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. 1995 Jun;15(6):2955–2961. doi: 10.1128/mcb.15.6.2955

Positive control of yeast meiotic genes by the negative regulator UME6.

K S Bowdish 1, H E Yuan 1, A P Mitchell 1
PMCID: PMC230526  PMID: 7760793

Abstract

The yeast meiotic activator IME1 stimulates transcription of many early meiotic genes. These genes share a 5' sequence called URS1. URS1 sites function as repression sites in cells that lack IME1; we show here that URS1 sites are weak activation sequences in cells that express IME1. Repression through URS1 sites is known to depend upon the URS1-binding protein UME6. We have identified a UME6 allele (previously called rim16-12) that causes a defect in IME1-dependent activation of meiotic genes but not in repression through URS1 sites. In contrast, a ume6 null mutation causes defects in both IME1-dependent activation and in repression through URS1 sites. A LexA-UME6 fusion protein is an IME1-dependent transcriptional activator, whereas a LexA-UME6 fusion carrying the rim16-12 substitution cannot activate transcription. These findings argue that IME1 activates meiotic genes by converting UME6 from a negative regulator to a positive regulator; the rim16-12 mutant protein is defective in conversion to a positive regulator.

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Selected References

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

  1. Bowdish K. S., Mitchell A. P. Bipartite structure of an early meiotic upstream activation sequence from Saccharomyces cerevisiae. Mol Cell Biol. 1993 Apr;13(4):2172–2181. doi: 10.1128/mcb.13.4.2172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bowdish K. S., Yuan H. E., Mitchell A. P. Analysis of RIM11, a yeast protein kinase that phosphorylates the meiotic activator IME1. Mol Cell Biol. 1994 Dec;14(12):7909–7919. doi: 10.1128/mcb.14.12.7909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buckingham L. E., Wang H. T., Elder R. T., McCarroll R. M., Slater M. R., Esposito R. E. Nucleotide sequence and promoter analysis of SPO13, a meiosis-specific gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9406–9410. doi: 10.1073/pnas.87.23.9406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Guarente L., Mason T. Heme regulates transcription of the CYC1 gene of S. cerevisiae via an upstream activation site. Cell. 1983 Apr;32(4):1279–1286. doi: 10.1016/0092-8674(83)90309-4. [DOI] [PubMed] [Google Scholar]
  5. Kane S. M., Roth R. Carbohydrate metabolism during ascospore development in yeast. J Bacteriol. 1974 Apr;118(1):8–14. doi: 10.1128/jb.118.1.8-14.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Law D. T., Segall J. The SPS100 gene of Saccharomyces cerevisiae is activated late in the sporulation process and contributes to spore wall maturation. Mol Cell Biol. 1988 Feb;8(2):912–922. doi: 10.1128/mcb.8.2.912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Lopes J. M., Schulze K. L., Yates J. W., Hirsch J. P., Henry S. A. The INO1 promoter of Saccharomyces cerevisiae includes an upstream repressor sequence (URS1) common to a diverse set of yeast genes. J Bacteriol. 1993 Jul;175(13):4235–4238. doi: 10.1128/jb.175.13.4235-4238.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Luche R. M., Smart W. C., Marion T., Tillman M., Sumrada R. A., Cooper T. G. Saccharomyces cerevisiae BUF protein binds to sequences participating in DNA replication in addition to those mediating transcriptional repression (URS1) and activation. Mol Cell Biol. 1993 Sep;13(9):5749–5761. doi: 10.1128/mcb.13.9.5749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Luche R. M., Sumrada R., Cooper T. G. A cis-acting element present in multiple genes serves as a repressor protein binding site for the yeast CAR1 gene. Mol Cell Biol. 1990 Aug;10(8):3884–3895. doi: 10.1128/mcb.10.8.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Mitchell A. P., Bowdish K. S. Selection for early meiotic mutants in yeast. Genetics. 1992 May;131(1):65–72. doi: 10.1093/genetics/131.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Mitchell A. P. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev. 1994 Mar;58(1):56–70. doi: 10.1128/mr.58.1.56-70.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Park H. D., Luche R. M., Cooper T. G. The yeast UME6 gene product is required for transcriptional repression mediated by the CAR1 URS1 repressor binding site. Nucleic Acids Res. 1992 Apr 25;20(8):1909–1915. doi: 10.1093/nar/20.8.1909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Park H. O., Craig E. A. Transcriptional regulation of a yeast HSP70 gene by heat shock factor and an upstream repression site-binding factor. Genes Dev. 1991 Jul;5(7):1299–1308. doi: 10.1101/gad.5.7.1299. [DOI] [PubMed] [Google Scholar]
  15. Rose M. D., Broach J. R. Cloning genes by complementation in yeast. Methods Enzymol. 1991;194:195–230. doi: 10.1016/0076-6879(91)94017-7. [DOI] [PubMed] [Google Scholar]
  16. Rose M. D., Novick P., Thomas J. H., Botstein D., Fink G. R. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene. 1987;60(2-3):237–243. doi: 10.1016/0378-1119(87)90232-0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Smith H. E., Driscoll S. E., Sia R. A., Yuan H. E., Mitchell A. P. Genetic evidence for transcriptional activation by the yeast IME1 gene product. Genetics. 1993 Apr;133(4):775–784. doi: 10.1093/genetics/133.4.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Smith H. E., Su S. S., Neigeborn L., Driscoll S. E., Mitchell A. P. Role of IME1 expression in regulation of meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Dec;10(12):6103–6113. doi: 10.1128/mcb.10.12.6103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Strich R., Slater M. R., Esposito R. E. Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10018–10022. doi: 10.1073/pnas.86.24.10018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Strich R., Surosky R. T., Steber C., Dubois E., Messenguy F., Esposito R. E. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 1994 Apr 1;8(7):796–810. doi: 10.1101/gad.8.7.796. [DOI] [PubMed] [Google Scholar]
  24. Su S. S., Mitchell A. P. Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics. 1993 Jan;133(1):67–77. doi: 10.1093/genetics/133.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sumrada R. A., Cooper T. G. Ubiquitous upstream repression sequences control activation of the inducible arginase gene in yeast. Proc Natl Acad Sci U S A. 1987 Jun;84(12):3997–4001. doi: 10.1073/pnas.84.12.3997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Torchia T. E., Hamilton R. W., Cano C. L., Hopper J. E. Disruption of regulatory gene GAL80 in Saccharomyces cerevisiae: effects on carbon-controlled regulation of the galactose/melibiose pathway genes. Mol Cell Biol. 1984 Aug;4(8):1521–1527. doi: 10.1128/mcb.4.8.1521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Vershon A. K., Hollingsworth N. M., Johnson A. D. Meiotic induction of the yeast HOP1 gene is controlled by positive and negative regulatory sites. Mol Cell Biol. 1992 Sep;12(9):3706–3714. doi: 10.1128/mcb.12.9.3706. [DOI] [PMC free article] [PubMed] [Google Scholar]

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