Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1990 Jun;9(6):1727–1735. doi: 10.1002/j.1460-2075.1990.tb08296.x

The plant G box promoter sequence activates transcription in Saccharomyces cerevisiae and is bound in vitro by a yeast activity similar to GBF, the plant G box binding factor.

R G Donald 1, U Schindler 1, A Batschauer 1, A R Cashmore 1
PMCID: PMC551875  PMID: 2161333

Abstract

G box and I box sequences of the Arabidopsis thaliana ribulose-bisphosphate-1,5-carboxylase small subunit (RBCS) promoter are required for expression mediated by the Arabidopsis rbcS-1A promoter in transgenic tobacco plants and are bound in vitro by factors from plant nuclear extracts termed GBF and GA-1, respectively. We show here that a -390 to -60 rbcS-1A promoter fragment containing the G box and two I boxes activates transcription from a truncated iso-1-cytochrome c (CYC1) gene promoter in Saccharomyces cerevisiae. Mutagenesis of either the rbcS-1A G box or both I box sequences eliminated the expression mediated by this fragment. When polymerized, I box oligonucleotides were also capable of enhancing expression from the truncated CYC1 promoter. Single-copy G box sequences from the Arabidopsis rbcS-1A, Arabidopsis Adh and tomato rbcS-3A promoters were more potent activators and were used in mobility shift assays to identify a DNA binding activity in yeast functionally similar to GBF. In methylation interference experiments, the binding specificity of the yeast protein was indistinguishable from that obtained with plant nuclear extracts.

Full text

PDF
1727

Images in this article

1729Fig. 3.
on p.1729
1730Fig. 4.
on p.1730
1731Fig. 5.
on p.1731
1732Fig. 6.
on p.1732

Selected References

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

  1. Arima K., Oshima T., Kubota I., Nakamura N., Mizunaga T., Toh-e A. The nucleotide sequence of the yeast PHO5 gene: a putative precursor of repressible acid phosphatase contains a signal peptide. Nucleic Acids Res. 1983 Mar 25;11(6):1657–1672. doi: 10.1093/nar/11.6.1657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beckmann H., Kadesch T. Identification of a yeast protein with properties similar to those of the immunoglobulin heavy-chain enhancer-binding protein NF-muE3. Mol Cell Biol. 1989 Oct;9(10):4535–4540. doi: 10.1128/mcb.9.10.4535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bostian K. A., Lemire J. M., Halvorson H. O. Physiological control of repressible acid phosphatase gene transcripts in Saccharomyces cerevisiae. Mol Cell Biol. 1983 May;3(5):839–853. doi: 10.1128/mcb.3.5.839. [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: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  5. Bram R. J., Kornberg R. D. Isolation of a Saccharomyces cerevisiae centromere DNA-binding protein, its human homolog, and its possible role as a transcription factor. Mol Cell Biol. 1987 Jan;7(1):403–409. doi: 10.1128/mcb.7.1.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buratowski S., Hahn S., Sharp P. A., Guarente L. Function of a yeast TATA element-binding protein in a mammalian transcription system. Nature. 1988 Jul 7;334(6177):37–42. doi: 10.1038/334037a0. [DOI] [PubMed] [Google Scholar]
  7. Burke R. L., Tekamp-Olson P., Najarian R. The isolation, characterization, and sequence of the pyruvate kinase gene of Saccharomyces cerevisiae. J Biol Chem. 1983 Feb 25;258(4):2193–2201. [PubMed] [Google Scholar]
  8. Carthew R. W., Chodosh L. A., Sharp P. A. An RNA polymerase II transcription factor binds to an upstream element in the adenovirus major late promoter. Cell. 1985 Dec;43(2 Pt 1):439–448. doi: 10.1016/0092-8674(85)90174-6. [DOI] [PubMed] [Google Scholar]
  9. Cavallini B., Huet J., Plassat J. L., Sentenac A., Egly J. M., Chambon P. A yeast activity can substitute for the HeLa cell TATA box factor. Nature. 1988 Jul 7;334(6177):77–80. doi: 10.1038/334077a0. [DOI] [PubMed] [Google Scholar]
  10. Chang C., Meyerowitz E. M. Molecular cloning and DNA sequence of the Arabidopsis thaliana alcohol dehydrogenase gene. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1408–1412. doi: 10.1073/pnas.83.5.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chodosh L. A., Baldwin A. S., Carthew R. W., Sharp P. A. Human CCAAT-binding proteins have heterologous subunits. Cell. 1988 Apr 8;53(1):11–24. doi: 10.1016/0092-8674(88)90483-7. [DOI] [PubMed] [Google Scholar]
  12. Chodosh L. A., Buratowski S., Sharp P. A. A yeast protein possesses the DNA-binding properties of the adenovirus major late transcription factor. Mol Cell Biol. 1989 Feb;9(2):820–822. doi: 10.1128/mcb.9.2.820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chodosh L. A., Carthew R. W., Sharp P. A. A single polypeptide possesses the binding and transcription activities of the adenovirus major late transcription factor. Mol Cell Biol. 1986 Dec;6(12):4723–4733. doi: 10.1128/mcb.6.12.4723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Donald R. G., Cashmore A. R. Mutation of either G box or I box sequences profoundly affects expression from the Arabidopsis rbcS-1A promoter. EMBO J. 1990 Jun;9(6):1717–1726. doi: 10.1002/j.1460-2075.1990.tb08295.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fischer J. A., Giniger E., Maniatis T., Ptashne M. GAL4 activates transcription in Drosophila. Nature. 1988 Apr 28;332(6167):853–856. doi: 10.1038/332853a0. [DOI] [PubMed] [Google Scholar]
  17. Gidoni D., Brosio P., Bond-Nutter D., Bedbrook J., Dunsmuir P. Novel cis-acting elements in Petunia Cab gene promoters. Mol Gen Genet. 1989 Jan;215(2):337–344. doi: 10.1007/BF00339739. [DOI] [PubMed] [Google Scholar]
  18. Giuliano G., Pichersky E., Malik V. S., Timko M. P., Scolnik P. A., Cashmore A. R. An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7089–7093. doi: 10.1073/pnas.85.19.7089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Green P. J., Kay S. A., Chua N. H. Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A gene. EMBO J. 1987 Sep;6(9):2543–2549. doi: 10.1002/j.1460-2075.1987.tb02542.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Green P. J., Yong M. H., Cuozzo M., Kano-Murakami Y., Silverstein P., Chua N. H. Binding site requirements for pea nuclear protein factor GT-1 correlate with sequences required for light-dependent transcriptional activation of the rbcS-3A gene. EMBO J. 1988 Dec 20;7(13):4035–4044. doi: 10.1002/j.1460-2075.1988.tb03297.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  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. Guarente L. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 1983;101:181–191. doi: 10.1016/0076-6879(83)01013-7. [DOI] [PubMed] [Google Scholar]
  24. Harshman K. D., Moye-Rowley W. S., Parker C. S. Transcriptional activation by the SV40 AP-1 recognition element in yeast is mediated by a factor similar to AP-1 that is distinct from GCN4. Cell. 1988 Apr 22;53(2):321–330. doi: 10.1016/0092-8674(88)90393-5. [DOI] [PubMed] [Google Scholar]
  25. Hayes T. E., Sengupta P., Cochran B. H. The human c-fos serum response factor and the yeast factors GRM/PRTF have related DNA-binding specificities. Genes Dev. 1988 Dec;2(12B):1713–1722. doi: 10.1101/gad.2.12b.1713. [DOI] [PubMed] [Google Scholar]
  26. Horikoshi M., Carey M. F., Kakidani H., Roeder R. G. Mechanism of action of a yeast activator: direct effect of GAL4 derivatives on mammalian TFIID-promoter interactions. Cell. 1988 Aug 26;54(5):665–669. doi: 10.1016/s0092-8674(88)80011-4. [DOI] [PubMed] [Google Scholar]
  27. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Jones R. H., Moreno S., Nurse P., Jones N. C. Expression of the SV40 promoter in fission yeast: identification and characterization of an AP-1-like factor. Cell. 1988 May 20;53(4):659–667. doi: 10.1016/0092-8674(88)90581-8. [DOI] [PubMed] [Google Scholar]
  29. Kakidani H., Ptashne M. GAL4 activates gene expression in mammalian cells. Cell. 1988 Jan 29;52(2):161–167. doi: 10.1016/0092-8674(88)90504-1. [DOI] [PubMed] [Google Scholar]
  30. Kaneko Y., Hayashi N., Toh-e A., Banno I., Oshima Y. Structural characteristics of the PHO8 gene encoding repressible alkaline phosphatase in Saccharomyces cerevisiae. Gene. 1987;58(1):137–148. doi: 10.1016/0378-1119(87)90036-9. [DOI] [PubMed] [Google Scholar]
  31. Kodaki T., Yamashita S. Yeast phosphatidylethanolamine methylation pathway. Cloning and characterization of two distinct methyltransferase genes. J Biol Chem. 1987 Nov 15;262(32):15428–15435. [PubMed] [Google Scholar]
  32. Kuhlemeier C., Cuozzo M., Green P. J., Goyvaerts E., Ward K., Chua N. H. Localization and conditional redundancy of regulatory elements in rbcS-3A, a pea gene encoding the small subunit of ribulose-bisphosphate carboxylase. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4662–4666. doi: 10.1073/pnas.85.13.4662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kuhlemeier C., Fluhr R., Green P. J., Chua N. H. Sequences in the pea rbcS-3A gene have homology to constitutive mammalian enhancers but function as negative regulatory elements. Genes Dev. 1987 May;1(3):247–255. doi: 10.1101/gad.1.3.247. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Lam E., Benfey P. N., Gilmartin P. M., Fang R. X., Chua N. H. Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7890–7894. doi: 10.1073/pnas.86.20.7890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Lin Y. S., Carey M. F., Ptashne M., Green M. R. GAL4 derivatives function alone and synergistically with mammalian activators in vitro. Cell. 1988 Aug 26;54(5):659–664. doi: 10.1016/s0092-8674(88)80010-2. [DOI] [PubMed] [Google Scholar]
  37. Lin Y. S., Green M. R. Identification and purification of a Saccharomyces cerevisiae protein with the DNA binding specificity of mammalian activating transcription factor. Proc Natl Acad Sci U S A. 1989 Jan;86(1):109–113. doi: 10.1073/pnas.86.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Ma J., Przibilla E., Hu J., Bogorad L., Ptashne M. Yeast activators stimulate plant gene expression. Nature. 1988 Aug 18;334(6183):631–633. doi: 10.1038/334631a0. [DOI] [PubMed] [Google Scholar]
  39. Maarse A. C., Grivell L. A. Nucleotide sequence of the gene encoding the 11-kDa subunit of the ubiquinol-cytochrome-c oxidoreductase in Saccharomyces cerevisiae. Eur J Biochem. 1987 Jun 1;165(2):419–425. doi: 10.1111/j.1432-1033.1987.tb11455.x. [DOI] [PubMed] [Google Scholar]
  40. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  41. Meyhack B., Bajwa W., Rudolph H., Hinnen A. Two yeast acid phosphatase structural genes are the result of a tandem duplication and show different degrees of homology in their promoter and coding sequences. EMBO J. 1982;1(6):675–680. doi: 10.1002/j.1460-2075.1982.tb01229.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Rose M., Botstein D. Construction and use of gene fusions to lacZ (beta-galactosidase) that are expressed in yeast. Methods Enzymol. 1983;101:167–180. doi: 10.1016/0076-6879(83)01012-5. [DOI] [PubMed] [Google Scholar]
  43. Russell D. W., Smith M., Williamson V. M., Young E. T. Nucleotide sequence of the yeast alcohol dehydrogenase II gene. J Biol Chem. 1983 Feb 25;258(4):2674–2682. [PubMed] [Google Scholar]
  44. Sawadogo M., Roeder R. G. Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region. Cell. 1985 Nov;43(1):165–175. doi: 10.1016/0092-8674(85)90021-2. [DOI] [PubMed] [Google Scholar]
  45. Schulze-Lefert P., Dangl J. L., Becker-André M., Hahlbrock K., Schulz W. Inducible in vivo DNA footprints define sequences necessary for UV light activation of the parsley chalcone synthase gene. EMBO J. 1989 Mar;8(3):651–656. doi: 10.1002/j.1460-2075.1989.tb03422.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sengstag C., Hinnen A. A 28-bp segment of the Saccharomyces cerevisiae PHO5 upstream activator sequence confers phosphate control to the CYC1-lacZ gene fusion. Gene. 1988 Jul 30;67(2):223–228. doi: 10.1016/0378-1119(88)90399-x. [DOI] [PubMed] [Google Scholar]
  47. Staiger D., Kaulen H., Schell J. A CACGTG motif of the Antirrhinum majus chalcone synthase promoter is recognized by an evolutionarily conserved nuclear protein. Proc Natl Acad Sci U S A. 1989 Sep;86(18):6930–6934. doi: 10.1073/pnas.86.18.6930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Struhl K. The DNA-binding domains of the jun oncoprotein and the yeast GCN4 transcriptional activator protein are functionally homologous. Cell. 1987 Sep 11;50(6):841–846. doi: 10.1016/0092-8674(87)90511-3. [DOI] [PubMed] [Google Scholar]
  49. Tekamp-Olson P., Najarian R., Burke R. L. The isolation, characterization and nucleotide sequence of the phosphoglucoisomerase gene of Saccharomyces cerevisiae. Gene. 1988 Dec 15;73(1):153–161. doi: 10.1016/0378-1119(88)90321-6. [DOI] [PubMed] [Google Scholar]
  50. To-E A., Ueda Y., Kakimoto S. I., Oshima Y. Isolation and characterization of acid phosphatase mutants in Saccharomyces cerevisiae. J Bacteriol. 1973 Feb;113(2):727–738. doi: 10.1128/jb.113.2.727-738.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Vogel K., Hörz W., Hinnen A. The two positively acting regulatory proteins PHO2 and PHO4 physically interact with PHO5 upstream activation regions. Mol Cell Biol. 1989 May;9(5):2050–2057. doi: 10.1128/mcb.9.5.2050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Walter P., Gangloff J., Bonnet J., Boulanger Y., Ebel J. P., Fasiolo F. Primary structure of the Saccharomyces cerevisiae gene for methionyl-tRNA synthetase. Proc Natl Acad Sci U S A. 1983 May;80(9):2437–2441. doi: 10.1073/pnas.80.9.2437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Webster N., Jin J. R., Green S., Hollis M., Chambon P. The yeast UASG is a transcriptional enhancer in human HeLa cells in the presence of the GAL4 trans-activator. Cell. 1988 Jan 29;52(2):169–178. doi: 10.1016/0092-8674(88)90505-3. [DOI] [PubMed] [Google Scholar]
  54. Wiederrecht G., Shuey D. J., Kibbe W. A., Parker C. S. The Saccharomyces and Drosophila heat shock transcription factors are identical in size and DNA binding properties. Cell. 1987 Feb 13;48(3):507–515. doi: 10.1016/0092-8674(87)90201-7. [DOI] [PubMed] [Google Scholar]

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

RESOURCES