Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1992 Apr;130(4):703–716. doi: 10.1093/genetics/130.4.703

Commitment to Meiosis in Saccharomyces Cerevisiae: Involvement of the Spo14 Gene

S M Honigberg 1, C Conicella 1, R E Espositio 1
PMCID: PMC1204922  PMID: 1582554

Abstract

This paper describes the identification, cloning and phenotypic analysis of SPO14, a new gene required for meiosis and spore formation. Studies of strains carrying a temperature-sensitive mutation or a disruption/duplication allele indicate that spo14 mutants have the unusual property of being able to return to mitotic division, even from the late stages of meiotic development. Early meiotic events, such as DNA replication and intragenic and intergenic recombination, occur normally. In contrast, later meiotic processes are defective in spo14 mutants: the meiosis I division appears to be executed at slightly depressed levels, the meiosis II division is reduced more severely, and no spores are formed. Epistasis tests using mutants defective in recombination or reductional division support these findings. Based on these data, we suggest that the SPO14 gene product is involved in the coordinate induction of late meiotic events and that this induction is responsible for the phenomenon of commitment.

Full Text

The Full Text of this article is available as a PDF (5.1 MB).

Selected References

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

  1. Dawes I. W., Hardie I. D. Selective killing of vegetative cells in sporulated yeast cultures by exposure to diethyl ether. Mol Gen Genet. 1974;131(4):281–289. doi: 10.1007/BF00264859. [DOI] [PubMed] [Google Scholar]
  2. Dirick L., Nasmyth K. Positive feedback in the activation of G1 cyclins in yeast. Nature. 1991 Jun 27;351(6329):754–757. doi: 10.1038/351754a0. [DOI] [PubMed] [Google Scholar]
  3. Dower W. J., Miller J. F., Ragsdale C. W. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 1988 Jul 11;16(13):6127–6145. doi: 10.1093/nar/16.13.6127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dresser M. E., Giroux C. N. Meiotic chromosome behavior in spread preparations of yeast. J Cell Biol. 1988 Mar;106(3):567–573. doi: 10.1083/jcb.106.3.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Engebrecht J., Roeder G. S. Yeast mer1 mutants display reduced levels of meiotic recombination. Genetics. 1989 Feb;121(2):237–247. doi: 10.1093/genetics/121.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Esposito M. S., Esposito R. E., Arnaud M., Halvorson H. O. Conditional mutants of meiosis in yeast. J Bacteriol. 1970 Oct;104(1):202–210. doi: 10.1128/jb.104.1.202-210.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Esposito M. S., Esposito R. E. The genetic control of sporulation in Saccharomyces. I. The isolation of temperature-sensitive sporulation-deficient mutants. Genetics. 1969 Jan;61(1):79–89. doi: 10.1093/genetics/61.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Esposito R. E., Dresser M., Breitenbach M. Identifying sporulation genes, visualizing synaptonemal complexes, and large-scale spore and spore wall purification. Methods Enzymol. 1991;194:110–131. doi: 10.1016/0076-6879(91)94010-a. [DOI] [PubMed] [Google Scholar]
  9. Esposito R. E., Esposito M. S. Genetic recombination and commitment to meiosis in Saccharomyces. Proc Natl Acad Sci U S A. 1974 Aug;71(8):3172–3176. doi: 10.1073/pnas.71.8.3172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. GANESAN A. T., HOLTER H., ROBERTS C. Some observations on sporulation in Saccharomyces. C R Trav Lab Carlsberg Chim. 1958;31(1):1–6. [PubMed] [Google Scholar]
  11. 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]
  12. Hartwell L. H., Weinert T. A. Checkpoints: controls that ensure the order of cell cycle events. Science. 1989 Nov 3;246(4930):629–634. doi: 10.1126/science.2683079. [DOI] [PubMed] [Google Scholar]
  13. Horesh O., Simchen G., Friedmann A. Morphogenesis of the synapton during yeast meiosis. Chromosoma. 1979 Oct 2;75(1):101–115. doi: 10.1007/BF00330628. [DOI] [PubMed] [Google Scholar]
  14. Hoyt M. A., Totis L., Roberts B. T. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell. 1991 Aug 9;66(3):507–517. doi: 10.1016/0092-8674(81)90014-3. [DOI] [PubMed] [Google Scholar]
  15. Kassir Y., Granot D., Simchen G. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell. 1988 Mar 25;52(6):853–862. doi: 10.1016/0092-8674(88)90427-8. [DOI] [PubMed] [Google Scholar]
  16. Kilmartin J. V., 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. doi: 10.1083/jcb.93.3.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Klapholz S., Esposito R. E. Isolation of SPO12-1 and SPO13-1 from a natural variant of yeast that undergoes a single meiotic division. Genetics. 1980 Nov;96(3):567–588. doi: 10.1093/genetics/96.3.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Klapholz S., Waddell C. S., Esposito R. E. The role of the SPO11 gene in meiotic recombination in yeast. Genetics. 1985 Jun;110(2):187–216. doi: 10.1093/genetics/110.2.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Li R., Murray A. W. Feedback control of mitosis in budding yeast. Cell. 1991 Aug 9;66(3):519–531. doi: 10.1016/0092-8674(81)90015-5. [DOI] [PubMed] [Google Scholar]
  20. Malone R. E., Esposito R. E. Recombinationless meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1981 Oct;1(10):891–901. doi: 10.1128/mcb.1.10.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Menees T. M., Roeder G. S. MEI4, a yeast gene required for meiotic recombination. Genetics. 1989 Dec;123(4):675–682. doi: 10.1093/genetics/123.4.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mitchell A. P. Two switches govern entry into meiosis in yeast. Prog Clin Biol Res. 1988;267:47–66. [PubMed] [Google Scholar]
  23. Moens P. B., Rapport E. Spindles, spindle plaques, and meiosis in the yeast Saccharomyces cerevisiae (Hansen). J Cell Biol. 1971 Aug;50(2):344–361. doi: 10.1083/jcb.50.2.344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mortimer R. K., Schild D., Contopoulou C. R., Kans J. A. Genetic map of Saccharomyces cerevisiae, edition 10. Yeast. 1989 Sep-Oct;5(5):321–403. doi: 10.1002/yea.320050503. [DOI] [PubMed] [Google Scholar]
  25. Murray A. W., Kirschner M. W. Dominoes and clocks: the union of two views of the cell cycle. Science. 1989 Nov 3;246(4930):614–621. doi: 10.1126/science.2683077. [DOI] [PubMed] [Google Scholar]
  26. Murray A. W., Szostak J. W. Chromosome segregation in mitosis and meiosis. Annu Rev Cell Biol. 1985;1:289–315. doi: 10.1146/annurev.cb.01.110185.001445. [DOI] [PubMed] [Google Scholar]
  27. Padmore R., Cao L., Kleckner N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell. 1991 Sep 20;66(6):1239–1256. doi: 10.1016/0092-8674(91)90046-2. [DOI] [PubMed] [Google Scholar]
  28. Roman H, Phillips M M, Sands S M. Studies of Polyploid Saccharomyces. I. Tetraploid Segregation. Genetics. 1955 Jul;40(4):546–561. doi: 10.1093/genetics/40.4.546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  30. Schild D., Byers B. Meiotic effects of DNA-defective cell division cycle mutations of Saccharomyces cerevisiae. Chromosoma. 1978 Dec 21;70(1):109–130. doi: 10.1007/BF00292220. [DOI] [PubMed] [Google Scholar]
  31. Shilo V., Simchen G., Shilo B. Initiation of meiosis in cell cycle initiation mutants of Saccharomyces cerevisiae. Exp Cell Res. 1978 Mar 15;112(2):241–248. doi: 10.1016/0014-4827(78)90206-9. [DOI] [PubMed] [Google Scholar]
  32. Shortle D., Haber J. E., Botstein D. Lethal disruption of the yeast actin gene by integrative DNA transformation. Science. 1982 Jul 23;217(4557):371–373. doi: 10.1126/science.7046050. [DOI] [PubMed] [Google Scholar]
  33. Shuster E. O., Byers B. Pachytene arrest and other meiotic effects of the start mutations in Saccharomyces cerevisiae. Genetics. 1989 Sep;123(1):29–43. doi: 10.1093/genetics/123.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sikorski R. S., 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. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Simchen G. Are mitotic functions required in meiosis? Genetics. 1974 Apr;76(4):745–753. doi: 10.1093/genetics/76.4.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Simchen G., Piñon R., Salts Y. Sporulation in Saccharomyces cerevisiae: premeiotic DNA synthesis, readiness and commitment. Exp Cell Res. 1972 Nov;75(1):207–218. doi: 10.1016/0014-4827(72)90538-1. [DOI] [PubMed] [Google Scholar]
  37. Smith H. E., Mitchell A. P. A transcriptional cascade governs entry into meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1989 May;9(5):2142–2152. doi: 10.1128/mcb.9.5.2142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Thomas J. H., Botstein D. A gene required for the separation of chromosomes on the spindle apparatus in yeast. Cell. 1986 Jan 17;44(1):65–76. doi: 10.1016/0092-8674(86)90485-x. [DOI] [PubMed] [Google Scholar]
  39. Toda T., Uno I., Ishikawa T., Powers S., Kataoka T., Broek D., Cameron S., Broach J., Matsumoto K., Wigler M. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell. 1985 Jan;40(1):27–36. doi: 10.1016/0092-8674(85)90305-8. [DOI] [PubMed] [Google Scholar]
  40. Weinert T. A., Hartwell L. H. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science. 1988 Jul 15;241(4863):317–322. doi: 10.1126/science.3291120. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES