Abstract
Identification of transcription initiation sites in the promoter region of the tobacco chloroplast rRNA operon has been carried out by ribonuclease protection of in vitro capped RNAs and primer extension experiments. A promoter with typical chloroplast-10 and-35 motifs (P1) drives initiation of transcription from position-116 relative to the mature 16s rRNA sequence. In addition, we have found that a second primary transcript starts at position-64. This proximal promoter (P2) lacks any elements similar to those reported so far in chloroplast promoter regions, and hence P2 represents a novel-type promoter. Both transcripts are present in chloroplasts from green leaves and in non-photosynthetic proplastids from heterotrophically cultured cells (BY2), but their relative amounts appear to differ. The steady state level of the P2 transcript, with respect to P1, is higher in BY2 proplastids than in leaf chloroplasts.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Baeza L, Bertrand A, Mache R, Lerbs-Mache S (1991) Characterization of a protein-binding sequence in the promoter region of the 16s rRNA gene of the spinach chloroplast genome. Nucleic Acids Res 13:3577–3581
Berends-Sexton T, Christopher DA, Mullet JE (1990) Light-induced switch in barley psbD-psbC promoter utilization: a novel mechanism regulating chloroplast gene expression. EMBO J 9: 4485–4494
Briat JF, Dron M, Loiseaux S, Mache R (1982) Structure and transcription of the spinach chloroplast rDNA leader region. Nucleic Acids Res 10:6865–6878
Christopher DA, Kim M, Mullet JE (1992) A novel light-regulated promoter is conserved in cereal and dicot chloroplasts. Plant Cell 4:785–798
Delp G, Kössel H (1991) rRNAs and rRNA genes of plastids. In: Bogorad L, Vasil IK (eds) The molecular biology of plastids. Academic press, San Diego, pp 139–167
De Vries S, Hogé H, Bisseling T (1988) Isolation of polysomal RNA from plant tissues. In: Gelvin SB, Schilperoot RA, Verma DPS (eds) Plant molecular biology manual. Kluwer Academic Publishers, Dordrecht, The Netherlands, B6:1–13
Gegenheimer P, Apirion A (1981) Processing of prokaryotic ribonucleic acid. Microbiol Rev 45:502–541
Gruissem W, Tonkyn JC (1993) Control mechanisms of plastid gene expression. Crit Rev Plant Sci 12:19–55
Haley J, Bogorad L (1990) Alternative promoters are used for genes within maize chloroplast polycistronic transcription units. Plant Cell 2:323–333
Hess WR, Prombona A, Fieder B, Subramanian AR, Börner T (1993) 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 12:563–571
Hiratsuka J, Shimada H, Whittier RF, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li Y, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: Intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194
Igloi GL, Kössel H (1992) The transcriptional apparatus of chloroplasts. Crit Rev Plant Sci 10:525–558
Kapoor S, Wakasugi T, Deno H, Sugiura M (1994) An atpE-specific promoter within the coding region of atpB gene in tobacco chloroplast DNA. Cur Genet 26:263–268
Keuss RJA, Dekker AF, Van Roon MA, Groot GSP (1983) The nucleotide sequences of the regions flanking the genes coding for 23s, 16s and 4.5s ribosomal RNA on chloroplast DNA from Spirodela oligorhiza. Nucleic Acids Res 11:6465–6474
Lerbs-Mache S (1993) 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 USA 90:5509–5513
Mache R (1990) Chloroplast ribosomal proteins and their genes. Plant Sci 72:1–12
Meng BY, Wakasugi T, Sugiura M (1991) Two promoters within the psbK-psbI-trnG gene cluster in tobacco chloroplast DNA. Curr Genet 20:259–264
Neuhaus H, Scholz A, Link G (1989) Structure and expression of a split chloroplast gene from mustard (Sinapis alba): ribosomal protein gene rps16 reveals unusual transcription features and complex RNA maturation. Curr Genet 15:63–70
Przybyl E, Fritzsche E, Edwards K, Kössel H, Falk H, Thompson JA, Link G (1984) The ribosomal RNA genes from chloroplasts of mustard (Sinapis alba L.): mapping and sequencing of the leader sequence. Plant Mol Biol 3:147–158
Rochaix JD (1992) Post-transcriptional steps in the expression of chloroplast genes. Annu Rev Cell Biol 8:1–28
Schwarz Z, Kössel H, Schwarz E, Bogorad L (1981) A gene coding for tRNAval is located near the 5′ terminus of the 16s rRNA gene in Zea mays chloroplast genome. Proc Natl Acad Sci USA 78:4748–4752
Shapiro DR, Tewari KK (1986) Nucleotide sequences of transfer RNA genes in the Pisum sativum chloroplast DNA. Plant Mol Biol 6:1–12
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
Srivastava AK, Schlessinger D (1990) rRNA processing in Escherichia coli. In: Hill WE, Dahlberg A, Garret RA, Moore PB, Schlessinger D, Warner JR (eds) The ribosome. Structure, function and evolution. Am Soc Microbiol, Washington, DC, pp 426–434
Strittmatter G, Gozdzicka-Jozefiak A, Kössel H (1985) Identification of an rRNA promoter from Zea mays chloroplasts which excludes the proximal tRNAvalGAC from the primary transcript. EMBO J 4:599–604
Subramanian AR, Stahl D, Prombona A (1991) In: Bogorad L, Vasil IK (eds) The molecular biology of the plastids. Academic press, San Diego, pp 191–215
Sugiura M (1989) The chloroplast chromosomes in land plants. Annu Rev Cell Biol 5:51–70
Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168
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
Tiller K, Link G (1993) Phosphorylation and dephosphorylation affect functional characteristics of chloroplast and etioplast transcription systems from mustard (Sinapis alba). EMBO J 12:1745–1753
Tohdoh N, Sugiura M (1982) The complete nucleotide sequence of a 16s ribosomal RNA gene from tobacco chloroplasts. Gene 17:213–218
Tohdoh N, Shinozaki K, Sugiura M (1981) Sequence of a putative promoter region for the rRNA genes of tobacco chloroplast DNA. Nucleic Acids Res 9:5399–5406
Vera A, Sugiura M (1992) Combination of in vitro capping and ribonuclease protection improves the detection of transcription start sites in chloroplasts. Plant Mol Biol 19:309–311
Vera A, Sugiura M (1994) A novel RNA gene in the tobacco plastid genome: its possible role in the maturation of 16s rRNA. EMBO J 13:2211–2217
Vera A, Matsubayashi T, Sugiura M (1992) Active transcription from a promoter positioned within the coding region of a divergently oriented gene: the tobacco chloroplast rpl32 gene. Mol Gen Genet 233:151–156
Vera A, Yokoi F, Sugiura M (1993) The existence of pre-mature 16s rRNA species in plastid ribosomes. FEBS Lett 327:29–31
Von Allmen JM, Stutz E (1988) The soybean chloroplast genome: nucleotide sequence of a region containing tRNA-Val(GAC) and 16s rRNA gene. Nucleic Acids Res 16:1200
Weil JH (1987) Organization and expression of the chloroplast genome. Plant Sci 49:149–157
Wolfe KH, Katz-Downie DS, Morden CW, Palmer JD (1992) Evolution of the plastid ribosomal RNA operon in a nongreen parasitic plant: accelerated sequence evolution, altered promoter structure, and tRNA pseudogenes. Plant Mol Biol 18:1037–1048
Yao WB, Meng BY, Tanaka M, Sugiura M (1989) An additional promoter within the protein-coding region of the psbD-psbC gene cluster in tobacco chloroplast DNA. Nucleic Acids Res 17:9583–9591
Yasuda T, Kuroiwa T, Nagata T (1988) Preferential synthesis of plastid DNA and increased replication of plastids in cultured tobacco cells following medium renewal. Planta 174:235–241
Author information
Authors and Affiliations
Additional information
Communicated by H. Kössel
Rights and permissions
About this article
Cite this article
Vera, A., Sugiura, M. Chloroplast rRNA transcription from structurally different tandem promoters: an additional novel-type promoter. Curr Genet 27, 280–284 (1995). https://doi.org/10.1007/BF00326161
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00326161