Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1981 Jun 1;89(3):395–405. doi: 10.1083/jcb.89.3.395

Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle

PMCID: PMC2111815  PMID: 7019215

Abstract

Temperature-sensitive yeast mutants defective in gene CDC24 continued to grow (i.e., increase in cell mass and cell volume) at restrictive temperature (36 degrees C) but were unable to form buds. Staining with the fluorescent dye Calcofluor showed that the mutants were also unable to form normal bud scars (the discrete chitin rings formed in the cell wall at budding sites) at 36 degrees C; instead, large amounts of chitin were deposited randomly over the surfaces of the growing unbudded cells. Labeling of cell-wall mannan with fluorescein isothiocyanate-conjugated concanavalin A suggested that mannan incorporation was also delocalized in mutant cells grown at 36 degrees C. Although the mutants have well-defined execution points just before bud emergence, inactivation of the CDC24 gene product in budded cells led both to selective growth of mother cells rather than of buds and to delocalized chitin deposition, indicating that the CDC24 gene product functions in the normal localization of growth in budded as well as in unbudded cells. Growth of the mutant strains at temperatures less than 36 degrees C revealed allele-specific differences in behavior. Two strains produced buds of abnormal shape during growth at 33 degrees C. Moreover, these same strains displayed abnormal localization of budding sites when growth at 24 degrees C (the normal permissive temperature for the mutants); in each case, the abnormal pattern of budding sites segregated with the temperature sensitivity in crosses. Thus, the CDC24 gene product seems to be involved in selection of the budding site, formation of the chitin ring at that site, the subsequent localization of new cell wall growth to the budding site and the growing bud, and the balance between tip growth and uniform growth of the bud that leads to the normal cell shape.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. BERGER L. R., REYNOLDS D. M. The chitinase system of a strain of Streptomyces griseus. Biochim Biophys Acta. 1958 Sep;29(3):522–534. doi: 10.1016/0006-3002(58)90008-8. [DOI] [PubMed] [Google Scholar]
  2. Byers B., Goetsch L. A highly ordered ring of membrane-associated filaments in budding yeast. J Cell Biol. 1976 Jun;69(3):717–721. doi: 10.1083/jcb.69.3.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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] [Google Scholar]
  5. Cabib E., Bowers B. Timing and function of chitin synthesis in yeast. J Bacteriol. 1975 Dec;124(3):1586–1593. doi: 10.1128/jb.124.3.1586-1593.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cabib E. Molecular aspects of yeast morphogenesis. Annu Rev Microbiol. 1975;29:191–214. doi: 10.1146/annurev.mi.29.100175.001203. [DOI] [PubMed] [Google Scholar]
  7. Culotti J., Hartwell L. H. Genetic control of the cell division cycle in yeast. 3. Seven genes controlling nuclear division. Exp Cell Res. 1971 Aug;67(2):389–401. doi: 10.1016/0014-4827(71)90424-1. [DOI] [PubMed] [Google Scholar]
  8. FREIFELDER D. Bud position in Saccharomyces cerevisiae. J Bacteriol. 1960 Oct;80:567–568. doi: 10.1128/jb.80.4.567-568.1960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Farkas V. Biosynthesis of cell walls of fungi. Microbiol Rev. 1979 Jun;43(2):117–144. doi: 10.1128/mr.43.2.117-144.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Farkas V., Kovarík J., Kosinová A., Bauer S. Autoradiographic study of mannan incorporation into the growing cell walls of Saccharomyces cerevisiae. J Bacteriol. 1974 Jan;117(1):265–269. doi: 10.1128/jb.117.1.265-269.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Field C., Schekman R. Localized secretion of acid phosphatase reflects the pattern of cell surface growth in Saccharomyces cerevisiae. J Cell Biol. 1980 Jul;86(1):123–128. doi: 10.1083/jcb.86.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hartwell L. H., Culotti J., Pringle J. R., Reid B. J. Genetic control of the cell division cycle in yeast. Science. 1974 Jan 11;183(4120):46–51. doi: 10.1126/science.183.4120.46. [DOI] [PubMed] [Google Scholar]
  13. Hartwell L. H., Culotti J., Reid B. Genetic control of the cell-division cycle in yeast. I. Detection of mutants. Proc Natl Acad Sci U S A. 1970 Jun;66(2):352–359. doi: 10.1073/pnas.66.2.352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hartwell L. H. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res. 1971 Dec;69(2):265–276. doi: 10.1016/0014-4827(71)90223-0. [DOI] [PubMed] [Google Scholar]
  15. Hartwell L. H. Macromolecule synthesis in temperature-sensitive mutants of yeast. J Bacteriol. 1967 May;93(5):1662–1670. doi: 10.1128/jb.93.5.1662-1670.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hartwell L. H., Mortimer R. K., Culotti J., Culotti M. Genetic Control of the Cell Division Cycle in Yeast: V. Genetic Analysis of cdc Mutants. Genetics. 1973 Jun;74(2):267–286. doi: 10.1093/genetics/74.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hartwell L. H. Periodic density fluctuation during the yeast cell cycle and the selection of synchronous cultures. J Bacteriol. 1970 Dec;104(3):1280–1285. doi: 10.1128/jb.104.3.1280-1285.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hartwell L. H. Saccharomyces cerevisiae cell cycle. Bacteriol Rev. 1974 Jun;38(2):164–198. doi: 10.1128/br.38.2.164-198.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hartwell L. H., Unger M. W. 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. doi: 10.1083/jcb.75.2.422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hicks J. B., Strathern J. N., Herskowitz I. Interconversion of Yeast Mating Types III. Action of the Homothallism (HO) Gene in Cells Homozygous for the Mating Type Locus. Genetics. 1977 Mar;85(3):395–405. doi: 10.1093/genetics/85.3.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Johnson B. F., Gibson E. J. Autoradiographic analysis of regional cell wall growth of yeasts. III. Saccharomyces cerevisiae. Exp Cell Res. 1966 Mar;41(3):580–591. doi: 10.1016/s0014-4827(66)80108-8. [DOI] [PubMed] [Google Scholar]
  22. Johnston G. C., Pringle J. R., Hartwell L. H. Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp Cell Res. 1977 Mar 1;105(1):79–98. doi: 10.1016/0014-4827(77)90154-9. [DOI] [PubMed] [Google Scholar]
  23. Pringle J. R. Induction, selection, and experimental uses of temperature-sensitive and other conditional mutants of yeast. Methods Cell Biol. 1975;12:233–272. doi: 10.1016/s0091-679x(08)60959-0. [DOI] [PubMed] [Google Scholar]
  24. Pringle J. R., Mor J. R. Methods for monitoring the growth of yeast cultures and for dealing with the clumping problem. Methods Cell Biol. 1975;11:131–168. doi: 10.1016/s0091-679x(08)60320-9. [DOI] [PubMed] [Google Scholar]
  25. Pringle J. R. The use of conditional lethal cell cycle mutants for temporal and functional sequence mapping of cell cycle events. J Cell Physiol. 1978 Jun;95(3):393–405. doi: 10.1002/jcp.1040950318. [DOI] [PubMed] [Google Scholar]
  26. REISSIG J. L., STORMINGER J. L., LELOIR L. F. A modified colorimetric method for the estimation of N-acetylamino sugars. J Biol Chem. 1955 Dec;217(2):959–966. [PubMed] [Google Scholar]
  27. Schekman R., Brawley V. Localized deposition of chitin on the yeast cell surface in response to mating pheromone. Proc Natl Acad Sci U S A. 1979 Feb;76(2):645–649. doi: 10.1073/pnas.76.2.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Seichertová O., Beran K., Holan Z., Pokorný V. The chitin-glucan complex of Saccharomyces cerevisiae. II. Location of the complex in the encircling region of the bud sear. Folia Microbiol (Praha) 1973;18(3):207–211. doi: 10.1007/BF02872858. [DOI] [PubMed] [Google Scholar]
  29. Seichertová O., Beran K., Holan Z., Pokorný V. The chitin-glucan complex of Saccharomyces cerevisiae. III. Electron-microscopic study of the prebudding stage. Folia Microbiol (Praha) 1975;20(5):371–378. doi: 10.1007/BF02877037. [DOI] [PubMed] [Google Scholar]
  30. Shearn A., Hersperger G., Hersperger E., Pentz E. S., Denker P. Multiple Allele Approach to the Study of Genes in DROSOPHILA MELANOGASTER That Are Involved in Imaginal Disc Development. Genetics. 1978 Jun;89(2):355–370. doi: 10.1093/genetics/89.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sloat B. F., Pringle J. R. A mutant of yeast defective in cellular morphogenesis. Science. 1978 Jun 9;200(4346):1171–1173. doi: 10.1126/science.349694. [DOI] [PubMed] [Google Scholar]
  32. Tkacz J. S., Cybulska E. B., Lampen J. O. Specific staining of wall mannan in yeast cells with fluorescein-conjugated concanavalin A. J Bacteriol. 1971 Jan;105(1):1–5. doi: 10.1128/jb.105.1.1-5.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tkacz J. S., Lampen J. O. Wall replication in saccharomyces species: use of fluorescein-conjugated concanavalin A to reveal the site of mannan insertion. J Gen Microbiol. 1972 Sep;72(2):243–247. doi: 10.1099/00221287-72-2-243. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Wilkinson L. E., Pringle J. R. Transient G1 arrest of S. cerevisiae cells of mating type alpha by a factor produced by cells of mating type a. Exp Cell Res. 1974 Nov;89(1):175–187. doi: 10.1016/0014-4827(74)90200-6. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES