces cerevisiae. J Cell Biol. 1991 Aug;114(3):515–532. doi: 10.1083/jcb.114.3.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Snyder M. The SPA2 protein of yeast localizes to sites of cell growth. J Cell Biol. 1989 Apr;108(4):1419–1429. doi: 10.1083/jcb.108.4.1419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tkacz J. S., MacKay V. L. Sexual conjugation in yeast. Cell surface changes in response to the action of mating hormones. J Cell Biol. 1979 Feb;80(2):326–333. doi: 10.1083/jcb.80.2.326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Trueheart J., Boeke J. D., Fink G. R. Two genes required for cell fusion during yeast conjugation: evidence for a pheromone-induced surface protein. Mol Cell Biol. 1987 Jul;7(7):2316–2328. doi: 10.1128/mcb.7.7.2316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Watzele M., Klis F., Tanner W. Purification and characterization of the inducible a agglutinin of Saccharomyces cerevisiae. EMBO J. 1988 May;7(5):1483–1488. doi: 10.1002/j.1460-2075.1988.tb02966.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES