Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1996 Jun 3;15(11):2802–2809.

Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants.

L A Allison 1, L D Simon 1, P Maliga 1
PMCID: PMC450217  PMID: 8654377

Abstract

The plastid genome in higher plants encodes subunits of an Escherichia coli-like RNA polymerase which initiates transcription of plastid genes from sequences resembling E.coli sigma70-type promoters. By deleting the gene for the essential beta subunit of the tobacco E.coli-like RNA polymerase, we have established the existence of a second plastid transcription system which does not utilize E.coli-like promoters. In contrast to the E.coli-like RNA polymerase, the novel transcription machinery preferentially transcribes genetic system genes rather than photosynthetic genes. Although the mutant plants are photosynthetically defective, transcription by this polymerase is sufficient for plastid maintenance and plant development.

Full text

PDF
2803

Images in this article

2803Image
on p.2803
2804Image
on p.2804
2805Image
on p.2805
2805Image
on p.2805
2806Image
on p.2806
2806Image
on p.2806

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  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. Baeza L., Bertrand A., Mache R., Lerbs-Mache S. Characterization of a protein binding sequence in the promoter region of the 16S rRNA gene of the spinach chloroplast genome. Nucleic Acids Res. 1991 Jul 11;19(13):3577–3581. doi: 10.1093/nar/19.13.3577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baldauf S. L., Palmer J. D. Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature. 1990 Mar 15;344(6263):262–265. doi: 10.1038/344262a0. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Christopher D. A., Kim M., Mullet J. E. A novel light-regulated promoter is conserved in cereal and dicot chloroplasts. Plant Cell. 1992 Jul;4(7):785–798. doi: 10.1105/tpc.4.7.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gantt J. S., Baldauf S. L., Calie P. J., Weeden N. F., Palmer J. D. Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J. 1991 Oct;10(10):3073–3078. doi: 10.1002/j.1460-2075.1991.tb07859.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Glass R. E., Jones S. T., Nene V., Nomura T., Fujita N., Ishihama A. Genetic studies on the beta subunit of Escherichia coli RNA polymerase. VIII. Localisation of a region involved in promoter selectivity. Mol Gen Genet. 1986 Jun;203(3):487–491. doi: 10.1007/BF00422074. [DOI] [PubMed] [Google Scholar]
  8. Gruissem W., Elsner-Menzel C., Latshaw S., Narita J. O., Schaffer M. A., Zurawski G. A subpopulation of spinach chloroplast tRNA genes does not require upstream promoter elements for transcription. Nucleic Acids Res. 1986 Oct 10;14(19):7541–7556. doi: 10.1093/nar/14.19.7541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hanley-Bowdoin L., Orozco E. M., Jr, Chua N. H. In vitro synthesis and processing of a maize chloroplast transcript encoded by the ribulose 1,5-bisphosphate carboxylase large subunit gene. Mol Cell Biol. 1985 Oct;5(10):2733–2745. doi: 10.1128/mcb.5.10.2733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hess W. R., Hoch B., Zeltz P., Hübschmann T., Kössel H., Börner T. Inefficient rpl2 splicing in barley mutants with ribosome-deficient plastids. Plant Cell. 1994 Oct;6(10):1455–1465. doi: 10.1105/tpc.6.10.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. 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]
  14. Klein U., De Camp J. D., Bogorad L. Two types of chloroplast gene promoters in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3453–3457. doi: 10.1073/pnas.89.8.3453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Klein U., Salvador M. L., Bogorad L. Activity of the Chlamydomonas chloroplast rbcL gene promoter is enhanced by a remote sequence element. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10819–10823. doi: 10.1073/pnas.91.23.10819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Little M. C., Hallick R. B. Chloroplast rpoA, rpoB, and rpoC genes specify at least three components of a chloroplast DNA-dependent RNA polymerase active in tRNA and mRNA transcription. J Biol Chem. 1988 Oct 5;263(28):14302–14307. [PubMed] [Google Scholar]
  18. Morden C. W., Wolfe K. H., dePamphilis C. W., Palmer J. D. Plastid translation and transcription genes in a non-photosynthetic plant: intact, missing and pseudo genes. EMBO J. 1991 Nov;10(11):3281–3288. doi: 10.1002/j.1460-2075.1991.tb04892.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Nakazono M., Hirai A. Identification of the entire set of transferred chloroplast DNA sequences in the mitochondrial genome of rice. Mol Gen Genet. 1993 Jan;236(2-3):341–346. doi: 10.1007/BF00277131. [DOI] [PubMed] [Google Scholar]
  21. Neuhaus H., Scholz A., Link G. Structure and expression of a split chloroplast gene from mustard (Sinapis alba): ribosomal protein gene rps16 reveals unusual transcriptional features and complex RNA maturation. Curr Genet. 1989 Jan;15(1):63–70. doi: 10.1007/BF00445753. [DOI] [PubMed] [Google Scholar]
  22. Pfannschmidt T., Link G. Separation of two classes of plastid DNA-dependent RNA polymerases that are differentially expressed in mustard (Sinapis alba L.) seedlings. Plant Mol Biol. 1994 Apr;25(1):69–81. doi: 10.1007/BF00024199. [DOI] [PubMed] [Google Scholar]
  23. Poethig S. Genetic mosaics and cell lineage analysis in plants. Trends Genet. 1989 Aug;5(8):273–277. doi: 10.1016/0168-9525(89)90101-7. [DOI] [PubMed] [Google Scholar]
  24. Reinbothe S., Reinbothe C., Heintzen C., Seidenbecher C., Parthier B. A methyl jasmonate-induced shift in the length of the 5' untranslated region impairs translation of the plastid rbcL transcript in barley. EMBO J. 1993 Apr;12(4):1505–1512. doi: 10.1002/j.1460-2075.1993.tb05794.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rochaix J. D. Chlamydomonas reinhardtii as the photosynthetic yeast. Annu Rev Genet. 1995;29:209–230. doi: 10.1146/annurev.ge.29.120195.001233. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Shinozaki K., Sugiura M. The nucleotide sequence of the tobacco chloroplast gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Gene. 1982 Nov;20(1):91–102. doi: 10.1016/0378-1119(82)90090-7. [DOI] [PubMed] [Google Scholar]
  28. Staub J. M., Maliga P. Translation of psbA mRNA is regulated by light via the 5'-untranslated region in tobacco plastids. Plant J. 1994 Oct;6(4):547–553. doi: 10.1046/j.1365-313x.1994.6040547.x. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Svab Z., Hajdukiewicz P., Maliga P. Stable transformation of plastids in higher plants. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8526–8530. doi: 10.1073/pnas.87.21.8526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Svab Z., Maliga P. High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):913–917. doi: 10.1073/pnas.90.3.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Yao W. B., Meng B. Y., Tanaka M., Sugiura M. An additional promoter within the protein-coding region of the psbD-psbC gene cluster in tobacco chloroplast DNA. Nucleic Acids Res. 1989 Dec 11;17(23):9583–9591. doi: 10.1093/nar/17.23.9583. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES