Abstract
Rapid evolution of ribosomal RNA (rRNA) gene promoters often prevents their recognition in a foreign species. Unlike animal systems, we show that foreign plant rRNA gene promoters are recognized in an alien species, but tend to program transcription by a different polymerase. In plants, RNA polymerase I transcripts initiate at a TATATA element (+1 is underlined) important for promoter strength and start-site selection. However, transcripts initiate from +32 following transfection of a tomato promoter into Arabidopsis. The rRNA gene promoter of a more closely related species, Brassica oleracea, programs both +1 and +29 transcription. A point mutation at +2 improving the identity between the Brassica and Arabidopsis promoters increases +1 transcription, indicating a role for the initiator element in species-specificity. Brassica +29 transcripts can be translated to express a luciferase reporter gene, implicating RNA polymerase II. TATA mutations that disrupt TATA-binding protein (TBP) interactions inhibit +29 transcription and luciferase expression. Co-expressed TBP proteins bearing compensatory mutations restore +29 transcription and luciferase activity, suggesting a direct TBP-TATA interaction. Importantly, +1 transcription is unaffected by the TATA mutations, suggesting that in the context of pol I recognition, the TATA-containing initiator element serves a function other than TBP binding.
Full Text
The Full Text of this article is available as a PDF (208.2 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Barker R. F., Harberd N. P., Jarvis M. G., Flavell R. B. Structure and evolution of the intergenic region in a ribosomal DNA repeat unit of wheat. J Mol Biol. 1988 May 5;201(1):1–17. doi: 10.1016/0022-2836(88)90434-2. [DOI] [PubMed] [Google Scholar]
- Barnes W. M. Variable patterns of expression of luciferase in transgenic tobacco leaves. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9183–9187. doi: 10.1073/pnas.87.23.9183. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bell S. P., Jantzen H. M., Tjian R. Assembly of alternative multiprotein complexes directs rRNA promoter selectivity. Genes Dev. 1990 Jun;4(6):943–954. doi: 10.1101/gad.4.6.943. [DOI] [PubMed] [Google Scholar]
- Bennett R. I., Smith A. G. The complete nucleotide sequence of the intergenic spacer region of an rDNA operon from Brassica oleracea and its comparison with other crucifers. Plant Mol Biol. 1991 Jun;16(6):1095–1098. doi: 10.1007/BF00016085. [DOI] [PubMed] [Google Scholar]
- Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
- Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
- Buratowski S., Hahn S., Guarente L., Sharp P. A. Five intermediate complexes in transcription initiation by RNA polymerase II. Cell. 1989 Feb 24;56(4):549–561. doi: 10.1016/0092-8674(89)90578-3. [DOI] [PubMed] [Google Scholar]
- Comai L., Tanese N., Tjian R. The TATA-binding protein and associated factors are integral components of the RNA polymerase I transcription factor, SL1. Cell. 1992 Mar 6;68(5):965–976. doi: 10.1016/0092-8674(92)90039-f. [DOI] [PubMed] [Google Scholar]
- Conrad-Webb H., Butow R. A. A polymerase switch in the synthesis of rRNA in Saccharomyces cerevisiae. Mol Cell Biol. 1995 May;15(5):2420–2428. doi: 10.1128/mcb.15.5.2420. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cormack B. P., Struhl K. The TATA-binding protein is required for transcription by all three nuclear RNA polymerases in yeast cells. Cell. 1992 May 15;69(4):685–696. doi: 10.1016/0092-8674(92)90232-2. [DOI] [PubMed] [Google Scholar]
- Delcasso-Tremousaygue D., Grellet F., Panabieres F., Ananiev E. D., Delseny M. Structural and transcriptional characterization of the external spacer of a ribosomal RNA nuclear gene from a higher plant. Eur J Biochem. 1988 Mar 15;172(3):767–776. doi: 10.1111/j.1432-1033.1988.tb13956.x. [DOI] [PubMed] [Google Scholar]
- Doelling J. H., Gaudino R. J., Pikaard C. S. Functional analysis of Arabidopsis thaliana rRNA gene and spacer promoters in vivo and by transient expression. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7528–7532. doi: 10.1073/pnas.90.16.7528. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doelling J. H., Pikaard C. S. The minimal ribosomal RNA gene promoter of Arabidopsis thaliana includes a critical element at the transcription initiation site. Plant J. 1995 Nov;8(5):683–692. doi: 10.1046/j.1365-313x.1995.08050683.x. [DOI] [PubMed] [Google Scholar]
- Fan H., Yakura K., Miyanishi M., Sugita M., Sugiura M. In vitro transcription of plant RNA polymerase I-dependent rRNA genes is species-specific. Plant J. 1995 Aug;8(2):295–298. doi: 10.1046/j.1365-313x.1995.08020295.x. [DOI] [PubMed] [Google Scholar]
- Filipowicz W., Kiss T., Marshallsay C., Waibel F. U-snRNA genes, U-snRNAs and U-snRNPs of higher plants. Mol Biol Rep. 1990;14(2-3):125–129. doi: 10.1007/BF00360443. [DOI] [PubMed] [Google Scholar]
- Gerstner J., Schiebel K., von Waldburg G., Hemleben V. Complex organization of the length heterogeneous 5' external spacer of mung bean (Vigna radiata) ribosomal DNA. Genome. 1988 Oct;30(5):723–733. doi: 10.1139/g88-120. [DOI] [PubMed] [Google Scholar]
- Gong X., Radebaugh C. A., Geiss G. K., Simon M. N., Paule M. R. Site-directed photo-cross-linking of rRNA transcription initiation complexes. Mol Cell Biol. 1995 Sep;15(9):4956–4963. doi: 10.1128/mcb.15.9.4956. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grummt I., Roth E., Paule M. R. Ribosomal RNA transcription in vitro is species specific. Nature. 1982 Mar 11;296(5853):173–174. doi: 10.1038/296173a0. [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]
- Johnson S. P., Warner J. R. Unusual enhancer function in yeast rRNA transcription. Mol Cell Biol. 1989 Nov;9(11):4986–4993. doi: 10.1128/mcb.9.11.4986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karpen G. H., Schaefer J. E., Laird C. D. A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation. Genes Dev. 1988 Dec;2(12B):1745–1763. doi: 10.1101/gad.2.12b.1745. [DOI] [PubMed] [Google Scholar]
- Learned R. M., Cordes S., Tjian R. Purification and characterization of a transcription factor that confers promoter specificity to human RNA polymerase I. Mol Cell Biol. 1985 Jun;5(6):1358–1369. doi: 10.1128/mcb.5.6.1358. [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]
- Lobo S. M., Lister J., Sullivan M. L., Hernandez N. The cloned RNA polymerase II transcription factor IID selects RNA polymerase III to transcribe the human U6 gene in vitro. Genes Dev. 1991 Aug;5(8):1477–1489. doi: 10.1101/gad.5.8.1477. [DOI] [PubMed] [Google Scholar]
- McMullen M. D., Hunter B., Phillips R. L., Rubenstein I. The structure of the maize ribosomal DNA spacer region. Nucleic Acids Res. 1986 Jun 25;14(12):4953–4968. doi: 10.1093/nar/14.12.4953. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miesfeld R., Arnheim N. Species-specific rDNA transcription is due to promoter-specific binding factors. Mol Cell Biol. 1984 Feb;4(2):221–227. doi: 10.1128/mcb.4.2.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mishima Y., Financsek I., Kominami R., Muramatsu M. Fractionation and reconstitution of factors required for accurate transcription of mammalian ribosomal RNA genes: identification of a species-dependent initiation factor. Nucleic Acids Res. 1982 Nov 11;10(21):6659–6670. doi: 10.1093/nar/10.21.6659. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moss T., Stefanovsky V. Y. Promotion and regulation of ribosomal transcription in eukaryotes by RNA polymerase I. Prog Nucleic Acid Res Mol Biol. 1995;50:25–66. doi: 10.1016/s0079-6603(08)60810-7. [DOI] [PubMed] [Google Scholar]
- Nogi Y., Yano R., Nomura M. Synthesis of large rRNAs by RNA polymerase II in mutants of Saccharomyces cerevisiae defective in RNA polymerase I. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3962–3966. doi: 10.1073/pnas.88.9.3962. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pape L. K., Windle J. J., Sollner-Webb B. Half helical turn spacing changes convert a frog into a mouse rDNA promoter: a distant upstream domain determines the helix face of the initiation site. Genes Dev. 1990 Jan;4(1):52–62. doi: 10.1101/gad.4.1.52. [DOI] [PubMed] [Google Scholar]
- Perry K. L., Palukaitis P. Transcription of tomato ribosomal DNA and the organization of the intergenic spacer. Mol Gen Genet. 1990 Mar;221(1):103–112. doi: 10.1007/BF00280374. [DOI] [PubMed] [Google Scholar]
- Petes T. D. Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell. 1980 Mar;19(3):765–774. doi: 10.1016/s0092-8674(80)80052-3. [DOI] [PubMed] [Google Scholar]
- Piller K. J., Baerson S. R., Polans N. O., Kaufman L. S. Structural analysis of the short length ribosomal DNA variant from Pisum sativum L. cv. Alaska. Nucleic Acids Res. 1990 Jun 11;18(11):3135–3145. doi: 10.1093/nar/18.11.3135. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Radebaugh C. A., Matthews J. L., Geiss G. K., Liu F., Wong J. M., Bateman E., Camier S., Sentenac A., Paule M. R. TATA box-binding protein (TBP) is a constituent of the polymerase I-specific transcription initiation factor TIF-IB (SL1) bound to the rRNA promoter and shows differential sensitivity to TBP-directed reagents in polymerase I, II, and III transcription factors. Mol Cell Biol. 1994 Jan;14(1):597–605. doi: 10.1128/mcb.14.1.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reeder R. H. Enhancers and ribosomal gene spacers. Cell. 1984 Sep;38(2):349–351. doi: 10.1016/0092-8674(84)90489-6. [DOI] [PubMed] [Google Scholar]
- Reeder R. H. Regulatory elements of the generic ribosomal gene. Curr Opin Cell Biol. 1989 Jun;1(3):466–474. doi: 10.1016/0955-0674(89)90007-0. [DOI] [PubMed] [Google Scholar]
- Rhoads R. E. Cap recognition and the entry of mRNA into the protein synthesis initiation cycle. Trends Biochem Sci. 1988 Feb;13(2):52–56. doi: 10.1016/0968-0004(88)90028-x. [DOI] [PubMed] [Google Scholar]
- Rudloff U., Eberhard D., Grummt I. The conserved core domain of the human TATA binding protein is sufficient to assemble the multisubunit RNA polymerase I-specific transcription factor SL1. Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8229–8233. doi: 10.1073/pnas.91.17.8229. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rudloff U., Eberhard D., Tora L., Stunnenberg H., Grummt I. TBP-associated factors interact with DNA and govern species specificity of RNA polymerase I transcription. EMBO J. 1994 Jun 1;13(11):2611–2616. doi: 10.1002/j.1460-2075.1994.tb06551.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Safrany G., Tanaka N., Kishimoto T., Ishikawa Y., Kato H., Kominami R., Muramatsu M. Structural determinant of the species-specific transcription of the mouse rRNA gene promoter. Mol Cell Biol. 1989 Jan;9(1):349–353. doi: 10.1128/mcb.9.1.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scheer U., Weisenberger D. The nucleolus. Curr Opin Cell Biol. 1994 Jun;6(3):354–359. doi: 10.1016/0955-0674(94)90026-4. [DOI] [PubMed] [Google Scholar]
- Schnapp A., Rosenbauer H., Grummt I. Trans-acting factors involved in species-specificity and control of mouse ribosomal gene transcription. 1991 May 29-Jun 12Mol Cell Biochem. 104(1-2):137–147. doi: 10.1007/BF00229813. [DOI] [PubMed] [Google Scholar]
- Schultz M. C., Reeder R. H., Hahn S. Variants of the TATA-binding protein can distinguish subsets of RNA polymerase I, II, and III promoters. Cell. 1992 May 15;69(4):697–702. doi: 10.1016/0092-8674(92)90233-3. [DOI] [PubMed] [Google Scholar]
- Strubin M., Struhl K. Yeast and human TFIID with altered DNA-binding specificity for TATA elements. Cell. 1992 Feb 21;68(4):721–730. doi: 10.1016/0092-8674(92)90147-5. [DOI] [PubMed] [Google Scholar]
- Szostak J. W., Wu R. Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae. Nature. 1980 Apr 3;284(5755):426–430. doi: 10.1038/284426a0. [DOI] [PubMed] [Google Scholar]
- Toloczyki C., Feix G. Occurrence of 9 homologous repeat units in the external spacer region of a nuclear maize rRNA gene unit. Nucleic Acids Res. 1986 Jun 25;14(12):4969–4986. doi: 10.1093/nar/14.12.4969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Torres R. A., Zentgraf U., Hemleben V. Species and genus specificity of the intergenic spacer (IGS) in the ribosomal RNA genes of Cucurbitaceae. Z Naturforsch C. 1989 Nov-Dec;44(11-12):1029–1034. doi: 10.1515/znc-1989-11-1224. [DOI] [PubMed] [Google Scholar]
- Tremousaygue D., Laudie M., Grellet F., Delseny M. The Brassica oleracea rDNA spacer revisited. Plant Mol Biol. 1992 Mar;18(5):1013–1018. doi: 10.1007/BF00019222. [DOI] [PubMed] [Google Scholar]
- Vincentz M., Flavell R. B. Mapping of ribosomal RNA transcripts in wheat. Plant Cell. 1989 Jun;1(6):579–589. doi: 10.1105/tpc.1.6.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Waibel F., Filipowicz W. The spacing between two promoter elements determines RNA polymerase specificity during transcription of U small nuclear RNA genes of Arabidopsis. Mol Biol Rep. 1990;14(2-3):149–149. doi: 10.1007/BF00360453. [DOI] [PubMed] [Google Scholar]
- Wilkinson J. K., Sollner-Webb B. Transcription of Xenopus ribosomal RNA genes by RNA polymerase I in vitro. J Biol Chem. 1982 Dec 10;257(23):14375–14383. [PubMed] [Google Scholar]
- Wobbe C. R., Struhl K. Yeast and human TATA-binding proteins have nearly identical DNA sequence requirements for transcription in vitro. Mol Cell Biol. 1990 Aug;10(8):3859–3867. doi: 10.1128/mcb.10.8.3859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zawel L., Reinberg D. Initiation of transcription by RNA polymerase II: a multi-step process. Prog Nucleic Acid Res Mol Biol. 1993;44:67–108. doi: 10.1016/s0079-6603(08)60217-2. [DOI] [PubMed] [Google Scholar]
- Zentgraf U., Ganal M., Hemleben V. Length heterogeneity of the rRNA precursor in cucumber (Cucumis sativus). Plant Mol Biol. 1990 Sep;15(3):465–474. doi: 10.1007/BF00019163. [DOI] [PubMed] [Google Scholar]