Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1994 Apr 15;13(8):1881–1887. doi: 10.1002/j.1460-2075.1994.tb06457.x

A zinc finger protein controls the onset of premeiotic DNA synthesis of fission yeast in a Mei2-independent cascade.

A Sugiyama 1, K Tanaka 1, K Okazaki 1, H Nojima 1, H Okayama 1
PMCID: PMC395029  PMID: 8168486

Abstract

In the fission yeast Schizosaccharomyces pombe, meiosis is initiated by the action of Mei2 in a complex cascade activated following conjugation. We have isolated a new gene named rep1+ that is required for the initiation of premeiotic DNA synthesis. rep1+ encodes a 53 kDa protein with one zinc finger motif that is essential for function, and effectively rescues a null mutant of the res1+ gene but only partially a temperature-sensitive mutant of the cdc10+ gene, both of which are required for the onset of mitotic, as well as premeiotic, S phase. Deletion of rep1+ has no apparent effects on the mitotic cell cycle or conjugation, but blocks the initiation of premeiotic DNA synthesis. However, this defect is partially suppressed when rapidly growing cells are induced to conjugate, indicating that the rep1+ function is at least partly substituted by those of the genes controlling the 'start' of the mitotic cell cycle. The rep1 null mutant fails to induce the res2+ gene, a newly identified res1+ homolog cooperating with Cdc10 and acting for the onset of mitotic and premeiotic DNA synthesis, as well as for meiotic division. The rep1+ gene itself is induced moderately during nitrogen starvation but highly during conjugation, and this induction is dependent on both ste11+ and mating pheromones but independent of mei2+. Thus, rep1+ controls the initiation of premeiotic DNA synthesis via induction and/or activation of Res2 and some other essential factors in a cascade independent of Mei2.

Full text

PDF
1881

Images in this article

Selected References

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

  1. Andrews B. J., Herskowitz I. Identification of a DNA binding factor involved in cell-cycle control of the yeast HO gene. Cell. 1989 Apr 7;57(1):21–29. doi: 10.1016/0092-8674(89)90168-2. [DOI] [PubMed] [Google Scholar]
  2. Andrews B. J., Herskowitz I. The yeast SWI4 protein contains a motif present in developmental regulators and is part of a complex involved in cell-cycle-dependent transcription. Nature. 1989 Dec 14;342(6251):830–833. doi: 10.1038/342830a0. [DOI] [PubMed] [Google Scholar]
  3. Aves S. J., Durkacz B. W., Carr A., Nurse P. Cloning, sequencing and transcriptional control of the Schizosaccharomyces pombe cdc10 'start' gene. EMBO J. 1985 Feb;4(2):457–463. doi: 10.1002/j.1460-2075.1985.tb03651.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beach D., Rodgers L., Gould J. ran1+ controls the transition from mitotic division to meiosis in fission yeast. Curr Genet. 1985;10(4):297–311. doi: 10.1007/BF00365626. [DOI] [PubMed] [Google Scholar]
  5. Breeden L., Nasmyth K. Similarity between cell-cycle genes of budding yeast and fission yeast and the Notch gene of Drosophila. Nature. 1987 Oct 15;329(6140):651–654. doi: 10.1038/329651a0. [DOI] [PubMed] [Google Scholar]
  6. Bresch C., Müller G., Egel R. Genes involved in meiosis and sporulation of a yeast. Mol Gen Genet. 1968;102(4):301–306. doi: 10.1007/BF00433721. [DOI] [PubMed] [Google Scholar]
  7. Butler G., Thiele D. J. ACE2, an activator of yeast metallothionein expression which is homologous to SWI5. Mol Cell Biol. 1991 Jan;11(1):476–485. doi: 10.1128/mcb.11.1.476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Caligiuri M., Beach D. Sct1 functions in partnership with Cdc10 in a transcription complex that activates cell cycle START and inhibits differentiation. Cell. 1993 Feb 26;72(4):607–619. doi: 10.1016/0092-8674(93)90079-6. [DOI] [PubMed] [Google Scholar]
  9. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dohrmann P. R., Butler G., Tamai K., Dorland S., Greene J. R., Thiele D. J., Stillman D. J. Parallel pathways of gene regulation: homologous regulators SWI5 and ACE2 differentially control transcription of HO and chitinase. Genes Dev. 1992 Jan;6(1):93–104. doi: 10.1101/gad.6.1.93. [DOI] [PubMed] [Google Scholar]
  11. Egel R., Egel-Mitani M. Premeiotic DNA synthesis in fission yeast. Exp Cell Res. 1974 Sep;88(1):127–134. doi: 10.1016/0014-4827(74)90626-0. [DOI] [PubMed] [Google Scholar]
  12. Egel R., Nielsen O., Weilguny D. Sexual differentiation in fission yeast. Trends Genet. 1990 Nov;6(11):369–373. doi: 10.1016/0168-9525(90)90279-f. [DOI] [PubMed] [Google Scholar]
  13. Elder R. T., Loh E. Y., Davis R. W. RNA from the yeast transposable element Ty1 has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc Natl Acad Sci U S A. 1983 May;80(9):2432–2436. doi: 10.1073/pnas.80.9.2432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fernandez Sarabia M. J., McInerny C., Harris P., Gordon C., Fantes P. The cell cycle genes cdc22+ and suc22+ of the fission yeast Schizosaccharomyces pombe encode the large and small subunits of ribonucleotide reductase. Mol Gen Genet. 1993 Apr;238(1-2):241–251. doi: 10.1007/BF00279553. [DOI] [PubMed] [Google Scholar]
  15. Gordon C. B., Fantes P. A. The cdc22 gene of Schizosaccharomyces pombe encodes a cell cycle-regulated transcript. EMBO J. 1986 Nov;5(11):2981–2985. doi: 10.1002/j.1460-2075.1986.tb04595.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grallert B., Sipiczki M. Common genes and pathways in the regulation of the mitotic and meiotic cell cycles of Schizosaccharomyces pombe. Curr Genet. 1991 Aug;20(3):199–204. doi: 10.1007/BF00326233. [DOI] [PubMed] [Google Scholar]
  17. Igarashi M., Nagata A., Jinno S., Suto K., Okayama H. Wee1(+)-like gene in human cells. Nature. 1991 Sep 5;353(6339):80–83. doi: 10.1038/353080a0. [DOI] [PubMed] [Google Scholar]
  18. Koch C., Moll T., Neuberg M., Ahorn H., Nasmyth K. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science. 1993 Sep 17;261(5128):1551–1557. doi: 10.1126/science.8372350. [DOI] [PubMed] [Google Scholar]
  19. Leupold U., Sipiczki M., Egel R. Pheromone production and response in sterile mutants of fission yeast. Curr Genet. 1991 Jul;20(1-2):79–85. doi: 10.1007/BF00312769. [DOI] [PubMed] [Google Scholar]
  20. Lowndes N. F., McInerny C. J., Johnson A. L., Fantes P. A., Johnston L. H. Control of DNA synthesis genes in fission yeast by the cell-cycle gene cdc10+. Nature. 1992 Jan 30;355(6359):449–453. doi: 10.1038/355449a0. [DOI] [PubMed] [Google Scholar]
  21. Miyamoto M., Tanaka K., Okayama H. res2+, a new member of the cdc10+/SWI4 family, controls the 'start' of mitotic and meiotic cycles in fission yeast. EMBO J. 1994 Apr 15;13(8):1873–1880. doi: 10.1002/j.1460-2075.1994.tb06456.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Moreno S., Klar A., Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991;194:795–823. doi: 10.1016/0076-6879(91)94059-l. [DOI] [PubMed] [Google Scholar]
  23. Nagata A., Igarashi M., Jinno S., Suto K., Okayama H. An additional homolog of the fission yeast cdc25+ gene occurs in humans and is highly expressed in some cancer cells. New Biol. 1991 Oct;3(10):959–968. [PubMed] [Google Scholar]
  24. Nasmyth K., Dirick L. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell. 1991 Sep 6;66(5):995–1013. doi: 10.1016/0092-8674(91)90444-4. [DOI] [PubMed] [Google Scholar]
  25. Obara T., Nakafuku M., Yamamoto M., Kaziro Y. Isolation and characterization of a gene encoding a G-protein alpha subunit from Schizosaccharomyces pombe: involvement in mating and sporulation pathways. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5877–5881. doi: 10.1073/pnas.88.13.5877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Okayama H., Kawaichi M., Brownstein M., Lee F., Yokota T., Arai K. High-efficiency cloning of full-length cDNA; construction and screening of cDNA expression libraries for mammalian cells. Methods Enzymol. 1987;154:3–28. doi: 10.1016/0076-6879(87)54067-8. [DOI] [PubMed] [Google Scholar]
  27. Okazaki K., Okazaki N., Kume K., Jinno S., Tanaka K., Okayama H. High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res. 1990 Nov 25;18(22):6485–6489. doi: 10.1093/nar/18.22.6485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Okazaki N., Okazaki K., Tanaka K., Okayama H. The ste4+ gene, essential for sexual differentiation of Schizosaccharomyces pombe, encodes a protein with a leucine zipper motif. Nucleic Acids Res. 1991 Dec;19(25):7043–7047. doi: 10.1093/nar/19.25.7043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stillman D. J., Bankier A. T., Seddon A., Groenhout E. G., Nasmyth K. A. Characterization of a transcription factor involved in mother cell specific transcription of the yeast HO gene. EMBO J. 1988 Feb;7(2):485–494. doi: 10.1002/j.1460-2075.1988.tb02836.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sugimoto A., Iino Y., Maeda T., Watanabe Y., Yamamoto M. Schizosaccharomyces pombe ste11+ encodes a transcription factor with an HMG motif that is a critical regulator of sexual development. Genes Dev. 1991 Nov;5(11):1990–1999. doi: 10.1101/gad.5.11.1990. [DOI] [PubMed] [Google Scholar]
  32. Tanaka K., Okazaki K., Okazaki N., Ueda T., Sugiyama A., Nojima H., Okayama H. A new cdc gene required for S phase entry of Schizosaccharomyces pombe encodes a protein similar to the cdc 10+ and SWI4 gene products. EMBO J. 1992 Dec;11(13):4923–4932. doi: 10.1002/j.1460-2075.1992.tb05599.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES