Abstract
The genes transcribed by RNA polymerase (pol) III can be placed into four distinct groups based on the nature and position of their promoter elements. In the higher eukaryotes equivalent genes usually belong to the same sub-type of pol III promoters and there are few examples of genes which have changed promoter type during evolution. In this work we demonstrate that the promoter of the Arabidopsis thaliana 7SL RNA gene is located upstream of the coding region and is identical to the promoters of pol III-specific plant U-small nuclear RNA (U-snRNA) genes. Sequence analysis of two different 7SL genes from A. thaliana revealed that both genes contain two sequence elements in their 5' flanking regions identical in sequence and position to the highly conserved USE and TATA elements of the pol III-transcribed plant U-snRNA genes. Mutational analysis of these elements in the At7SL-2 gene indicates that the USE and TATA elements are both necessary and account for > or = 90% of the transcriptional activity of this gene in transfected plant protoplasts. Within the coding region of both genes there is a sequence element which is a 10/11 nt match to the consensus B-box element of tRNA genes, however, this element is not important for gene activity. These findings distinguish the plant genes from the human 7SL gene, which has both internal and upstream promoter elements and its upstream elements are different from those found in the human U-snRNA genes.
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Selected References
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- Bredow S., Kleinert H., Benecke B. J. Sequence and factor requirements for faithful in vitro transcription of human 7SL DNA. Gene. 1990 Feb 14;86(2):217–225. doi: 10.1016/0378-1119(90)90282-v. [DOI] [PubMed] [Google Scholar]
- Bredow S., Sürig D., Müller J., Kleinert H., Benecke B. J. Activating-transcription-factor (ATF) regulates human 7S L RNA transcription by RNA polymerase III in vivo and in vitro. Nucleic Acids Res. 1990 Dec 11;18(23):6779–6784. doi: 10.1093/nar/18.23.6779. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burnol A. F., Margottin F., Schultz P., Marsolier M. C., Oudet P., Sentenac A. Basal promoter and enhancer element of yeast U6 snRNA gene. J Mol Biol. 1993 Oct 20;233(4):644–658. doi: 10.1006/jmbi.1993.1542. [DOI] [PubMed] [Google Scholar]
- Campos N., Palau J., Zwieb C. Diversity of 7 SL RNA from the signal recognition particle of maize endosperm. Nucleic Acids Res. 1989 Feb 25;17(4):1573–1588. doi: 10.1093/nar/17.4.1573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carbon P., Krol A. Transcription of the Xenopus laevis selenocysteine tRNA(Ser)Sec gene: a system that combines an internal B box and upstream elements also found in U6 snRNA genes. EMBO J. 1991 Mar;10(3):599–606. doi: 10.1002/j.1460-2075.1991.tb07987.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Connelly S., Filipowicz W. Activity of chimeric U small nuclear RNA (snRNA)/mRNA genes in transfected protoplasts of Nicotiana plumbaginifolia: U snRNA 3'-end formation and transcription initiation can occur independently in plants. Mol Cell Biol. 1993 Oct;13(10):6403–6415. doi: 10.1128/mcb.13.10.6403. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gabrielsen O. S., Sentenac A. RNA polymerase III (C) and its transcription factors. Trends Biochem Sci. 1991 Nov;16(11):412–416. doi: 10.1016/0968-0004(91)90166-s. [DOI] [PubMed] [Google Scholar]
- Geiduschek E. P., Tocchini-Valentini G. P. Transcription by RNA polymerase III. Annu Rev Biochem. 1988;57:873–914. doi: 10.1146/annurev.bi.57.070188.004301. [DOI] [PubMed] [Google Scholar]
- Goodall G. J., Filipowicz W. The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell. 1989 Aug 11;58(3):473–483. doi: 10.1016/0092-8674(89)90428-5. [DOI] [PubMed] [Google Scholar]
- Goodall G. J., Wiebauer K., Filipowicz W. Analysis of pre-mRNA processing in transfected plant protoplasts. Methods Enzymol. 1990;181:148–161. doi: 10.1016/0076-6879(90)81117-d. [DOI] [PubMed] [Google Scholar]
- Haas B., Klanner A., Ramm K., Sänger H. L. The 7S RNA from tomato leaf tissue resembles a signal recognition particle RNA and exhibits a remarkable sequence complementarity to viroids. EMBO J. 1988 Dec 20;7(13):4063–4074. doi: 10.1002/j.1460-2075.1988.tb03300.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heard D. J., Kiss T., Filipowicz W. Both Arabidopsis TATA binding protein (TBP) isoforms are functionally identical in RNA polymerase II and III transcription in plant cells: evidence for gene-specific changes in DNA binding specificity of TBP. EMBO J. 1993 Sep;12(9):3519–3528. doi: 10.1002/j.1460-2075.1993.tb06026.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hernandez N. TBP, a universal eukaryotic transcription factor? Genes Dev. 1993 Jul;7(7B):1291–1308. doi: 10.1101/gad.7.7b.1291. [DOI] [PubMed] [Google Scholar]
- Howe J. G., Shu M. D. Epstein-Barr virus small RNA (EBER) genes: unique transcription units that combine RNA polymerase II and III promoter elements. Cell. 1989 Jun 2;57(5):825–834. doi: 10.1016/0092-8674(89)90797-6. [DOI] [PubMed] [Google Scholar]
- Kiss T., Marshallsay C., Filipowicz W. 7-2/MRP RNAs in plant and mammalian cells: association with higher order structures in the nucleolus. EMBO J. 1992 Oct;11(10):3737–3746. doi: 10.1002/j.1460-2075.1992.tb05459.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kiss T., Marshallsay C., Filipowicz W. Alteration of the RNA polymerase specificity of U3 snRNA genes during evolution and in vitro. Cell. 1991 May 3;65(3):517–526. doi: 10.1016/0092-8674(91)90469-f. [DOI] [PubMed] [Google Scholar]
- Kiss T., Solymosy F. Molecular analysis of a U3 RNA gene locus in tomato: transcription signals, the coding region, expression in transgenic tobacco plants and tandemly repeated pseudogenes. Nucleic Acids Res. 1990 Apr 25;18(8):1941–1949. doi: 10.1093/nar/18.8.1941. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kleinert H., Gladen A., Geisler M., Benecke B. J. Differential regulation of transcription of human 7 S K and 7 S L RNA genes. J Biol Chem. 1988 Aug 15;263(23):11511–11515. [PubMed] [Google Scholar]
- Krol A., Ebel J. P., Rinke J., Luhrmann R. U1, U2 and U5 small nuclear RNAs are found in plants cells. Complete nucleotide sequence of the U5 RNA family from pea nuclei. Nucleic Acids Res. 1983 Dec 20;11(24):8583–8594. doi: 10.1093/nar/11.24.8583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kunkel G. R. RNA polymerase III transcription of genes that lack internal control regions. Biochim Biophys Acta. 1991 Jan 17;1088(1):1–9. doi: 10.1016/0167-4781(91)90146-d. [DOI] [PubMed] [Google Scholar]
- Lee B. J., Kang S. G., Hatfield D. Transcription of Xenopus selenocysteine tRNA Ser (formerly designated opal suppressor phosphoserine tRNA) gene is directed by multiple 5'-extragenic regulatory elements. J Biol Chem. 1989 Jun 5;264(16):9696–9702. [PubMed] [Google Scholar]
- Marques J. P., Gualberto J. M., Palme K. Sequence of the Arabidopsis thaliana 7SL RNA gene. Nucleic Acids Res. 1993 Jul 25;21(15):3581–3581. doi: 10.1093/nar/21.15.3581. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marshallsay C., Kiss T., Filipowicz W. Amplification of plant U3 and U6 snRNA gene sequences using primers specific for an upstream promoter element and conserved intragenic regions. Nucleic Acids Res. 1990 Jun 25;18(12):3459–3466. doi: 10.1093/nar/18.12.3459. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marshallsay C., Prehn S., Zwieb C. cDNA cloning of the wheat germ SRP 7S RNAs. Nucleic Acids Res. 1989 Feb 25;17(4):1771–1771. doi: 10.1093/nar/17.4.1771. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Myslinski E., Schuster C., Krol A., Carbon P. Promoter strength and structure dictate module composition in RNA polymerase III transcriptional activator elements. J Mol Biol. 1993 Nov 20;234(2):311–318. doi: 10.1006/jmbi.1993.1588. [DOI] [PubMed] [Google Scholar]
- Nakaar V., Dare A. O., Hong D., Ullu E., Tschudi C. Upstream tRNA genes are essential for expression of small nuclear and cytoplasmic RNA genes in trypanosomes. Mol Cell Biol. 1994 Oct;14(10):6736–6742. doi: 10.1128/mcb.14.10.6736. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Palida F. A., Hale C., Sprague K. U. Transcription of a silkworm tRNA(cAla) gene is directed by two AT-rich upstream sequence elements. Nucleic Acids Res. 1993 Dec 25;21(25):5875–5881. doi: 10.1093/nar/21.25.5875. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parry H. D., Mattaj I. W. Positive and negative functional interactions between promoter elements from different classes of RNA polymerase III-transcribed genes. EMBO J. 1990 Apr;9(4):1097–1104. doi: 10.1002/j.1460-2075.1990.tb08215.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ribes V., Dehoux P., Tollervey D. 7SL RNA from Schizosaccharomyces pombe is encoded by a single copy essential gene. EMBO J. 1988 Jan;7(1):231–237. doi: 10.1002/j.1460-2075.1988.tb02804.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharp S. J., Schaack J., Cooley L., Burke D. J., Söll D. Structure and transcription of eukaryotic tRNA genes. CRC Crit Rev Biochem. 1985;19(2):107–144. doi: 10.3109/10409238509082541. [DOI] [PubMed] [Google Scholar]
- Shimomura S., Liu W., Inohara N., Watanabe S., Futai M. Structure of the gene for an auxin-binding protein and a gene for 7SL RNA from Arabidopsis thaliana. Plant Cell Physiol. 1993 Jun;34(4):633–637. [PubMed] [Google Scholar]
- Strub K., Moss J., Walter P. Binding sites of the 9- and 14-kilodalton heterodimeric protein subunit of the signal recognition particle (SRP) are contained exclusively in the Alu domain of SRP RNA and contain a sequence motif that is conserved in evolution. Mol Cell Biol. 1991 Aug;11(8):3949–3959. doi: 10.1128/mcb.11.8.3949. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ullu E., Weiner A. M. Upstream sequences modulate the internal promoter of the human 7SL RNA gene. 1985 Nov 28-Dec 4Nature. 318(6044):371–374. doi: 10.1038/318371a0. [DOI] [PubMed] [Google Scholar]
- Vankan P., Filipowicz W. A U-snRNA gene-specific upstream element and a -30 'TATA box' are required for transcription of the U2 snRNA gene of Arabidopsis thaliana. EMBO J. 1989 Dec 1;8(12):3875–3882. doi: 10.1002/j.1460-2075.1989.tb08566.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Waibel F., Filipowicz W. RNA-polymerase specificity of transcription of Arabidopsis U snRNA genes determined by promoter element spacing. Nature. 1990 Jul 12;346(6280):199–202. doi: 10.1038/346199a0. [DOI] [PubMed] [Google Scholar]
- Waibel F., Filipowicz W. U6 snRNA genes of Arabidopsis are transcribed by RNA polymerase III but contain the same two upstream promoter elements as RNA polymerase II-transcribed U-snRNA genes. Nucleic Acids Res. 1990 Jun 25;18(12):3451–3458. doi: 10.1093/nar/18.12.3451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willis I. M. RNA polymerase III. Genes, factors and transcriptional specificity. Eur J Biochem. 1993 Feb 15;212(1):1–11. doi: 10.1111/j.1432-1033.1993.tb17626.x. [DOI] [PubMed] [Google Scholar]
- Zwieb C. The secondary structure of the 7SL RNA in the signal recognition particle: functional implications. Nucleic Acids Res. 1985 Sep 11;13(17):6105–6124. doi: 10.1093/nar/13.17.6105. [DOI] [PMC free article] [PubMed] [Google Scholar]