Abstract
The meiotic effects of several cell division cycle (cdc) mutations of Saccharomyces cerevisiae have been investigated by electron microscopy and by genetic and biochemical methods. Diploid strains homozygous for cdc mutations known to confer defects on vegetative DNA synthesis were subjected to restrictive conditions during meiosis. Electron microscopy revealed that all four mutants were conditionally arrested in meiosis after duplication of the spindle pole bodies but before spindle formation for the first meiotic division. None of these mutants became committed to recombination or contained synaptonemal complex at the meiotic arrest. — The mutants differed in their ability to undergo premeiotic DNA synthesis under restrictive conditions. Both cdc8 and cdc21, which are defective in the propagation of vegetative DNA synthesis, also failed to undergo premeiotic DNA synthesis. The arrest of these mutants at the stage before meiosis I spindle formation could be attributed to the failure of DNA synthesis because inhibition of synthesis by hydroxyurea also caused arrest at this stage. — Premeiotic DNA synthesis occurred before the arrest of cdc7, which is defective in the initiation of vegetative DNA synthesis, and of cdc2, which synthesizes vegetative DNA but does so defectively. The meiotic arrest of cdc7 homozygotes was partially reversible. Even if further semiconservative DNA replication was inhibited by the addition of hydroxyurea, released cells rapidly underwent commitment to recombination and formation of synaptonemal complexes. The cdc7 homozygote is therefore reversibly arrested in meiosis after DNA replication, whereas vegetative cultures have previously been shown to be defective only in the initiation of DNA synthesis.
Similar content being viewed by others
References
Baker, B.S., Carpenter, A.T.C., Esposito, M.S., Esposito, R.E., Sandler, L.: The genetic control of meiosis. Ann. Rev. Genet. 10, 53–134 (1976)
Bisson, L., Thorner, J.: Thymidine-5′-monophosphate-requiring mutants of Saccharomyces cerevisiae are deficient in thymidylate synthetase. J. Bact. 132, 44–50 (1977)
Byers, B., Goetsch, L.: Duplication of spindle plaques and integration of the yeast cell cycle. Cold Spr. Harb. Symp. quant. Biol. 38, 123–131 (1974)
Byers, B., Goetsch, L.: Electron microscopic observations on the meiotic karyotype of diploid and tetraploid Saccharomyces cerevisiae. Proc. nat. Acad. Sci. (Wash.) 72, 5056–5060 (1975)
Croes, A.F.: Induction of meiosis in yeast. I. Timing of cytological and biochemical events. Planta (Berl.) 76, 209–226 (1967)
Esposito, M.S., Esposito, R.E.: Mutants of meiosis and ascospore formation. In: Methods in cell biology (D.M. Prescott, ed.) vol. 11, pp. 303–326. New York: Academic Press 1975
Esposito, R.E., Esposito, M.S.: Genetic recombination and commitment to meiosis in Saccharomyces. Proc. nat. Acad. Sci. (Wash.) 71, 3172–3176 (1974)
Fogel, S., Roth, R.: Mutations affecting meiotic gene conversion in yeast. Molec. gen. Genet. 130, 189–201 (1974)
Game, J.C.: Yeast cell cycle mutant cdc21 is a temperature-sensitive thymidylate auxotroph. Molec. gen. Genet. 146, 313–315 (1976)
Gowen, J.W.: Meiosis as a genetic character in Drosophila melanogaster J. exp. Zool. 65, 83–106 (1933)
Gowen, M.S., Gowen, J.W.: Complete linkage in Drosophila melanogaster. Amer. Naturalist 56, 286–288 (1922)
Hartwell, L.H.: Macromolecule synthesis in temperature-sensitive mutants of yeast. J. Bact. 93, 1662–1670 (1967)
Hartwell, L.H.: Three additional genes required for deoxyribonucleic acid synthesis in Saccharomyces cerevisiae. J. Bact. 115, 966–974 (1973)
Hartwell, L.H.: Saccharomyces cerevisiae cell cycle. Bact. Rev. 38, 164–198 (1974)
Hartwell, L.H.: Sequential function of gene products relative to DNA synthesis in the yeast cell cycle. J. molec. Biol. 104, 803–817 (1976)
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 74, 267–286 (1973)
Henderson, S.A.: The time and place of meiotic crossing over. Ann. Rev. Genet. 4, 295–324 (1970)
Hopper, A.K., Hall, B.D.: Mating type and sporulation in yeast. I. Mutations which alter matingtype control over sporulation. Genetics 80, 41–59 (1975)
Hopper, A.K., Kirsch, J., Hall, B.D.: Mating type and sporulation in yeast. II. Meiosis, recombination, and radiation sensitivity in an αα diploid with altered sporulation control. Genetics 80, 61–76 (1975)
Hotta, Y., Chandley, A.C., Stern, H.: Biochemical analysis of meiosis in the male mouse. II. DNA metabolism at pachytene. Chromosoma (Berl.) 62, 255–268 (1977)
Hotta, Y., Ito, M., Stern, H.: Synthesis of DNA during meiosis. Proc. nat. Acad. Sci (Wash.) 56, 1184–1191 (1966)
Hotta, Y., Stern, H.: Analysis of DNA synthesis during meiotic prophase in Lilium. J. molec. Biol. 55, 337–355 (1971)
Kissane, J.M., Robins, E.: The fluorometric measurement of DNA in animal tissues with special reference to the central nervous system. J. biol. Chem. 233, 184–188 (1958)
Lindsley, D.L., Sandler, L.: The genetic analysis of meiosis in female Drosophila melanogaster. Phil. Trans. roy. Soc. London, B 277, 295–312 (1977)
Lu, B.C., Jeng, D.Y.: Meiosis in Coprinus. VII. The prekaryogamy S-phase and the postkaryogamy DNA replication in C. lagopus. J. Cell Sci. 17, 461–470 (1975)
Moens, P.B., Esposito, R.E., Esposito, M.S.: Aberrant nuclear behavior at meiosis and anucleate spore formation by sporulation-deficient (spo) mutants of Saccharomyces cerevisiae. Exp. Cell Res. 83, 166–174 (1974)
Moens, P.B., Mowat, M., Esposito, M.S., Esposito, R.E.: Meiosis in a temperature-sensitive DNA-synthesis mutant and in an apomictic yeast strain (Saccharomyces cerevisiae). Phil. Trans. roy. Soc. London, B 277, 351–358 (1977)
Newlon, C.S., Fangman, W.L.: Mitochondrial DNA synthesis in cell cycle mutants of Saccharomyces cerevisiae. Cell 5, 423–428 (1975)
Rossen, J.M., Westergaard, M.: Studies on the mechanism of crossing over. II. Meiosis and the time of meiotic chromosome replication in the ascomycete Neottiella rutilans (Fr.) Dennis. C.R. Trav. Lab. Carlsberg 35, 233–260 (1966)
Roth, R.: Chromosome replication during meiosis: identification of gene functions required for premeiotic DNA synthesis. Proc. nat. Acad. Sci. (Wash.) 70, 3087–3091 (1973)
Roth, R., Fogel, S.: A system selective for yeast mutants deficient in meiotic recombination. Molec. gen. Genet. 112, 295–305 (1971)
Roth, T.F., Ito, M.: DNA dependent formation of the synaptinemal complex at meiotic prophase. J. Cell. Biol. 35, 247–255 (1967)
Schild, D., Byers, B.: Terminal phenotypes in meiosis of DNA-defective cdc mutants of yeast. Genetics 86, s56 (1977)
Sherman, F., Roman, H.: Evidence for two types of allelic recombination in yeast. Genetics 48, 255–261 (1963)
Silva-Lopez, E., Zamb, T.J., Roth, R.: Role of premeiotic replication in gene conversion. Nature (Lond.) 253, 212–214 (1975)
Simchen, G.: Are mitotic functions required in meiosis? Genetics 76, 745–753 (1974)
Simchen, G., Hirschberg, J.: Effects of the mitotic cell-cycle mutation cdc4 on yeast meiosis. Genetics 86, 57–72 (1977)
Simchen, G., Idar, D., Kassir, Y.: Recombination and hydroxyurea inhibition of DNA synthesis in yeast meiosis. Molec. gen. Genet. 144, 21–27 (1976)
Simonet, J.M.: Mutations affecting meiosis in Podospora anserina. II. Effect of mei2 mutants on recombination. Molec. gen. Genet. 123, 263–281 (1973)
Slater, M.L.: Effect of reversible inhibition of deoxyribonucleic acid synthesis on the yeast cell cycle. J. Bact. 113, 263–270 (1973)
Westergaard, M., Wettstein, D. von: The synaptinemal complex. Ann. Rev. Genet. 6, 71–110 (1972)
Woods, D.R., Bevan, E.A.: Studies on the nature of the killer factor produced by Saccharomyces cerevisiae. J. gen. Microbiol. 51, 115–126 (1968)
Zamb, T.J., Roth, R.: Role of mitotic replication genes in chromosome duplication during meiosis. Proc. nat. Acad. Sci. (Wash.) 74, 3951–3955 (1977)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Schild, D., Byers, B. Meiotic effects of DNA-defective cell division cycle mutations of Saccharomyces cerevisiae . Chromosoma 70, 109–130 (1978). https://doi.org/10.1007/BF00292220
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00292220