Abstract
We isolated a complementary DNA (cDNA) that encoded a TATA-binding protein (TBP) from a cDNA library of tobacco (Nicotiana tabacum) suspension-cultured cells (BY-2). A comparison among deduced amino acid sequences of plant TBPs revealed the presence of a long conserved region within the amino acid sequence of the TBP. Genomic Southern analysis revealed that tobacco TBP (tTBP) is encoded by only a small number of copies of a gene in the tobacco genome. Addition of recombinant tTBP to an extract of tobacco nuclei (TNE) enhanced the basal transcriptional activity in vitro. This result indicates that the level of tTBP is a rate-limiting factor for basal transcriptional activity in TNE. We subsequently succeeded in the functional complementation of TATA-dependent initiation of transcription that was associated with a plant promoter in a homologous plant system. Addition of bacterially expressed recombinant tTBP to a heat-inactivated TNE restored transcriptional activity, as did the addition of human TBP. Moreover, heating of the recombinant tTBP eliminated its ability to restore transcriptional activity. It appears that the heat inactivation of TNE was caused by the heat inactivation of tTBP in TNE.
Abbreviations: DTT, dithiothreitol; GTF, general transcription factor; PAGE, polyacrylamide gel electrophoresis; SDS, sodium dodecyl sulfate; TBP, TATA-binding protein; TNE, extract of tobacco nuclei
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References
Roeder RG: The complexities of eukaryotic transcription initiation: regulation of preinitiation complex assembly. Trends Biochem Sci 16: 402-408 (1991).
Zawel L, Reinberg D: Advances in RNA polymerase II transcription. Curr Opin Cell Biol 4: 488-495 (1992).
Gabrielsen OS, Sentenac A: RNA polymerase III(C) and its transcription factors. Trends Biochem Sci 16: 412-416 (1991).
Cormac BP, Struhl K: The TATA-binding protein is required for transcription by all three nuclear RNA polymerases in yeast cells. Cell 69: 685-696 (1992).
Schultz MC, Reeder RH, Hahn S: Variants of the TATA-binding protein can distinguish subsets of RNA polymerase I, II, and III promoters. Cell 69: 697-702 (1992).
Sharp PA: TATA-binding protein is a classless factor. Cell 68: 819-821 (1992).
White RJ, Jackson SP: The TATA-binding protein; a central role in transcription by RNA polymerase I, II, and III. Trends Genet 8: 284-288 (1992).
Van Dyke MW, Roeder RG, Sawadogo M: Physical analysis of transcription preinitiation complex assembly on class II gene promoters. Science 241: 1335-1338 (1988).
Buratowski S, Hahn S, Guarente L, Sharp A: Five intermediate complexes in transcription initiation by RNA polymerase II. Cell 56: 549-561 (1991).
Inostroza J, Flores O, Reinberg D: Factors involved in specific transcription by mammalian RNA polymerase II. J Biol Chem 266: 9304-9308 (1991).
Nikolov DB, Hu S-H, Lin J, Gasch A, Hoffmann A, Horikoshi M, Chua N-H, Roeder RG, Burley S: Crystal structure of TFIID TATA-box binding protein. Nature 360: 40-46 (1992).
Mukumoto F, Hirose S, Imaseki H, Yamazaki K-I: DNA sequence requirement of a TATAelement-binding protein from Arabidopsisfor transcription in vitro. Plant Mol Biol 23: 995- 1003 (1993).
Yamaguchi Y, Mukumoto F, Imaseki H, Yamazaki K-I: Preparation of in vitrotranscription system of plant origin, with methods and templates for assessing its fidelity. In: Gelvin SB, Schilperoort RA (eds) Plant Molecular Biology Manual, 2nd ed., E2: 1-15. Kluwer Academic Publishers, Dordrecht, the Netherlands (1994).
Kato A, Matsumoto T, Koiwai A, Mizusaki S, Nishida K, Noguchi M, Tamaki E: In: (Terui G (ed) Fermentation Technology Today, pp. 689-695. Society Fermention Technology, Osaka, Japan (1972).
Linsmaier EM, Skoog F: Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18: 100-127 (1965).
Nagata T, Okada K, Takebe I, Matsui C: Delivery of tobacco mosaic virus RNA into plant protoplasts mediated by reverse-phase evaporation vesicles (liposomes). Mol Gen Genet 184: 161-165 (1981).
Takahashi T, Komeda Y: Characterization of two genes encoding small heat-shock proteins in Arabidopsis thaliana. Mol Gen Genet 219: 365-372 (1989).
Sawadogo M, Roeder RG: Factors involved in specific transcription by human RNA polymerase II: analysis by rapid and quantitative in vitroassay. Proc Natl Acad Sci USA 82: 4394- 4398 (1985).
Mori H, Yoshikawa Y, Nishimura I, Nishimura M: Pumpkin malate synthase: cloning and sequencing of the cDNA and nothern blot analysis. Eur J Biochem 197: 331-336 (1991).
Sanger F, Nicklen S, Coulson AR: DNA sequence with chainterminating inhibitors. ProcNatlAcad SciUSA 74: 5463-5467 (1977).
Takeda T, Hirokawa H, Yamazaki K-I: Bending of DNA in solution caused by a protein from Arabidopsisthat binds to a TATA element. Biosci Biotechnol Biochem 58: 916-920 (1994).
Gasch A, Hoffmann A, Horikoshi M, Roeder RG, Chua N-H: Arabidopsis thalianacontains two genes for TFIID. Nature 346: 390-394 (1990).
Holdsworth MJ, Grierson C, Schuch W, Bevan M: DNA-binding properties of cloned TATA-binding protein frompotato tubers. Plant Mol Biol 19: 455-464 (1992).
Haaß MM, Feix G: Two different cDNAs encoding TFIID proteins of maize. FEBS Lett 301: 294-298 (1992).
Kawata T, Minami M, Tamura T, Sumita K, Iwabuchi M: Isolation and characterization of cDNA clone encoding the TATA box-binding protein (TFIID) from wheat. Plant Mol Biol 19: 867-872 (1992).
Apsit V, Freeberg JA, Chase MR, Davis EA, Ackerman S: Wheat TFIID TATA-binding protein. Nucl Acids Res 21: 1494 (1993).
Hoffmann A, Sinn E, Yamamoto T, Wang J, Roy A, Horikoshi M, Roeder RG: Highly conserved core domain and unique N terminus with presumptive regulatory motifs in a human TATA factor (TFIID). Nature 346: 387-390 (1990).
Horikoshi M, Wang CK, Fujii H, Cromlish JA, Weil PA, Roeder RG: Cloning and structure of a yeast gene encoding a general transcription factor TFIID that binds to the TATA box. Nature 341: 299-303 (1989).
Hahn S, Buratowski S, Sharp PA, Guarente L: Isolation of the gene encoding the yeast TATA-binding protein TFIID; a gene identical to the SPT15 suppressor of TY element insertion. Cell 58: 1173-1181 (1989).
Schmidt M, Kao CC, Pei R, Berk AJ: Yeast TATA-box transcription factor gene. Proc Natl Acad Sci USA 86: 7785-7789 (1989).
Cavallini B, Faus I, Matthes H, Chipoulet JM, Winsor B, Egly JM, Chambon P: Cloning of the gene encoding the yeast protein BTF1Y, which can substitute for the human TATA box-binding factor. Proc Natl Acad Sci USA 86: 9803-9807 (1989).
Hoey T, Dynlacht BD, Peterson MG, Pugh BF, Tjian R: Isolation and characterization of the Drosophilagene encoding the TATAbox-binding protein, TFIID. Cell 61: 1179-1186 (1990).
Muhich ML, Iida CT, Horikoshi M, Roeder RG, Parker CS: cDNA clone encoding Drosophilatranscription factor TFIID. Proc Natl Acad Sci USA 87: 9148-9152 (1990).
Nakajima N, Horikoshi M, Roeder RG: Factors involved in specific transcription by mammalian RNA polymerase II: purification, genetic specificity, and TATA box-promoter interactions of TFIID. Mol Cell Biol 8: 4028-4040 (1988).
Lee DK, Dejong J, Hashimoto S, Horikoshi M, Roeder RG: TFIIA induces conformational changes in TFIID via interactions with the basic repeat. Mol Cell Biol 12: 5189-5196 (1992).
Buratowski S, Zhou H: Transcription factor IID mutants defective for interaction with transcription factor IIA. Science 255: 1130-1132 (1992).
Strubin M, Struhl K: Yeast and human TFIID with altered DNA-binding specificity for TATA elements. Cell 68: 721- 730 (1992).
Feaver WJ, Gileadi O, Kornberg RD: Purification and characterization of yeast RNA polymerase II transcription factor b*. J Biol Chem 266: 19000-19005 (1991).
Yamamoto T, Horikoshi M, Wang J, Hasegawa S, Weil PA, Roeder RG: A bipartite DNA-binding domain composed of direct repeats in the TATA box-binding factor TFIID. Proc Natl Acad Sci USA 89: 2844-2848 (1992).
Franklin BP: Mechanism of transcription complex assembly. Curr Opin Cell Biol 8: 303-311 (1996).
Kim TK, Zhao Y, Ge H, Bernstein R, Roeder RG: TATA-binding protein residues implicated in a functional interplay between negative cofactor NC2 (Dr1) and general factors TFIIA and TFIIB. J Biol Chem 270: 10976-10981 (1995).
Heard DJ, Kiss T, Filipowicz W: Both Arabidopsis TATA binding protein (TBP) isoforms are functionally identical in RNA polymerase II and III transcription in plant cell: evidence for gene-specific changes in DNA binding specificity of TBP. EMBO J 12: 3519-3528 (1993).
Yoshida K, Kasai T, Garcia MRC, Sawada S, Shimizu S, Yamazaki K-I, Komeda Y, Shinmyo A: Heat-inducible expression system for foreign gene in cultured tobacco cells with using the HSP18.2 promoter of Arabidopsis thaliana. Appl Microbiol Biotechnol 44: 466-472 (1995).
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Iwataki, N., Hoya, A. & Yamazaki, Ki. Restoration of TATA-dependent transcription in a heat-inactivated extract of tobacco nuclei by recombinant TATA-binding protein (TBP) from tobacco. Plant Mol Biol 34, 69–79 (1997). https://doi.org/10.1023/A:1005759521285
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DOI: https://doi.org/10.1023/A:1005759521285