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. 1997 Jul 1;16(13):4041–4048. doi: 10.1093/emboj/16.13.4041

The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids.

P T Hajdukiewicz 1, L A Allison 1, P Maliga 1
PMCID: PMC1170027  PMID: 9233813

Abstract

The plastid genome in photosynthetic higher plants encodes subunits of an Escherichia coli-like RNA polymerase (PEP) which initiates transcription from E.coli sigma70-type promoters. We have previously established the existence of a second nuclear-encoded plastid RNA polymerase (NEP) in photosynthetic higher plants. We report here that many plastid genes and operons have at least one promoter each for PEP and NEP (Class II transcription unit). However, a subset of plastid genes, including photosystem I and II genes, are transcribed from PEP promoters only (Class I genes), while in some instances (e.g. accD) genes are transcribed exclusively by NEP (Class III genes). Sequence alignment identified a 10 nucleotide NEP promoter consensus around the transcription initiation site. Distinct NEP and PEP promoters reported here provide a general mechanism for group-specific gene expression through recognition by the two RNA polymerases.

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Selected References

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  1. Allison L. A., Maliga P. Light-responsive and transcription-enhancing elements regulate the plastid psbD core promoter. EMBO J. 1995 Aug 1;14(15):3721–3730. doi: 10.1002/j.1460-2075.1995.tb00042.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allison L. A., Simon L. D., Maliga P. Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J. 1996 Jun 3;15(11):2802–2809. [PMC free article] [PubMed] [Google Scholar]
  3. Baumgartner B. J., Rapp J. C., Mullet J. E. Plastid Genes Encoding the Transcription/Translation Apparatus Are Differentially Transcribed Early in Barley (Hordeum vulgare) Chloroplast Development (Evidence for Selective Stabilization of psbA mRNA). Plant Physiol. 1993 Mar;101(3):781–791. doi: 10.1104/pp.101.3.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carrillo N., Seyer P., Tyagi A., Herrmann R. G. Cytochrome b-559 genes from Oenothera hookeri and Nicotiana tabacum show a remarkably high degree of conservation as compared to spinach. The enigma of cytochrome b-559: highly conserved genes and proteins but no known function. Curr Genet. 1986;10(8):619–624. doi: 10.1007/BF00418129. [DOI] [PubMed] [Google Scholar]
  5. DuBell A. N., Mullet J. E. Differential Transcription of Pea Chloroplast Genes during Light-Induced Leaf Development (Continuous Far-Red Light Activates Chloroplast Transcription). Plant Physiol. 1995 Sep;109(1):105–112. doi: 10.1104/pp.109.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gray J. C., Hird S. M., Dyer T. A. Nucleotide sequence of a wheat chloroplast gene encoding the proteolytic subunit of an ATP-dependent protease. Plant Mol Biol. 1990 Dec;15(6):947–950. doi: 10.1007/BF00039435. [DOI] [PubMed] [Google Scholar]
  7. Hess W. R., Prombona A., Fieder B., Subramanian A. R., Börner T. Chloroplast rps15 and the rpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids: evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J. 1993 Feb;12(2):563–571. doi: 10.1002/j.1460-2075.1993.tb05688.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Iratni R., Baeza L., Andreeva A., Mache R., Lerbs-Mache S. Regulation of rDNA transcription in chloroplasts: promoter exclusion by constitutive repression. Genes Dev. 1994 Dec 1;8(23):2928–2938. doi: 10.1101/gad.8.23.2928. [DOI] [PubMed] [Google Scholar]
  9. Kapoor S., Wakasugi T., Deno H., Sugiura M. An atpE-specific promoter within the coding region of the atpB gene in tobacco chloroplast DNA. Curr Genet. 1994 Sep;26(3):263–268. doi: 10.1007/BF00309558. [DOI] [PubMed] [Google Scholar]
  10. Kim M., Mullet J. E. Identification of a sequence-specific DNA binding factor required for transcription of the barley chloroplast blue light-responsive psbD-psbC promoter. Plant Cell. 1995 Sep;7(9):1445–1457. doi: 10.1105/tpc.7.9.1445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lerbs-Mache S. The 110-kDa polypeptide of spinach plastid DNA-dependent RNA polymerase: single-subunit enzyme or catalytic core of multimeric enzyme complexes? Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5509–5513. doi: 10.1073/pnas.90.12.5509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Matsubayashi T., Wakasugi T., Shinozaki K., Yamaguchi-Shinozaki K., Zaita N., Hidaka T., Meng B. Y., Ohto C., Tanaka M., Kato A. Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of the splice sites in ndhA and ndhB pre-mRNAs. Mol Gen Genet. 1987 Dec;210(3):385–393. doi: 10.1007/BF00327187. [DOI] [PubMed] [Google Scholar]
  13. Maurizi M. R., Clark W. P., Kim S. H., Gottesman S. Clp P represents a unique family of serine proteases. J Biol Chem. 1990 Jul 25;265(21):12546–12552. [PubMed] [Google Scholar]
  14. Meng B. Y., Tanaka M., Wakasugi T., Ohme M., Shinozaki K., Sugiura M. Cotranscription of the genes encoding two P700 chlorophyll a apoproteins with the gene for ribosomal protein CS14: determination of the transcriptional initiation site by in vitro capping. Curr Genet. 1988 Oct;14(4):395–400. doi: 10.1007/BF00419998. [DOI] [PubMed] [Google Scholar]
  15. Mullet J. E. Dynamic regulation of chloroplast transcription. Plant Physiol. 1993 Oct;103(2):309–313. doi: 10.1104/pp.103.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Orozco E. M., Jr, Chen L. J., Eilers R. J. The divergently transcribed rbcL and atpB genes of tobacco plastid DNA are separated by nineteen base pairs. Curr Genet. 1990 Jan;17(1):65–71. doi: 10.1007/BF00313250. [DOI] [PubMed] [Google Scholar]
  17. Raskin C. A., Diaz G. A., McAllister W. T. T7 RNA polymerase mutants with altered promoter specificities. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3147–3151. doi: 10.1073/pnas.90.8.3147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Sasaki Y., Hakamada K., Suama Y., Nagano Y., Furusawa I., Matsuno R. Chloroplast-encoded protein as a subunit of acetyl-CoA carboxylase in pea plant. J Biol Chem. 1993 Nov 25;268(33):25118–25123. [PubMed] [Google Scholar]
  19. Sasaki Y., Konishi T., Nagano Y. The Compartmentation of Acetyl-Coenzyme A Carboxylase in Plants. Plant Physiol. 1995 Jun;108(2):445–449. doi: 10.1104/pp.108.2.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Shinozaki K., Ohme M., Tanaka M., Wakasugi T., Hayashida N., Matsubayashi T., Zaita N., Chunwongse J., Obokata J., Yamaguchi-Shinozaki K. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 1986 Sep;5(9):2043–2049. doi: 10.1002/j.1460-2075.1986.tb04464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sun E., Wu B. W., Tewari K. K. In vitro analysis of the pea chloroplast 16S rRNA gene promoter. Mol Cell Biol. 1989 Dec;9(12):5650–5659. doi: 10.1128/mcb.9.12.5650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tanaka M, Obokata J, Chunwongse J, Shinozaki K, Sugiura M. Rapid splicing and stepwise processing of a transcript from the psbB operon in tobacco chloroplasts: determination of the intron sites in petB and petD. Mol Gen Genet. 1987 Oct;209(3):427–431. doi: 10.1007/BF00331145. [DOI] [PubMed] [Google Scholar]
  23. Tracy R. L., Stern D. B. Mitochondrial transcription initiation: promoter structures and RNA polymerases. Curr Genet. 1995 Aug;28(3):205–216. doi: 10.1007/BF00309779. [DOI] [PubMed] [Google Scholar]
  24. Vera A., Hirose T., Sugiura M. A ribosomal protein gene (rpl32) from tobacco chloroplast DNA is transcribed from alternative promoters: similarities in promoter region organization in plastid housekeeping genes. Mol Gen Genet. 1996 Jul 19;251(5):518–525. doi: 10.1007/BF02173640. [DOI] [PubMed] [Google Scholar]
  25. Vera A., Sugiura M. Chloroplast rRNA transcription from structurally different tandem promoters: an additional novel-type promoter. Curr Genet. 1995 Feb;27(3):280–284. doi: 10.1007/BF00326161. [DOI] [PubMed] [Google Scholar]
  26. Vera A., Sugiura M. Combination of in vitro capping and ribonuclease protection improves the detection of transcription start sites in chloroplasts. Plant Mol Biol. 1992 May;19(2):309–311. doi: 10.1007/BF00027352. [DOI] [PubMed] [Google Scholar]
  27. Wolfe K. H. Similarity between putative ATP-binding sites in land plant plastid ORF2280 proteins and the FtsH/CDC48 family of ATPases. Curr Genet. 1994 Apr;25(4):379–383. doi: 10.1007/BF00351493. [DOI] [PubMed] [Google Scholar]

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