Abstract
RNA polymerase (Pol) II- and RNA Pol III-transcribed small nuclear RNA (snRNA) genes of dicotyledonous plants contain two essential upstream promoter elements, the USE and TATA. The USE is a highly conserved plant snRNA gene-specific element, and its distance from the -30 TATA box, corresponding to approximately three and four helical DNA turns in Pol III and Pol II genes, respectively, is crucial for determining RNA Pol specificity of transcription. Sequences upstream of the USE play no role in snRNA gene transcription in dicot plants. Here we show that for expression of snRNA genes in maize, a monocotyledonous plant, the USE and TATA elements are essential, but not sufficient, for transcription. Efficient expression of both Pol II- and Pol III-specific snRNA genes in transfected maize protoplasts requires an additional element(s) positioned upstream of the USE. This element, named MSP (for monocot-specific promoter; consensus, RGCCCR), is present in one to three copies in monocot snRNA genes and is interchangeable between Pol II- and Pol III-specific genes. The efficiency of snRNA gene expression in maize protoplast is determined primarily by the strength of the MSP element(s); this contrasts with the situation in protoplasts of a dicot plant, Nicotiana plumbaginifolia, where promoter strength is a function of the quality of the USE element. Interestingly, the organization of monocot Pol III-specific snRNA gene promoters closely resembles those of equivalent vertebrate promoters. The data are discussed in the context of the coevolution of Pol II- and Pol III-specific snRNA gene promoters within many eukaryotic organisms.
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- Brown J. W., Waugh R. Maize U2 snRNAs: gene sequence and expression. Nucleic Acids Res. 1989 Nov 25;17(22):8991–9001. doi: 10.1093/nar/17.22.8991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carbon P., Murgo S., Ebel J. P., Krol A., Tebb G., Mattaj L. W. A common octamer motif binding protein is involved in the transcription of U6 snRNA by RNA polymerase III and U2 snRNA by RNA polymerase II. Cell. 1987 Oct 9;51(1):71–79. doi: 10.1016/0092-8674(87)90011-0. [DOI] [PubMed] [Google Scholar]
- Ciliberto G., Palla F., Tebb G., Mattaj I. W., Philipson L. Properties of a U1 RNA enhancer-like sequence. Nucleic Acids Res. 1987 Mar 25;15(6):2403–2416. doi: 10.1093/nar/15.6.2403. [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]
- Dahlberg J. E., Schenborn E. T. The human U1 snRNA promoter and enhancer do not direct synthesis of messenger RNA. Nucleic Acids Res. 1988 Jul 11;16(13):5827–5840. doi: 10.1093/nar/16.13.5827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eschenlauer J. B., Kaiser M. W., Gerlach V. L., Brow D. A. Architecture of a yeast U6 RNA gene promoter. Mol Cell Biol. 1993 May;13(5):3015–3026. doi: 10.1128/mcb.13.5.3015. [DOI] [PMC free article] [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]
- Fenoll C., Schwarz J. J., Black D. M., Schneider M., Howell S. H. The intergenic region of maize streak virus contains a GC-rich element that activates rightward transcription and binds maize nuclear factors. Plant Mol Biol. 1990 Dec;15(6):865–877. doi: 10.1007/BF00039426. [DOI] [PubMed] [Google Scholar]
- Filipowicz W., Kiss T. Structure and function of nucleolar snRNPs. Mol Biol Rep. 1993 Aug;18(2):149–156. doi: 10.1007/BF00986770. [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]
- 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]
- 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]
- Leader D., Connelly S., Filipowicz W., Waugh R., Brown J. W. Differential expression of U5snRNA gene variants in maize (Zea mays) protoplasts. Plant Mol Biol. 1993 Jan;21(1):133–143. doi: 10.1007/BF00039624. [DOI] [PubMed] [Google Scholar]
- Lescure A., Carbon P., Krol A. The different positioning of the proximal sequence element in the Xenopus RNA polymerase II and III snRNA promoters is a key determinant which confers RNA polymerase III specificity. Nucleic Acids Res. 1991 Feb 11;19(3):435–441. doi: 10.1093/nar/19.3.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lo P. C., Mount S. M. Drosophila melanogaster genes for U1 snRNA variants and their expression during development. Nucleic Acids Res. 1990 Dec 11;18(23):6971–6979. doi: 10.1093/nar/18.23.6971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lobo S. M., Hernandez N. A 7 bp mutation converts a human RNA polymerase II snRNA promoter into an RNA polymerase III promoter. Cell. 1989 Jul 14;58(1):55–67. doi: 10.1016/0092-8674(89)90402-9. [DOI] [PubMed] [Google Scholar]
- Lührmann R., Kastner B., Bach M. Structure of spliceosomal snRNPs and their role in pre-mRNA splicing. Biochim Biophys Acta. 1990 Nov 30;1087(3):265–292. doi: 10.1016/0167-4781(90)90001-i. [DOI] [PubMed] [Google Scholar]
- Margottin F., Dujardin G., Gérard M., Egly J. M., Huet J., Sentenac A. Participation of the TATA factor in transcription of the yeast U6 gene by RNA polymerase C. Science. 1991 Jan 25;251(4992):424–426. doi: 10.1126/science.1989075. [DOI] [PubMed] [Google Scholar]
- Marshallsay C., Connelly S., Filipowicz W. Characterization of the U3 and U6 snRNA genes from wheat: U3 snRNA genes in monocot plants are transcribed by RNA polymerase III. Plant Mol Biol. 1992 Sep;19(6):973–983. doi: 10.1007/BF00040529. [DOI] [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]
- Mattaj I. W., Dathan N. A., Parry H. D., Carbon P., Krol A. Changing the RNA polymerase specificity of U snRNA gene promoters. Cell. 1988 Nov 4;55(3):435–442. doi: 10.1016/0092-8674(88)90029-3. [DOI] [PubMed] [Google Scholar]
- Murgo S., Krol A., Carbon P. Sequence, organization and transcriptional analysis of a gene encoding a U1 snRNA from the axolotl, Ambystoma mexicanum. Gene. 1991 Mar 15;99(2):163–170. doi: 10.1016/0378-1119(91)90123-s. [DOI] [PubMed] [Google Scholar]
- Murphy S., Moorefield B., Pieler T. Common mechanisms of promoter recognition by RNA polymerases II and III. Trends Genet. 1989 Apr;5(4):122–126. doi: 10.1016/0168-9525(89)90043-7. [DOI] [PubMed] [Google Scholar]
- Mémet S., Saurin W., Sentenac A. RNA polymerases B and C are more closely related to each other than to RNA polymerase A. J Biol Chem. 1988 Jul 25;263(21):10048–10051. [PubMed] [Google Scholar]
- Parker R., Simmons T., Shuster E. O., Siliciano P. G., Guthrie C. Genetic analysis of small nuclear RNAs in Saccharomyces cerevisiae: viable sextuple mutant. Mol Cell Biol. 1988 Aug;8(8):3150–3159. doi: 10.1128/mcb.8.8.3150. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simmen K. A., Waldschmidt R., Bernués J., Parry H. D., Seifart K. H., Mattaj I. W. Proximal sequence element factor binding and species specificity in vertebrate U6 snRNA promoters. J Mol Biol. 1992 Feb 20;223(4):873–884. doi: 10.1016/0022-2836(92)90249-j. [DOI] [PubMed] [Google Scholar]
- Stefanovic B., Marzluff W. F. Characterization of two developmentally regulated sea urchin U2 small nuclear RNA promoters: a common required TATA sequence and independent proximal and distal elements. Mol Cell Biol. 1992 Feb;12(2):650–660. doi: 10.1128/mcb.12.2.650. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas J., Lea K., Zucker-Aprison E., Blumenthal T. The spliceosomal snRNAs of Caenorhabditis elegans. Nucleic Acids Res. 1990 May 11;18(9):2633–2642. doi: 10.1093/nar/18.9.2633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vankan P., Edoh D., Filipowicz W. Structure and expression of the U5 snRNA gene of Arabidopsis thaliana. Conserved upstream sequence elements in plant U-RNA genes. Nucleic Acids Res. 1988 Nov 25;16(22):10425–10440. doi: 10.1093/nar/16.22.10425. [DOI] [PMC free article] [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]
- Vankan P., Filipowicz W. Structure of U2 snRNA genes of Arabidopsis thaliana and their expression in electroporated plant protoplasts. EMBO J. 1988 Mar;7(3):791–799. doi: 10.1002/j.1460-2075.1988.tb02877.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]
- Wendelburg B. J., Marzluff W. F. Two promoter elements are necessary and sufficient for expression of the sea urchin U1 snRNA gene. Nucleic Acids Res. 1992 Jul 25;20(14):3743–3751. doi: 10.1093/nar/20.14.3743. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zamrod Z., Tyree C. M., Song Y., Stumph W. E. In vitro transcription of a Drosophila U1 small nuclear RNA gene requires TATA box-binding protein and two proximal cis-acting elements with stringent spacing requirements. Mol Cell Biol. 1993 Sep;13(9):5918–5927. doi: 10.1128/mcb.13.9.5918. [DOI] [PMC free article] [PubMed] [Google Scholar]