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Active transcription from a promoter positioned within the coding region of a divergently oriented gene: the tobacco chloroplastrp132 gene

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Summary

A new transcription unit has been identified and characterized in the small single-copy region of tobacco chloroplast DNA. A primary transcript (1550 nucleotides) spanning the entire transcription unit contains no significant open reading frames (ORFs), other than ORF55, recently identified as the gene encoding the ribosomal protein CL32 (rp132). The leader sequence extends 1101 nucleotides from therp132 initiation codon. Primer extension and in vitro capping experiments in combination with ribonuclease protection assays, revealed a promoter situated more than 322 by inside the coding region ofndhF, which is divergently oriented with respect torp132. A canonical Pribnow-box is found just upstream of the transcription start site, but a typical −35 motif was not detected. This is the first internal divergent promoter to be characterized in the chloroplast genome.

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References

  • Beck CF, Warren RAJ (1988) Divergent promoters, a common form of gene organization. Microbiol Rev 52:318–326

    Google Scholar 

  • Benny G, Boyen A, Charlier D, Lissens W, Feller A, Glansdorff N (1982) Promoter mapping and selection of operator mutants by using insertion by bacteriophage Mu in theargECBH divergent operon ofEscherichia coli K-12. J Bacteriol 151:62–67

    Google Scholar 

  • Berends T, Gamble PE, Mullet JE (1987) Characterization of the barley chloroplast transcription units containingpsaA-psaB psbD-psbC. Nucleic Acids Res 15:5217–5240

    Google Scholar 

  • Citron M, Schuster H (1990) The c4 repressors of bacteriophages P1 and P7 are antisense RNAs. Cell 62:591–598

    Google Scholar 

  • Haley J, Bogorad L (1990) Alternative promoters are used for genes within maize chloroplast polycistronic transcription units. Plant Cell 2:323–333

    Google Scholar 

  • Hanley-Bowdoin L, Chua NH (1987) Chloroplast promoters. Trends Biochem Sci 12:67–70

    Google Scholar 

  • Kapler GM, Zhang K, Beverley SM (1990) Nuclease mapping and DNA sequence analysis of transcripts from the dihydrofolate reductase-thymidylate synthase (R) region ofLeishmania major. Nucleic Acids Res 18:6399–6408

    Google Scholar 

  • Kennell JC, Pring DR (1989) Initiation and processing ofatp6, T-urf13 andORF221 transcripts from mitochondria of T cytoplasm maize. Mol Gen Genet 216:16–24

    Google Scholar 

  • Kohchi T, Yoshida T, Komano T, Ohyama K (1988) Divergent mRNA transcription in thepsbB operon. EMBO J 7:885–891

    Google Scholar 

  • Li Y, Sugiura M (1990) Three distinct ribonucleoproteins from tobacco chloroplast: each contains a unique aminoterminal acidic domain and two ribonucleoprotein consensus motifs. EMBO J 9:3059–3066

    Google Scholar 

  • Mache R (1990) Chloroplast ribosomal proteins and their genes. Plant Sci 72:1–12

    Google Scholar 

  • Matsubayashi T, Wakasugi T, Shinozaki K, Shinozaki KY, Zaita N, Hidaka T, Meng BY, Ohto C, Tanaka M, Kato A, Maruyama T, Sugiura M (1987) Six chloroplast genes homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of the spliced sites inndhA andndhB premRNAs. Mol Gen Genet 210:385–393

    Google Scholar 

  • Meng BY, Wakasugi T, Sugiura M (1991) Two promoters within thepsbK psbI-trnG gene cluster in tobacco chloroplast DNA. Curr Genet 20:259–264

    Google Scholar 

  • Neuhaus H, Scholz A, Link G (1989) Structure and expression of a split chloroplast gene from mustard (Sinapis alba): ribosomal protein generps16 reveals unusual transcription features and complex RNA maturation. Curr Genet 15:63–70

    Google Scholar 

  • Nomura T, Aiba H, Ishihama A (1985) Transcriptional organization of the convergent overlappingdnaQ-rnh genes ofEscherichia coli. J Biol Chem 260:7122–7125

    Google Scholar 

  • Ohto C, Torazawa K, Tanaka M, Shinozaki K, Sugiura M (1988) Transcription of ten ribosomal proteins from tobacco chloroplasts: a compilation of ribosomal protein genes found in the tobacco chloroplast genome. Plant Mol Biol 11:589–600

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Schwarz Z, Jolly SO, Steinmetz AA, Bogorad L (1981) Overlapping divergent genes in the maize chloroplast chromosome and in vitro transcription of the gene for tRNAHIs. Proc Natl Acad Sci USA 78:3423–3427

    Google Scholar 

  • Sexton TB, Christopher DA, Mullet JE (1990a) Light-induced switch in barleypsbD-psbC promoter utilization: a novel mechanism regulating chloroplast gene expression. EMBO J 9:4485–4494

    Google Scholar 

  • Sexton TB, Jones JT, Mullet JE (1990b) Sequence and transcriptional analysis of the barley ctDNA region upstream ofpsbD-psbC encodingtrnK (UUU),rps16, trnQ (UUG),psbK, psbI andtrnS (GCU). Curr Genet 17:445–454

    Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Shinozaki KY, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

    Google Scholar 

  • Simons RW, Kleckner N (1988) Biological regulation by antisense RNA in prokaryotes. Annu Rev Genet 22:567–600

    Google Scholar 

  • Sugiura M (1989) The chloroplast chromosomes in land plants. Annu Rev Cell Biol 5:51–70

    Google Scholar 

  • Sugiura M, Shinozaki K, Zaita N, Kusuda M, Kumano M (1986) Clone bank of the tobacco (Nicotiana tabacum) chloroplast genome as a set of overlapping restriction fragments: mapping of eleven ribosomal protein genes. Plant Sci 44:211–216

    Google Scholar 

  • Sugiura M, Torazawa K, Wakasugi T (1991) Chloroplast genes coding for ribosomal protein genes in land plants. In: Mache R, Stutz E, Subramanian AR (eds) The translational apparatus of photosynthetic organelles. Springer Verlag, Berlin, pp 59–69

    Google Scholar 

  • Thompson-Jaeger S, Domdey H (1990) The intron of the yeast actin gene contains the promoter for an antisense RNA. Curr Genet 17:269–273

    Google Scholar 

  • Vera A, Sugiura M (1992) Combination ofin vitro capping and ribonuclease protection improves the detection of transcription start sites in chloroplasts. Plant Mot Biol (in press)

  • Weil JH (1987) Organization and expression of the chloroplast genome. Plant Sci 49:149–157

    Google Scholar 

  • Wu J, Weiss B (1991) Two divergently transcribed genes,soxR andsoxS, control a superoxide response regulon ofEscherichia coli. J Bacteriol 173:2864–2871

    Google Scholar 

  • Yao WB, Meng BY, Tanaka M, Sugiura M (1989) An additional promoter within the protein-coding region of thepsbD -psbC gene cluster in tobacco chloroplast DNA. Nucleic Acids Res 17:9583–9591

    Google Scholar 

  • Yokoi F, Vassileva A, Hayashida N, Torazawa K, Wakasugi T, Sugiura M (1990) Chloroplast ribosomal protein L32 is encoded in the chloroplast genome. FEBS Lett 276:88–90

    Google Scholar 

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Communicated by R.G. Herrmann

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Vera, A., Matsubayashi, T. & Sugiura, M. Active transcription from a promoter positioned within the coding region of a divergently oriented gene: the tobacco chloroplastrp132 gene. Molec. Gen. Genet. 233, 151–156 (1992). https://doi.org/10.1007/BF00587573

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