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. 2000 Jun;155(2):539–549. doi: 10.1093/genetics/155.2.539

Schizosaccharomyces pombe Ste7p is required for both promotion and withholding of the entry to meiosis.

A Matsuyama 1, N Yabana 1, Y Watanabe 1, M Yamamoto 1
PMCID: PMC1461121  PMID: 10835379

Abstract

The fission yeast ste7 mutant cannot mate and undergo meiosis, but shows no defect in vegetative growth. We cloned and characterized the ste7 gene. The deduced ste7 gene product (Ste7p) was a protein of 569 amino acids with no significant similarity to other proteins. Transcription of ste7 was induced by nutrient starvation via the function of the transcription factor Ste11p. Disruption of the ste7 gene blocked both conjugation and meiosis, showing that Ste7p plays a positive role in these two processes, probably activating the pheromone signal pathway. Unexpectedly, overexpression of ste7(+) promoted conjugation but inhibited meiosis in wild-type cells. The temperature-sensitive pat1-114 mutant underwent ectopic conjugation at the semirestrictive temperature when its genetic background was ste7(+), whereas the same mutant initiated haploid meiosis when its genetic background was ste7Delta. Two-hybrid analysis suggested that Ste7p interacts physically with both Pat1p and Mei2p, which together constitute the major switch to initiate meiosis. Ste7p tagged with green fluorescent protein accumulated in haploid cells under nutrient starvation until they completed conjugation, but this protein disappeared when they were to enter meiosis. These observations suggest that Ste7p may have a function to suppress the onset of meiosis until the conjugation process has been duly completed.

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Selected References

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

  1. Aono T., Yanai H., Miki F., Davey J., Shimoda C. Mating pheromone-induced expression of the mat1-Pm gene of Schizosaccharomyces pombe: identification of signalling components and characterization of upstream controlling elements. Yeast. 1994 Jun;10(6):757–770. doi: 10.1002/yea.320100607. [DOI] [PubMed] [Google Scholar]
  2. Beach D., Piper M., Nurse P. Construction of a Schizosaccharomyces pombe gene bank in a yeast bacterial shuttle vector and its use to isolate genes by complementation. Mol Gen Genet. 1982;187(2):326–329. doi: 10.1007/BF00331138. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Cottarel G., Beach D., Deuschle U. Two new multi-purpose multicopy Schizosaccharomyces pombe shuttle vectors, pSP1 and pSP2. Curr Genet. 1993 May-Jun;23(5-6):547–548. doi: 10.1007/BF00312650. [DOI] [PubMed] [Google Scholar]
  5. Durfee T., Becherer K., Chen P. L., Yeh S. H., Yang Y., Kilburn A. E., Lee W. H., Elledge S. J. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 1993 Apr;7(4):555–569. doi: 10.1101/gad.7.4.555. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Gotoh Y., Nishida E., Shimanuki M., Toda T., Imai Y., Yamamoto M. Schizosaccharomyces pombe Spk1 is a tyrosine-phosphorylated protein functionally related to Xenopus mitogen-activated protein kinase. Mol Cell Biol. 1993 Oct;13(10):6427–6434. doi: 10.1128/mcb.13.10.6427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Grimm C., Kohli J., Murray J., Maundrell K. Genetic engineering of Schizosaccharomyces pombe: a system for gene disruption and replacement using the ura4 gene as a selectable marker. Mol Gen Genet. 1988 Dec;215(1):81–86. doi: 10.1007/BF00331307. [DOI] [PubMed] [Google Scholar]
  10. Gutz H. "Twin meiosis" and other ambivalences in the life cycle of Schizosaccharomyces pombe. Science. 1967 Nov 10;158(3802):796–798. doi: 10.1126/science.158.3802.796. [DOI] [PubMed] [Google Scholar]
  11. Heim R., Cubitt A. B., Tsien R. Y. Improved green fluorescence. Nature. 1995 Feb 23;373(6516):663–664. doi: 10.1038/373663b0. [DOI] [PubMed] [Google Scholar]
  12. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  13. Hughes D. A., Fukui Y., Yamamoto M. Homologous activators of ras in fission and budding yeast. Nature. 1990 Mar 22;344(6264):355–357. doi: 10.1038/344355a0. [DOI] [PubMed] [Google Scholar]
  14. Iino Y., Yamamoto M. Negative control for the initiation of meiosis in Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2447–2451. doi: 10.1073/pnas.82.8.2447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Isshiki T., Mochizuki N., Maeda T., Yamamoto M. Characterization of a fission yeast gene, gpa2, that encodes a G alpha subunit involved in the monitoring of nutrition. Genes Dev. 1992 Dec;6(12B):2455–2462. doi: 10.1101/gad.6.12b.2455. [DOI] [PubMed] [Google Scholar]
  16. Kitamura K., Maekawa H., Shimoda C. Fission yeast Ste9, a homolog of Hct1/Cdh1 and Fizzy-related, is a novel negative regulator of cell cycle progression during G1-phase. Mol Biol Cell. 1998 May;9(5):1065–1080. doi: 10.1091/mbc.9.5.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kitamura K., Shimoda C. The Schizosaccharomyces pombe mam2 gene encodes a putative pheromone receptor which has a significant homology with the Saccharomyces cerevisiae Ste2 protein. EMBO J. 1991 Dec;10(12):3743–3751. doi: 10.1002/j.1460-2075.1991.tb04943.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kominami K., Seth-Smith H., Toda T. Apc10 and Ste9/Srw1, two regulators of the APC-cyclosome, as well as the CDK inhibitor Rum1 are required for G1 cell-cycle arrest in fission yeast. EMBO J. 1998 Sep 15;17(18):5388–5399. doi: 10.1093/emboj/17.18.5388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. doi: 10.1073/pnas.82.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Li P., McLeod M. Molecular mimicry in development: identification of ste11+ as a substrate and mei3+ as a pseudosubstrate inhibitor of ran1+ kinase. Cell. 1996 Nov 29;87(5):869–880. doi: 10.1016/s0092-8674(00)81994-7. [DOI] [PubMed] [Google Scholar]
  21. Masuda T., Kariya K., Shinkai M., Okada T., Kataoka T. Protein kinase Byr2 is a target of Ras1 in the fission yeast Schizosaccharomyces pombe. J Biol Chem. 1995 Feb 3;270(5):1979–1982. doi: 10.1074/jbc.270.5.1979. [DOI] [PubMed] [Google Scholar]
  22. Maundrell K. nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine. J Biol Chem. 1990 Jul 5;265(19):10857–10864. [PubMed] [Google Scholar]
  23. McLeod M., Beach D. Homology between the ran1+ gene of fission yeast and protein kinases. EMBO J. 1986 Dec 20;5(13):3665–3671. doi: 10.1002/j.1460-2075.1986.tb04697.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McLeod M., Stein M., Beach D. The product of the mei3+ gene, expressed under control of the mating-type locus, induces meiosis and sporulation in fission yeast. EMBO J. 1987 Mar;6(3):729–736. doi: 10.1002/j.1460-2075.1987.tb04814.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nadin-Davis S. A., Nasim A. Schizosaccharomyces pombe ras1 and byr1 are functionally related genes of the ste family that affect starvation-induced transcription of mating-type genes. Mol Cell Biol. 1990 Feb;10(2):549–560. doi: 10.1128/mcb.10.2.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Neiman A. M., Stevenson B. J., Xu H. P., Sprague G. F., Jr, Herskowitz I., Wigler M., Marcus S. Functional homology of protein kinases required for sexual differentiation in Schizosaccharomyces pombe and Saccharomyces cerevisiae suggests a conserved signal transduction module in eukaryotic organisms. Mol Biol Cell. 1993 Jan;4(1):107–120. doi: 10.1091/mbc.4.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nielsen O., Egel R. The pat1 protein kinase controls transcription of the mating-type genes in fission yeast. EMBO J. 1990 May;9(5):1401–1406. doi: 10.1002/j.1460-2075.1990.tb08255.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. 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]
  31. Sipiczki M., Ferenczy L. Protoplast fusion of Schizosaccharomyces pombe Auxotrophic mutants of identical mating-type. Mol Gen Genet. 1977 Feb 28;151(1):77–81. doi: 10.1007/BF00446915. [DOI] [PubMed] [Google Scholar]
  32. Sipiczki M. The role of sterility genes (ste and aff) in the initiation of sexual development in Schizosaccharomyces pombe. Mol Gen Genet. 1988 Aug;213(2-3):529–534. doi: 10.1007/BF00339626. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Tanaka K., Davey J., Imai Y., Yamamoto M. Schizosaccharomyces pombe map3+ encodes the putative M-factor receptor. Mol Cell Biol. 1993 Jan;13(1):80–88. doi: 10.1128/mcb.13.1.80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Van Heeckeren W. J., Dorris D. R., Struhl K. The mating-type proteins of fission yeast induce meiosis by directly activating mei3 transcription. Mol Cell Biol. 1998 Dec;18(12):7317–7326. doi: 10.1128/mcb.18.12.7317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wang Y., Xu H. P., Riggs M., Rodgers L., Wigler M. byr2, a Schizosaccharomyces pombe gene encoding a protein kinase capable of partial suppression of the ras1 mutant phenotype. Mol Cell Biol. 1991 Jul;11(7):3554–3563. doi: 10.1128/mcb.11.7.3554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Watanabe Y., Shinozaki-Yabana S., Chikashige Y., Hiraoka Y., Yamamoto M. Phosphorylation of RNA-binding protein controls cell cycle switch from mitotic to meiotic in fission yeast. Nature. 1997 Mar 13;386(6621):187–190. doi: 10.1038/386187a0. [DOI] [PubMed] [Google Scholar]
  38. Willer M., Hoffmann L., Styrkársdóttir U., Egel R., Davey J., Nielsen O. Two-step activation of meiosis by the mat1 locus in Schizosaccharomyces pombe. Mol Cell Biol. 1995 Sep;15(9):4964–4970. doi: 10.1128/mcb.15.9.4964. [DOI] [PMC free article] [PubMed] [Google Scholar]

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