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. 1988 Oct;8(10):4009–4017. doi: 10.1128/mcb.8.10.4009

Control of yeast gene expression by transposable elements: maximum expression requires a functional Ty activator sequence and a defective Ty promoter.

L R Coney 1, G S Roeder 1
PMCID: PMC365469  PMID: 2847026

Abstract

Integration of a transposable element adjacent to a gene frequently results in an alteration in expression of the nearby gene. The purpose of our experiments was to identify cis-acting sequences within a yeast transposon (Ty) that are important for expression of the adjacent gene. The role of these sequences in Ty transcription was also analyzed in order to examine the relationship between Ty and adjacent gene expression. Three naturally occurring Ty elements located at the HIS4 locus were examined. These Ty elements differed by multiple sequence changes and had different effects on HIS4 expression. To determine which sequences were important to Ty and HIS4 expression, Ty::lacZ and Ty::HIS4::lacZ fusion genes were constructed and analyzed. Results of these experiments indicated that a sequence element is present in the Ty epsilon region that is necessary for HIS4 expression but which has only a modest effect on Ty transcription. Additionally, a mutation in the Ty promoter region decreased Ty transcription and increased HIS4 expression. The opposite effects of this mutation on Ty and adjacent gene expression were probably caused by promoter competition.

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Selected References

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

  1. Adams S. E., Mellor J., Gull K., Sim R. B., Tuite M. F., Kingsman S. M., Kingsman A. J. The functions and relationships of Ty-VLP proteins in yeast reflect those of mammalian retroviral proteins. Cell. 1987 Apr 10;49(1):111–119. doi: 10.1016/0092-8674(87)90761-6. [DOI] [PubMed] [Google Scholar]
  2. Boeke J. D., Garfinkel D. J., Styles C. A., Fink G. R. Ty elements transpose through an RNA intermediate. Cell. 1985 Mar;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7. [DOI] [PubMed] [Google Scholar]
  3. Boeke J. D., Styles C. A., Fink G. R. Saccharomyces cerevisiae SPT3 gene is required for transposition and transpositional recombination of chromosomal Ty elements. Mol Cell Biol. 1986 Nov;6(11):3575–3581. doi: 10.1128/mcb.6.11.3575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  5. Bram R. J., Lue N. F., Kornberg R. D. A GAL family of upstream activating sequences in yeast: roles in both induction and repression of transcription. EMBO J. 1986 Mar;5(3):603–608. doi: 10.1002/j.1460-2075.1986.tb04253.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brent R., Ptashne M. A bacterial repressor protein or a yeast transcriptional terminator can block upstream activation of a yeast gene. Nature. 1984 Dec 13;312(5995):612–615. doi: 10.1038/312612a0. [DOI] [PubMed] [Google Scholar]
  7. Broach J. R., Hicks J. B. Replication and recombination functions associated with the yeast plasmid, 2 mu circle. Cell. 1980 Sep;21(2):501–508. doi: 10.1016/0092-8674(80)90487-0. [DOI] [PubMed] [Google Scholar]
  8. Cameron J. R., Loh E. Y., Davis R. W. Evidence for transposition of dispersed repetitive DNA families in yeast. Cell. 1979 Apr;16(4):739–751. doi: 10.1016/0092-8674(79)90090-4. [DOI] [PubMed] [Google Scholar]
  9. Clare J., Farabaugh P. Nucleotide sequence of a yeast Ty element: evidence for an unusual mechanism of gene expression. Proc Natl Acad Sci U S A. 1985 May;82(9):2829–2833. doi: 10.1073/pnas.82.9.2829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Clark D. J., Bilanchone V. W., Haywood L. J., Dildine S. L., Sandmeyer S. B. A yeast sigma composite element, TY3, has properties of a retrotransposon. J Biol Chem. 1988 Jan 25;263(3):1413–1423. [PubMed] [Google Scholar]
  11. Company M., Errede B. Cell-type-dependent gene activation by yeast transposon Ty1 involves multiple regulatory determinants. Mol Cell Biol. 1987 Sep;7(9):3205–3211. doi: 10.1128/mcb.7.9.3205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Deschamps J., Wiame J. M. Mating-type effect on cis mutations leading to constitutivity of ornithine transaminase in diploid cells of Saccharomyces cerevisiae. Genetics. 1979 Jul;92(3):749–758. doi: 10.1093/genetics/92.3.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eibel H., Philippsen P. Preferential integration of yeast transposable element Ty into a promoter region. 1984 Jan 26-Feb 1Nature. 307(5949):386–388. doi: 10.1038/307386a0. [DOI] [PubMed] [Google Scholar]
  14. Elder R. T., St John T. P., Stinchcomb D. T., Davis R. W., Scherer S., Davis R. W. Studies on the transposable element Ty1 of yeast. I. RNA homologous to Ty1. II. Recombination and expression of Ty1 and adjacent sequences. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):581–591. doi: 10.1101/sqb.1981.045.01.075. [DOI] [PubMed] [Google Scholar]
  15. Errede B., Cardillo T. S., Sherman F., Dubois E., Deschamps J., Wiame J. M. Mating signals control expression of mutations resulting from insertion of a transposable repetitive element adjacent to diverse yeast genes. Cell. 1980 Nov;22(2 Pt 2):427–436. doi: 10.1016/0092-8674(80)90353-0. [DOI] [PubMed] [Google Scholar]
  16. Faye G., Leung D. W., Tatchell K., Hall B. D., Smith M. Deletion mapping of sequences essential for in vivo transcription of the iso-1-cytochrome c gene. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2258–2262. doi: 10.1073/pnas.78.4.2258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Garfinkel D. J., Boeke J. D., Fink G. R. Ty element transposition: reverse transcriptase and virus-like particles. Cell. 1985 Sep;42(2):507–517. doi: 10.1016/0092-8674(85)90108-4. [DOI] [PubMed] [Google Scholar]
  18. Giniger E., Varnum S. M., Ptashne M. Specific DNA binding of GAL4, a positive regulatory protein of yeast. Cell. 1985 Apr;40(4):767–774. doi: 10.1016/0092-8674(85)90336-8. [DOI] [PubMed] [Google Scholar]
  19. Goel A., Pearlman R. E. Transposable element-mediated enhancement of gene expression in Saccharomyces cerevisiae involves sequence-specific binding of a trans-acting factor. Mol Cell Biol. 1988 Jun;8(6):2572–2580. doi: 10.1128/mcb.8.6.2572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Guarente L., Hoar E. Upstream activation sites of the CYC1 gene of Saccharomyces cerevisiae are active when inverted but not when placed downstream of the "TATA box". Proc Natl Acad Sci U S A. 1984 Dec;81(24):7860–7864. doi: 10.1073/pnas.81.24.7860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Guarente L., Lauer G., Roberts T. M., Ptashne M. Improved methods for maximizing expression of a cloned gene: a bacterium that synthesizes rabbit beta-globin. Cell. 1980 Jun;20(2):543–553. doi: 10.1016/0092-8674(80)90640-6. [DOI] [PubMed] [Google Scholar]
  22. Guarente L., Ptashne M. Fusion of Escherichia coli lacZ to the cytochrome c gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2199–2203. doi: 10.1073/pnas.78.4.2199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Herbomel P., Bourachot B., Yaniv M. Two distinct enhancers with different cell specificities coexist in the regulatory region of polyoma. Cell. 1984 Dec;39(3 Pt 2):653–662. doi: 10.1016/0092-8674(84)90472-0. [DOI] [PubMed] [Google Scholar]
  24. Herr W., Clarke J. The SV40 enhancer is composed of multiple functional elements that can compensate for one another. Cell. 1986 May 9;45(3):461–470. doi: 10.1016/0092-8674(86)90332-6. [DOI] [PubMed] [Google Scholar]
  25. Hinnen A., Hicks J. B., Fink G. R. Transformation of yeast. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1929–1933. doi: 10.1073/pnas.75.4.1929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jauniaux J. C., Dubois E., Vissers S., Crabeel M., Wiame J. M. Molecular cloning, DNA structure, and RNA analysis of the arginase gene in Saccharomyces cerevisiae. A study of cis-dominant regulatory mutations. EMBO J. 1982;1(9):1125–1131. doi: 10.1002/j.1460-2075.1982.tb01307.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kingsman A. J., Gimlich R. L., Clarke L., Chinault A. C., Carbon J. Sequence variation in dispersed repetitive sequences in Saccharomyces cerevisiae. J Mol Biol. 1981 Feb 5;145(4):619–632. doi: 10.1016/0022-2836(81)90306-5. [DOI] [PubMed] [Google Scholar]
  28. Lemoine Y., Dubois E., Wiame J. M. The regulation of urea amidolyase of Saccharomyces cerevisiae: mating type influence on a constitutivity mutation acting in cis. Mol Gen Genet. 1978 Nov 9;166(3):251–258. [PubMed] [Google Scholar]
  29. Liao X. B., Clare J. J., Farabaugh P. J. The upstream activation site of a Ty2 element of yeast is necessary but not sufficient to promote maximal transcription of the element. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8520–8524. doi: 10.1073/pnas.84.23.8520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mellor J., Fulton S. M., Dobson M. J., Wilson W., Kingsman S. M., Kingsman A. J. A retrovirus-like strategy for expression of a fusion protein encoded by yeast transposon Ty1. Nature. 1985 Jan 17;313(5999):243–246. doi: 10.1038/313243a0. [DOI] [PubMed] [Google Scholar]
  31. Mellor J., Kingsman A. J., Kingsman S. M. Ty, an endogenous retrovirus of yeast? Yeast. 1986 Sep;2(3):145–152. doi: 10.1002/yea.320020302. [DOI] [PubMed] [Google Scholar]
  32. Mellor J., Malim M. H., Gull K., Tuite M. F., McCready S., Dibbayawan T., Kingsman S. M., Kingsman A. J. Reverse transcriptase activity and Ty RNA are associated with virus-like particles in yeast. Nature. 1985 Dec 12;318(6046):583–586. doi: 10.1038/318583a0. [DOI] [PubMed] [Google Scholar]
  33. Müller F., Brühl K. H., Freidel K., Kowallik K. V., Ciriacy M. Processing of TY1 proteins and formation of Ty1 virus-like particles in Saccharomyces cerevisiae. Mol Gen Genet. 1987 May;207(2-3):421–429. doi: 10.1007/BF00331610. [DOI] [PubMed] [Google Scholar]
  34. Rathjen P. D., Kingsman A. J., Kingsman S. M. The yeast ROAM mutation--identification of the sequences mediating host gene activation and cell-type control in the yeast retrotransposon, Ty. Nucleic Acids Res. 1987 Sep 25;15(18):7309–7324. doi: 10.1093/nar/15.18.7309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Roeder G. S., Farabaugh P. J., Chaleff D. T., Fink G. R. The origins of gene instability in yeast. Science. 1980 Sep 19;209(4463):1375–1380. doi: 10.1126/science.6251544. [DOI] [PubMed] [Google Scholar]
  36. Roeder G. S., Fink G. R. DNA rearrangements associated with a transposable element in yeast. Cell. 1980 Aug;21(1):239–249. doi: 10.1016/0092-8674(80)90131-2. [DOI] [PubMed] [Google Scholar]
  37. Roeder G. S., Fink G. R. Movement of yeast transposable elements by gene conversion. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5621–5625. doi: 10.1073/pnas.79.18.5621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Roeder G. S., Rose A. B., Pearlman R. E. Transposable element sequences involved in the enhancement of yeast gene expression. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5428–5432. doi: 10.1073/pnas.82.16.5428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  40. Rothstein R. J., Sherman F. Dependence on mating type for the overproduction of iso-2-cytochrome c in the yeast mutant CYC7-H2. Genetics. 1980 Apr;94(4):891–898. doi: 10.1093/genetics/94.4.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Scherer S., Mann C., Davis R. W. Reversion of a promoter deletion in yeast. Nature. 1982 Aug 26;298(5877):815–819. doi: 10.1038/298815a0. [DOI] [PubMed] [Google Scholar]
  42. Siliciano P. G., Tatchell K. Transcription and regulatory signals at the mating type locus in yeast. Cell. 1984 Jul;37(3):969–978. doi: 10.1016/0092-8674(84)90431-8. [DOI] [PubMed] [Google Scholar]
  43. Simchen G., Winston F., Styles C. A., Fink G. R. Ty-mediated gene expression of the LYS2 and HIS4 genes of Saccharomyces cerevisiae is controlled by the same SPT genes. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2431–2434. doi: 10.1073/pnas.81.8.2431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Struhl K. Genetic properties and chromatin structure of the yeast gal regulatory element: an enhancer-like sequence. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7865–7869. doi: 10.1073/pnas.81.24.7865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Struhl K. The yeast his3 promoter contains at least two distinct elements. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7385–7389. doi: 10.1073/pnas.79.23.7385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Taguchi A. K., Ciriacy M., Young E. T. Carbon source dependence of transposable element-associated gene activation in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Jan;4(1):61–68. doi: 10.1128/mcb.4.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Williamson V. M., Cox D., Young E. T., Russell D. W., Smith M. Characterization of transposable element-associated mutations that alter yeast alcohol dehydrogenase II expression. Mol Cell Biol. 1983 Jan;3(1):20–31. doi: 10.1128/mcb.3.1.20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Williamson V. M. Transposable elements in yeast. Int Rev Cytol. 1983;83:1–25. doi: 10.1016/s0074-7696(08)61684-8. [DOI] [PubMed] [Google Scholar]
  49. Williamson V. M., Young E. T., Ciriacy M. Transposable elements associated with constitutive expression of yeast alcohol dehydrogenase II. Cell. 1981 Feb;23(2):605–614. doi: 10.1016/0092-8674(81)90156-2. [DOI] [PubMed] [Google Scholar]
  50. Winston F., Chaleff D. T., Valent B., Fink G. R. Mutations affecting Ty-mediated expression of the HIS4 gene of Saccharomyces cerevisiae. Genetics. 1984 Jun;107(2):179–197. doi: 10.1093/genetics/107.2.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Winston F., Durbin K. J., Fink G. R. The SPT3 gene is required for normal transcription of Ty elements in S. cerevisiae. Cell. 1984 Dec;39(3 Pt 2):675–682. doi: 10.1016/0092-8674(84)90474-4. [DOI] [PubMed] [Google Scholar]

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