Abstract
Several promoter elements have previously been shown to influence the expression of the cab-E gene in Nicotiana plumbaginifolia. Here we demonstrate, by electrophoretic mobility shift and methylation interference assays, that a complex pattern of protein-DNA interactions characterizes this promoter. Among the multiple proteins identified, we focused on five different factors which either occupied important regulatory elements and/or were present in relatively large amounts in nuclear extracts. All of these proteins were distinguished on the basis of their recognition sequence and other biochemical parameters. One, GBF, interacted with a single sequence within the cab-E promoter homologous to the G-box found in many photoregulated and other plant promoters. A second factor, GA-1, bound to the GATA element which is located between the CAAT and TATA boxes of the cab-E and all other LHCII Type I CAB promoters. GA-1 also interacted in vitro with the I-boxes of the Arabidopsis rbcS-1A promoter and the as-2 site of the CaMV 35S promoter. Two other factors, GC-1 and AT-1, bound to multiple recognition sites localized within the GC-rich and AT-rich elements, respectively. GT-1, a protein which interacts with promoters of other light-regulated genes, bound to seven distinct sites distributed throughout the cab-E promoter.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adhya S. Multipartite genetic control elements: communication by DNA loop. Annu Rev Genet. 1989;23:227–250. doi: 10.1146/annurev.ge.23.120189.001303. [DOI] [PubMed] [Google Scholar]
- Arst H. N., Jr, Kudla B., Martinez-Rossi N., Caddick M. X., Sibley S., Davies R. W. Aspergillus and mouse share a new class of 'zinc finger' protein. Trends Genet. 1989 Sep;5(9):291–291. doi: 10.1016/0168-9525(89)90105-4. [DOI] [PubMed] [Google Scholar]
- Beckmann H., Su L. K., Kadesch T. TFE3: a helix-loop-helix protein that activates transcription through the immunoglobulin enhancer muE3 motif. Genes Dev. 1990 Feb;4(2):167–179. doi: 10.1101/gad.4.2.167. [DOI] [PubMed] [Google Scholar]
- Benfey P. N., Chua N. H. Regulated genes in transgenic plants. Science. 1989 Apr 14;244(4901):174–181. doi: 10.1126/science.244.4901.174. [DOI] [PubMed] [Google Scholar]
- Calame K. L. Immunoglobulin gene transcription: molecular mechanisms. Trends Genet. 1989 Dec;5(12):395–399. doi: 10.1016/0168-9525(89)90197-2. [DOI] [PubMed] [Google Scholar]
- Castresana C., Garcia-Luque I., Alonso E., Malik V. S., Cashmore A. R. Both positive and negative regulatory elements mediate expression of a photoregulated CAB gene from Nicotiana plumbaginifolia. EMBO J. 1988 Jul;7(7):1929–1936. doi: 10.1002/j.1460-2075.1988.tb03030.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen E. Y., Seeburg P. H. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA. 1985 Apr;4(2):165–170. doi: 10.1089/dna.1985.4.165. [DOI] [PubMed] [Google Scholar]
- Chiu R., Angel P., Karin M. Jun-B differs in its biological properties from, and is a negative regulator of, c-Jun. Cell. 1989 Dec 22;59(6):979–986. doi: 10.1016/0092-8674(89)90754-x. [DOI] [PubMed] [Google Scholar]
- Chodosh L. A., Carthew R. W., Morgan J. G., Crabtree G. R., Sharp P. A. The adenovirus major late transcription factor activates the rat gamma-fibrinogen promoter. Science. 1987 Oct 30;238(4827):684–688. doi: 10.1126/science.3672119. [DOI] [PubMed] [Google Scholar]
- Datta N., Cashmore A. R. Binding of a pea nuclear protein to promoters of certain photoregulated genes is modulated by phosphorylation. Plant Cell. 1989 Nov;1(11):1069–1077. doi: 10.1105/tpc.1.11.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deikman J., Fischer R. L. Interaction of a DNA binding factor with the 5'-flanking region of an ethylene-responsive fruit ripening gene from tomato. EMBO J. 1988 Nov;7(11):3315–3320. doi: 10.1002/j.1460-2075.1988.tb03202.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Donald R. G., Schindler U., Batschauer A., Cashmore A. R. 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. EMBO J. 1990 Jun;9(6):1727–1735. doi: 10.1002/j.1460-2075.1990.tb08296.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dynan W. S. Modularity in promoters and enhancers. Cell. 1989 Jul 14;58(1):1–4. doi: 10.1016/0092-8674(89)90393-0. [DOI] [PubMed] [Google Scholar]
- Fenoll C., Black D. M., Howell S. H. The intergenic region of maize streak virus contains promoter elements involved in rightward transcription of the viral genome. EMBO J. 1988 Jun;7(6):1589–1596. doi: 10.1002/j.1460-2075.1988.tb02984.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferl R. J., Nick H. S. In vivo detection of regulatory factor binding sites in the 5' flanking region of maize Adh1. J Biol Chem. 1987 Jun 15;262(17):7947–7950. [PubMed] [Google Scholar]
- Fluhr R., Kuhlemeier C., Nagy F., Chua N. H. Organ-specific and light-induced expression of plant genes. Science. 1986 May 30;232(4754):1106–1112. doi: 10.1126/science.232.4754.1106. [DOI] [PubMed] [Google Scholar]
- Fried M., Crothers D. M. Equilibria and kinetics of lac repressor-operator interactions by polyacrylamide gel electrophoresis. Nucleic Acids Res. 1981 Dec 11;9(23):6505–6525. doi: 10.1093/nar/9.23.6505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garner M. M., Revzin A. A gel electrophoresis method for quantifying the binding of proteins to specific DNA regions: application to components of the Escherichia coli lactose operon regulatory system. Nucleic Acids Res. 1981 Jul 10;9(13):3047–3060. doi: 10.1093/nar/9.13.3047. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Gidoni D., Dynan W. S., Tjian R. Multiple specific contacts between a mammalian transcription factor and its cognate promoters. 1984 Nov 29-Dec 5Nature. 312(5993):409–413. doi: 10.1038/312409a0. [DOI] [PubMed] [Google Scholar]
- Giuliano G., Hoffman N. E., Ko K., Scolnik P. A., Cashmore A. R. A light-entrained circadian clock controls transcription of several plant genes. EMBO J. 1988 Dec 1;7(12):3635–3642. doi: 10.1002/j.1460-2075.1988.tb03244.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Grob U., Stüber K. Discrimination of phytochrome dependent light inducible from non-light inducible plant genes. Prediction of a common light-responsive element (LRE) in phytochrome dependent light inducible plant genes. Nucleic Acids Res. 1987 Dec 10;15(23):9957–9973. doi: 10.1093/nar/15.23.9957. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jensen E. Ø, Marcker K. A., Schell J., Bruijn F. J. Interaction of a nodule specific, trans-acting factor with distinct DNA elements in the soybean leghaemoglobin Ibc(3) 5' upstream region. EMBO J. 1988 May;7(5):1265–1271. doi: 10.1002/j.1460-2075.1988.tb02940.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jofuku K. D., Okamuro J. K., Goldberg R. B. Interaction of an embryo DNA binding protein with a soybean lectin gene upstream region. Nature. 1987 Aug 20;328(6132):734–737. doi: 10.1038/328734a0. [DOI] [PubMed] [Google Scholar]
- Johnson P. F., McKnight S. L. Eukaryotic transcriptional regulatory proteins. Annu Rev Biochem. 1989;58:799–839. doi: 10.1146/annurev.bi.58.070189.004055. [DOI] [PubMed] [Google Scholar]
- Jones N. C., Rigby P. W., Ziff E. B. Trans-acting protein factors and the regulation of eukaryotic transcription: lessons from studies on DNA tumor viruses. Genes Dev. 1988 Mar;2(3):267–281. doi: 10.1101/gad.2.3.267. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Kuhlemeier C., Strittmatter G., Ward K., Chua N. H. The Pea rbcS-3A Promoter Mediates Light Responsiveness but not Organ Specificity. Plant Cell. 1989 Apr;1(4):471–478. doi: 10.1105/tpc.1.4.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lam E., Chua N. H. ASF-2: a factor that binds to the cauliflower mosaic virus 35S promoter and a conserved GATA motif in Cab promoters. Plant Cell. 1989 Dec;1(12):1147–1156. doi: 10.1105/tpc.1.12.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee W., Haslinger A., Karin M., Tjian R. Activation of transcription by two factors that bind promoter and enhancer sequences of the human metallothionein gene and SV40. Nature. 1987 Jan 22;325(6102):368–372. doi: 10.1038/325368a0. [DOI] [PubMed] [Google Scholar]
- Maier U. G., Brown J. W., Tologcyzki C., Feix G. Binding of a nuclear factor to a consensus sequence in the 5' flanking region of zein genes from maize. EMBO J. 1987 Jan;6(1):17–22. doi: 10.1002/j.1460-2075.1987.tb04712.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maity S. N., Golumbek P. T., Karsenty G., de Crombrugghe B. Selective activation of transcription by a novel CCAAT binding factor. Science. 1988 Jul 29;241(4865):582–585. doi: 10.1126/science.3399893. [DOI] [PubMed] [Google Scholar]
- 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]
- McKendree W. L., Paul A. L., DeLisle A. J., Ferl R. J. In vivo and in vitro characterization of protein interactions with the dyad G-box of the Arabidopsis Adh gene. Plant Cell. 1990 Mar;2(3):207–214. doi: 10.1105/tpc.2.3.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Metz B. A., Welters P., Hoffmann H. J., Jensen E. O., Schell J., de Bruijn F. J. Primary structure and promoter analysis of leghemoglobin genes of the stem-nodulated tropical legume Sesbania rostrata: conserved coding sequences, cis-elements and trans-acting factors. Mol Gen Genet. 1988 Oct;214(2):181–191. doi: 10.1007/BF00337709. [DOI] [PubMed] [Google Scholar]
- Mitchell P. J., Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989 Jul 28;245(4916):371–378. doi: 10.1126/science.2667136. [DOI] [PubMed] [Google Scholar]
- Mullineaux P. M., Donson J., Morris-Krsinich B. A., Boulton M. I., Davies J. W. The nucleotide sequence of maize streak virus DNA. EMBO J. 1984 Dec 20;3(13):3063–3068. doi: 10.1002/j.1460-2075.1984.tb02258.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perkins N. D., Nicolas R. H., Plumb M. A., Goodwin G. H. The purification of an erythroid protein which binds to enhancer and promoter elements of haemoglobin genes. Nucleic Acids Res. 1989 Feb 25;17(4):1299–1314. doi: 10.1093/nar/17.4.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Piechulla B., Gruissem W. Diurnal mRNA fluctuations of nuclear and plastid genes in developing tomato fruits. EMBO J. 1987 Dec 1;6(12):3593–3599. doi: 10.1002/j.1460-2075.1987.tb02690.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Sawadogo M., Van Dyke M. W., Gregor P. D., Roeder R. G. Multiple forms of the human gene-specific transcription factor USF. I. Complete purification and identification of USF from HeLa cell nuclei. J Biol Chem. 1988 Aug 25;263(24):11985–11993. [PubMed] [Google Scholar]
- Scafe C., Nonet M., Young R. A. RNA polymerase II mutants defective in transcription of a subset of genes. Mol Cell Biol. 1990 Mar;10(3):1010–1016. doi: 10.1128/mcb.10.3.1010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Scotto K. W., Kaulen H., Roeder R. G. Positive and negative regulation of the gene for transcription factor IIIA in Xenopus laevis oocytes. Genes Dev. 1989 May;3(5):651–662. doi: 10.1101/gad.3.5.651. [DOI] [PubMed] [Google Scholar]
- Simpson J., Timko M. P., Cashmore A. R., Schell J., Montagu M. V., Herrera-Estrella L. Light-inducible and tissue-specific expression of a chimaeric gene under control of the 5'-flanking sequence of a pea chlorophyll a/b-binding protein gene. EMBO J. 1985 Nov;4(11):2723–2729. doi: 10.1002/j.1460-2075.1985.tb03995.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- St Schell J. Transgenic plants as tools to study the molecular organization of plant genes. Science. 1987 Sep 4;237(4819):1176–1183. doi: 10.1126/science.237.4819.1176. [DOI] [PubMed] [Google Scholar]
- 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]
- Stougaard J., Sandal N. N., Grøn A., Kühle A., Marcker K. A. 5' Analysis of the soybean leghaemoglobin lbc(3) gene: regulatory elements required for promoter activity and organ specificity. EMBO J. 1987 Dec 1;6(12):3565–3569. doi: 10.1002/j.1460-2075.1987.tb02686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strittmatter G., Chua N. H. Artificial combination of two cis-regulatory elements generates a unique pattern of expression in transgenic plants. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8986–8990. doi: 10.1073/pnas.84.24.8986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trainor C. D., Evans T., Felsenfeld G., Boguski M. S. Structure and evolution of a human erythroid transcription factor. Nature. 1990 Jan 4;343(6253):92–96. doi: 10.1038/343092a0. [DOI] [PubMed] [Google Scholar]
- Travers A. A. DNA conformation and protein binding. Annu Rev Biochem. 1989;58:427–452. doi: 10.1146/annurev.bi.58.070189.002235. [DOI] [PubMed] [Google Scholar]
- Tsai S. F., Martin D. I., Zon L. I., D'Andrea A. D., Wong G. G., Orkin S. H. Cloning of cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells. Nature. 1989 Jun 8;339(6224):446–451. doi: 10.1038/339446a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Willmitzer L. The use of transgenic plants to study plant gene expression. Trends Genet. 1988 Jan;4(1):13–18. doi: 10.1016/0168-9525(88)90122-9. [DOI] [PubMed] [Google Scholar]
- de Bruijn F. J., Felix G., Grunenberg B., Hoffmann H. J., Metz B., Ratet P., Simons-Schreier A., Szabados L., Welters P., Schell J. Regulation of plant genes specifically induced in nitrogen-fixing nodules: role of cis-acting elements and trans-acting factors in leghemoglobin gene expression. Plant Mol Biol. 1989 Sep;13(3):319–325. doi: 10.1007/BF00025320. [DOI] [PubMed] [Google Scholar]