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. 1989 Sep;123(1):29–43. doi: 10.1093/genetics/123.1.29

Pachytene Arrest and Other Meiotic Effects of the Start Mutations in Saccharomyes Cerevisiae

E O Shuster 1, B Byers 1
PMCID: PMC1203788  PMID: 2680756

Abstract

Mutations in the Start class of cell division cycle genes (CDC28, CDC36 and CDC39) define the point in the G(1) phase of the vegetative cycle at which the cell becomes committed to completing another round of cell division. Genetic, cytological and biochemical data demonstrate that these mutations cause meiotic cells to become arrested at pachytene following completion of both chromosomal DNA replication and spindle pole body (SPB) duplication. In contrast these mutations have previously been found to cause arrest of the mitotic cell cycle prior to either of these landmark events, so the role of the Start genes in these events during vegetative growth must be indirect. Our observations are consistent with the hypothesis that CDC28, CDC36 and CDC39 are required for irreversible commitment to nuclear division in both the mitotic and meiotic pathways. CDC28 was additionally found to be required for the SPB separation that precedes spindle formation in preparation for the second meiotic division. Cytological and genetic analyses of this requirement revealed both that such separation may fail independently at either SPB and that ascospore formation can proceed independently of SPB separation.

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Selected References

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  1. Baker B. S., Carpenter A. T., Esposito M. S., Esposito R. E., Sandler L. The genetic control of meiosis. Annu Rev Genet. 1976;10:53–134. doi: 10.1146/annurev.ge.10.120176.000413. [DOI] [PubMed] [Google Scholar]
  2. Beach D., Durkacz B., Nurse P. Functionally homologous cell cycle control genes in budding and fission yeast. Nature. 1982 Dec 23;300(5894):706–709. doi: 10.1038/300706a0. [DOI] [PubMed] [Google Scholar]
  3. Boutelet F., Petitjean A., Hilger F. Yeast cdc35 mutants are defective in adenylate cyclase and are allelic with cyr1 mutants while CAS1, a new gene, is involved in the regulation of adenylate cyclase. EMBO J. 1985 Oct;4(10):2635–2641. doi: 10.1002/j.1460-2075.1985.tb03981.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Byers B., Goetsch L. Electron microscopic observations on the meiotic karyotype of diploid and tetraploid Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5056–5060. doi: 10.1073/pnas.72.12.5056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Byers B., Goetsch L. Reversible pachytene arrest of Saccharomyces cerevisiae at elevated temperature. Mol Gen Genet. 1982;187(1):47–53. doi: 10.1007/BF00384382. [DOI] [PubMed] [Google Scholar]
  7. Campbell D. Association of disomic chromosome loss with EMS-induced conversion in yeast. Genetics. 1980 Nov;96(3):613–625. doi: 10.1093/genetics/96.3.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Davidow L. S., Byers B. Enhanced gene conversion and postmeiotic segregation in pachytene-arrested Saccharomyces cerevisiae. Genetics. 1984 Feb;106(2):165–183. doi: 10.1093/genetics/106.2.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Davidow L. S., Goetsch L., Byers B. Preferential Occurrence of Nonsister Spores in Two-Spored Asci of SACCHAROMYCES CEREVISIAE: Evidence for Regulation of Spore-Wall Formation by the Spindle Pole Body. Genetics. 1980 Mar;94(3):581–595. doi: 10.1093/genetics/94.3.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dunphy W. G., Brizuela L., Beach D., Newport J. The Xenopus cdc2 protein is a component of MPF, a cytoplasmic regulator of mitosis. Cell. 1988 Jul 29;54(3):423–431. doi: 10.1016/0092-8674(88)90205-x. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Ferguson J., Ho J. Y., Peterson T. A., Reed S. I. Nucleotide sequence of the yeast cell division cycle start genes CDC28, CDC36, CDC37, and CDC39, and a structural analysis of the predicted products. Nucleic Acids Res. 1986 Aug 26;14(16):6681–6697. doi: 10.1093/nar/14.16.6681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Goetsch L., Byers B. Meiotic cytology of Saccharomyces cerevisiae in protoplast lysates. Mol Gen Genet. 1982;187(1):54–60. doi: 10.1007/BF00384383. [DOI] [PubMed] [Google Scholar]
  15. Golubovskaya I. N. Genetic control of meiosis. Int Rev Cytol. 1979;58:247–290. doi: 10.1016/s0074-7696(08)61477-1. [DOI] [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. Hayles J., Aves S., Nurse P. suc1 is an essential gene involved in both the cell cycle and growth in fission yeast. EMBO J. 1986 Dec 1;5(12):3373–3379. doi: 10.1002/j.1460-2075.1986.tb04653.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Henderson S. A. The time and place of meiotic crossing-over. Annu Rev Genet. 1970;4:295–324. doi: 10.1146/annurev.ge.04.120170.001455. [DOI] [PubMed] [Google Scholar]
  19. Hereford L. M., Hartwell L. H. Sequential gene function in the initiation of Saccharomyces cerevisiae DNA synthesis. J Mol Biol. 1974 Apr 15;84(3):445–461. doi: 10.1016/0022-2836(74)90451-3. [DOI] [PubMed] [Google Scholar]
  20. Hopper A. K., Hall B. D. Mating type and sporulation in yeast. I. Mutations which alter mating-type control over sporulation. Genetics. 1975 May;80(1):41–59. doi: 10.1093/genetics/80.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. KISSANE J. M., ROBINS E. The fluorometric measurement of deoxyribonucleic acid in animal tissues with special reference to the central nervous system. J Biol Chem. 1958 Jul;233(1):184–188. [PubMed] [Google Scholar]
  23. Kassir Y., Simchen G. Meiotic recombination and DNA synthesis in a new cell cycle mutant of Saccharomyces cerevisiae. Genetics. 1978 Sep;90(1):49–68. doi: 10.1093/genetics/90.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lee M. G., Norbury C. J., Spurr N. K., Nurse P. Regulated expression and phosphorylation of a possible mammalian cell-cycle control protein. Nature. 1988 Jun 16;333(6174):676–679. doi: 10.1038/333676a0. [DOI] [PubMed] [Google Scholar]
  25. Lee M. G., Nurse P. Complementation used to clone a human homologue of the fission yeast cell cycle control gene cdc2. Nature. 1987 May 7;327(6117):31–35. doi: 10.1038/327031a0. [DOI] [PubMed] [Google Scholar]
  26. Lörincz A. T., Reed S. I. Primary structure homology between the product of yeast cell division control gene CDC28 and vertebrate oncogenes. Nature. 1984 Jan 12;307(5947):183–185. doi: 10.1038/307183a0. [DOI] [PubMed] [Google Scholar]
  27. Lörincz A. T., Reed S. I. Sequence analysis of temperature-sensitive mutations in the Saccharomyces cerevisiae gene CDC28. Mol Cell Biol. 1986 Nov;6(11):4099–4103. doi: 10.1128/mcb.6.11.4099-4103.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Matsumoto K., Uno I., Ishikawa T. Initiation of meiosis in yeast mutants defective in adenylate cyclase and cyclic AMP-dependent protein kinase. Cell. 1983 Feb;32(2):417–423. doi: 10.1016/0092-8674(83)90461-0. [DOI] [PubMed] [Google Scholar]
  29. Matsumoto K., Uno I., Oshima Y., Ishikawa T. Isolation and characterization of yeast mutants deficient in adenylate cyclase and cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2355–2359. doi: 10.1073/pnas.79.7.2355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mendenhall M. D., Jones C. A., Reed S. I. Dual regulation of the yeast CDC28-p40 protein kinase complex: cell cycle, pheromone, and nutrient limitation effects. Cell. 1987 Sep 11;50(6):927–935. doi: 10.1016/0092-8674(87)90519-8. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Moens P. B., Rapport E. Synaptic structures in the nuclei of sporulating yeast, Saccharomyces cerevisiae (Hansen). J Cell Sci. 1971 Nov;9(3):665–677. doi: 10.1242/jcs.9.3.665. [DOI] [PubMed] [Google Scholar]
  33. Mortimer R. K., Hawthorne D. C. Genetic mapping in yeast. Methods Cell Biol. 1975;11:221–233. doi: 10.1016/s0091-679x(08)60325-8. [DOI] [PubMed] [Google Scholar]
  34. Mortimer R. K., Schild D. Genetic map of Saccharomyces cerevisiae, edition 9. Microbiol Rev. 1985 Sep;49(3):181–213. doi: 10.1128/mr.49.3.181-213.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. 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. doi: 10.1038/292558a0. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. ROMAN H. Studies of gene mutation in Saccharomyces. Cold Spring Harb Symp Quant Biol. 1956;21:175–185. doi: 10.1101/sqb.1956.021.01.015. [DOI] [PubMed] [Google Scholar]
  39. Reed S. I. The selection of S. cerevisiae mutants defective in the start event of cell division. Genetics. 1980 Jul;95(3):561–577. doi: 10.1093/genetics/95.3.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Reed S. I. The selection of amber mutations in genes required for completion of start, the controlling event of the cell division cycle of S. cerevisiae. Genetics. 1980 Jul;95(3):579–588. doi: 10.1093/genetics/95.3.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rhoades M. M., Dempsey E. Induction of chromosome doubling at meiosis by the elongate gene in maize. Genetics. 1966 Aug;54(2):505–522. doi: 10.1093/genetics/54.2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. SHERMAN F., ROMAN H. Evidence for two types of allelic recombination in yeast. Genetics. 1963 Feb;48:255–261. doi: 10.1093/genetics/48.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Schild D., Byers B. Diploid spore formation and other meiotic effects of two cell-division-cycle mutations of Saccharomyces cerevisiae. Genetics. 1980 Dec;96(4):859–876. doi: 10.1093/genetics/96.4.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. 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]
  46. Shuster J. R. "Start" mutants of Saccharomyces cerevisiae are suppressed in carbon catabolite-derepressing medium. J Bacteriol. 1982 Aug;151(2):1059–1061. doi: 10.1128/jb.151.2.1059-1061.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Shuster J. R. Mating-defective ste mutations are suppressed by cell division cycle start mutations in Saccharomyces cerevisiae. Mol Cell Biol. 1982 Sep;2(9):1052–1063. doi: 10.1128/mcb.2.9.1052-1063.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Simchen G., Kassir Y., Horesh-Cabilly O., Friedmann A. Elevated recombination and pairing structures during meiotic arrest in yeast of the nuclear division mutant cdc5. Mol Gen Genet. 1981;184(1):46–51. doi: 10.1007/BF00271193. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Stern H., Hotta Y. Biochemical controls of meiosis. Annu Rev Genet. 1973;7:37–66. doi: 10.1146/annurev.ge.07.120173.000345. [DOI] [PubMed] [Google Scholar]
  51. Williamson D. H., Fennell D. J. The use of fluorescent DNA-binding agent for detecting and separating yeast mitochondrial DNA. Methods Cell Biol. 1975;12:335–351. doi: 10.1016/s0091-679x(08)60963-2. [DOI] [PubMed] [Google Scholar]
  52. Williamson D. H., Johnston L. H., Fennell D. J., Simchen G. The timing of the S phase and other nuclear events in yeast meiosis. Exp Cell Res. 1983 Apr 15;145(1):209–217. doi: 10.1016/s0014-4827(83)80022-6. [DOI] [PubMed] [Google Scholar]
  53. Wolfner M., Yep D., Messenguy F., Fink G. R. Integration of amino acid biosynthesis into the cell cycle of Saccharomyces cerevisiae. J Mol Biol. 1975 Aug 5;96(2):273–290. doi: 10.1016/0022-2836(75)90348-4. [DOI] [PubMed] [Google Scholar]
  54. Zamb T. J., Roth R. Role of mitotic replication genes in chromosome duplication during meiosis. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3951–3955. doi: 10.1073/pnas.74.9.3951. [DOI] [PMC free article] [PubMed] [Google Scholar]

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