Skip to main content
SpringerLink
Log in

Sequence studies on the soybean chloroplast 16S–23S rDNA spacer region

Comparison with other angiosperm sequences and proposal of a generalized RNA secondary structure model for the intergenic regions

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The sequence of the ribosomal spacer region of soybean chloroplast DNA including the 3′ end of the 16S rRNA gene, the tRNAAla and tRNAIle genes (but not their introns), the three intergenic regions and the 5′ end of the 23S rRNA gene, has been determined. This sequence has been compared to corresponding regions of other angiosperm chloroplast DNAs. Secondary structure models are proposed for the entirety of the intergenic regions a, b and c and for the flanking rRNA regions. A model for a common secondary structure of the ribosomal spacer intergenic regions from chloroplasts of higher plants is proposed, which is supported by comparative evidence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Avril JF: DEA Informatique. Université Paris VI (1985).

  2. Bohnert HJ, Crouse EJ, Schmitt JM: Organization and expression of plastid genomes. Encycl Plant Physiol 14B: 475–530 (1982).

    Google Scholar 

  3. Bram RJ, Young RA, Steitz JA: The ribonuclease III site flanking 23S sequences in the 30S ribosomal precursor RNA ofE. coli. Cell 19: 393–401 (1980).

    Google Scholar 

  4. Crouse EJ, Schmitt JM, Bohnert HJ: Chloroplast and cyanobacterial genomes, genes and RNAs: a compilation. Plant Mol Biol Reporter 3: 43–89 (1985).

    Google Scholar 

  5. Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12: 387–395 (1984).

    Google Scholar 

  6. Edwards K, Bedbrook J, Dyer T, Kössel H: 4.5S rRNA fromZea mays chloroplasts shows structural homology with the 3′ end of prokaryotic 23S rRNA. Biochem Int 2: 533–538 (1981).

    Google Scholar 

  7. Edwards K, Kössel H: The rRNA operon fromZea mays chloroplast: nucleotide sequence of 23S rDNA and its homology withE. coli 23S rDNA. Nucleic Acids Res 9: 2853–2869 (1981).

    Google Scholar 

  8. Fox EF, Woese CR: 5S RNA secondary structure. Nature 256: 505–507 (1975).

    Google Scholar 

  9. Glotz C, Zwieb C, Brimacombe R: Secondary structure of the large subunit ribosomal RNA fromEscherichia coli, Zea mays chloroplast, and human and mouse mitochondrial ribosomes. Nucleic Acids Res 9: 3287–3306 (1981).

    Google Scholar 

  10. Guillemaut P, Weil JH: The nucleotide sequence of the maize and spinach chloroplast isoleucine transfer RNA encoded in the 16S to 23S rDNA spacer. Nucleic Acids Res 10: 1653–1659 (1982).

    Google Scholar 

  11. Graf L, Roux E, Stutz E: Nucleotide sequence of aEuglena gracilis chloroplast gene coding for the 16S rRNA: homologies toE. coli andZea mays chloroplast 16S rRNA. Nucleic Acids Res 10: 6369–6381 (1982).

    Google Scholar 

  12. Jacq B: Sequence homologies between eukaryotic 5.8S rRNA and the 5′ end of prokaryotic 23S rRNA: evidences for a common evolutionary origin. Nucleic Acids Res 9: 2913–2932 (1981).

    Google Scholar 

  13. Jarsch M, Böck A: Sequence of the 23S rRNA gene from the archaebacteriumMethanococcus vannielii: evolutionary and functional implications. Mol Gen Genet 200: 305–312 (1985).

    Google Scholar 

  14. Keus RJA, Dekker AF, vanRoon MA, Groot GSP: The nucleotide sequence of the regions flanking the genes coding for 23S, 16S and 4.5S ribosomal RNA on chloroplast DNA fromSpirodela oligorhiza. Nucleic Acids Res 11: 6465–6474 (1983).

    Google Scholar 

  15. Koch W, Edwards K, Kössel H: Sequencing of the 16S–23S spacer in a ribosomal RNA operon ofZea mays chloroplast DNA reveals two split tRNA genes. Cell 25: 203–213 (1981).

    Google Scholar 

  16. Kumano M, Tomioka N, Sugiura M: The complete nucleotide sequence of a 23S rRNA gene from a blue-green alga,Anacystis nidulans. Gene 24: 219–225 (1983).

    Google Scholar 

  17. Loughney K, Lund E, Dahlberg JE: tRNA genes are found between the 16S and 23S rRNA genes inBacillus subtilis. Nucleic Acids Res 10: 1607–1624 (1982).

    Google Scholar 

  18. MacKay RM: The origin of plant chloroplast 4.5S ribosomal RNA. FEBS Lett 123: 17–18 (1981).

    Google Scholar 

  19. Malthiery B, Bellon B, Giorgi D, Jacq B: Apple II Pascal programs for molecular biologists. Nucleic Acids Res 12: 569–579 (1984).

    Google Scholar 

  20. Maly P, Brimacombe R: Refined secondary structure models for the 16S and 23S ribosomal RNA ofEscherichia coli. Nucleic Acids Res 11: 7263–7286 (1983).

    Google Scholar 

  21. Mankin AS, Kagramanova VK: Complete nucleotide sequence of the single ribosomal operon ofHalobacterium halobium: secondary structure of the archaebacterial 23S rRNA. Mol Gen Genet 202: 152–161 (1986).

    Google Scholar 

  22. Maxam AM, Gilbert W: Sequencing end-labelled DNA with base specific chemical cleavages. In: Grossman L, Moldave K (eds) Methods in Enzymology, Vol. 65. Academic Press, New York (1980) pp 499–560.

    Google Scholar 

  23. Michel F, Dujon B: Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast- and nuclear-encoded members. EMBO J 2: 33–38 (1983).

    Google Scholar 

  24. Michot B, Bachellerie JP, Raynal F: Structure of mouse rRNA precursors. Complete sequence and potential folding of the spacer regions between 18S and 28S rRNA. Nucleic Acids Res 11: 3375–3391 (1983).

    Google Scholar 

  25. Michot B, Hassouna N, Bachellerie JP: Secondary structure of mouse 28S rRNA and general model for the folding of the large rRNA in eukaryotes. Nucleic Acids Res 12: 4259–4279 (1984).

    Google Scholar 

  26. Nazar RN: A 5.8S rRNA-like sequence in prokaryotic 23S rRNA. FEBS Lett 119: 212–214 (1980).

    Google Scholar 

  27. Nelles L, Fang BL, Volckaert G, Vandenberghe A, DeWachter R: Nucleotide sequence of a crustacean 18S ribosomal RNA gene and secondary structure of eukaryotic small subunit ribosomal RNAs. Nucleic Acids Res 12: 8749–8768 (1984).

    Google Scholar 

  28. Noller HF: Structure of ribosomal RNA. Ann Rev Biochem 53: 119–162 (1984).

    Google Scholar 

  29. Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeushi M, Chang Z, Aota SI, Inokuchi H, Ozeki H: Chloroplast gene organisation deduced from complete sequence of liverwortMarchantia polymorpha chloroplast DNA. Nature 322: 572–574 (1986).

    Google Scholar 

  30. Orozco EM Jr, Rushlow KE, Dodd JR, Hallick RB:Euglena gracilis chloroplast ribosomal RNA transcription units: II. Nucleotide sequence homology between the 16S–23S ribosomal spacer and the 16S ribosomal RNA leader regions. J Biol Chem 255: 10997–11003 (1980).

    Google Scholar 

  31. Palmer JD: Comparative organization of chloroplast genomes. Ann Rev Genet 19: 325–354 (1985).

    Google Scholar 

  32. Pillay DTN, Singh GP, deLanversin G: Structural organisation of soybean (Glycine max) plastid genome. In: Reddy GM, Coe EH Jr (eds) Gene Structure and Function in Higher Plants. Oxford and IBH Publishing Co, New Delhi (1983) pp 213–221.

    Google Scholar 

  33. Rochaix JD, Darlix JL: Composite structure of the chloroplast 23S ribosomal RNA genes ofChlamydomonas reinhardii. Evolutionary and functional implications. J Mol Biol 159: 383–395 (1982).

    Google Scholar 

  34. Schneider M, Rochaix JD: Sequence organisation of the chloroplast ribosomal spacer ofChlamydomonas reinhardii: uninterrupted tRNAIle and tRNAAla genes and extensive secondary structure. Plant Mol Biol 6: 265–270 (1986).

    Google Scholar 

  35. Schwarz Z, Kössel H: The primary structure of 16S rDNA fromZea mays chloroplast is homologous toE. coli 16S rRNA. Nature 283: 739–742 (1980).

    Google Scholar 

  36. Schwarz Z, Kössel H, Schwarz E, Bogorad L: A gene coding for tRNAVal is located near 5′ terminus of 16S rRNA gene inZea mays chloroplast genome. Proc Natl Acad Sci USA 78: 4748–4752 (1981).

    Google Scholar 

  37. Shine J, Dalgarno L: The 3′-terminal sequence ofEscherichia coli 16S ribosomal RNA: Complementarity of nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71: 1342–1346 (1974).

    Google Scholar 

  38. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, 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: The complete nucleotide sequence of the tobacco chloroplast genome: its gene organisation and expression. EMBO J 5: 2043–2049 (1986).

    Google Scholar 

  39. Singh G, de Lanversin G, Straus NA, Pillay DTN: Characterization of soybean chloroplast ribosomal genes. Curr Genet 9: 99–105 (1984).

    Google Scholar 

  40. Stiegler P, Carbon P, Ebel JP, Ehresmann C: A general secondary-structure model for procaryotic and eucaryotic RNAs of the small ribosomal subunits. Eur J Biochem 120: 487–495 (1981).

    Google Scholar 

  41. Smith TF, Waterman MS: Identification of common molecular subsequences. J Mol Biol 147: 195–197 (1981).

    Google Scholar 

  42. Takaiwa F, Sugiura M: Nucleotide sequence of the 16S–23S spacer region in an rRNA gene cluster from tobacco chloroplast DNA. Nucleic Acids Res 10: 2665–2676 (1982).

    Google Scholar 

  43. Takaiwa F, Sugiura M: The complete nucleotide sequence of a 23S rRNA gene from tobacco chloroplasts. Eur J Biochem 124: 13–19 (1982).

    Google Scholar 

  44. Tinocco I Jr, Uhlenbeck OC, Levine MD: Estimation of secondary structure in ribonucleic acids. Nature 230: 362–367 (1971).

    Google Scholar 

  45. Tohdoh N, Sugiura M: The complete nucleotide sequence of a 16S ribosomal RNA gene from tobacco chloroplasts. Gene 17: 213–218 (1982).

    Google Scholar 

  46. Tohdoh N, Shinozaki K, Sugiura M: Sequence of a putative promoter region for the rRNA genes of tobacco chloroplast DNA. Nucleic Acids Res 9: 5399–5406 (1981).

    Google Scholar 

  47. Tomioka N, Sugiura M: Nucleotide sequence of the 16S–23S spacer region in therrnA operon from a blue-green alga,Anacystis nidulans. Mol Gen Genet 193: 427–430 (1984).

    Google Scholar 

  48. Veldman GM, Klootwijk J, DeRegt VCHF, Planta RJ, Branlant C, Krol A, Ebel JP: The primary and secondary structure of yeast 26S rRNA. Nucleic Acids Res 9: 6935–6958 (1981).

    Google Scholar 

  49. Whitfeld PR, Bottomley W: Organization and structure of chloroplast genes. Ann Rev Plant Physiol 34: 279–310 (1983).

    Google Scholar 

  50. Williamson SE, Doolittle WF: Genes for tRNAIle and tRNAAla in the spacer between the 16S and 23S rRNA genes of a blue-green alga; strong homology to chloroplast tRNA genes and tRNA genes of theE. coli rrnD cluster. Nucleic Acids Res 11: 225–235 (1983).

    Google Scholar 

  51. Yamada T, Shimaji M: Peculiar feature of the organization of rRNA genes of theChlorella chloroplast DNA. Nucleic Acids Res 14: 3827–3839 (1986).

    Google Scholar 

  52. Young RA, Macklis R, Steitz JA: Sequence of the 16S–23S spacer region in two ribosomal RNA operons ofEscherichia coli. J Biol Chem 254: 3264–3271 (1979).

    Google Scholar 

  53. Young RA, Steitz JA: Complementary sequences 1700 nucleotides apart from a ribonuclease III cleavage site inEscherichia coli ribosomal precursor RNA. Proc Natl Acad Sci USA 75: 3593–3597 (1978).

    Google Scholar 

  54. Zucker M, Stiegler P: Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res 9: 133–148 (1981).

    Google Scholar 

Download references

Author information

Author notes

  1. Guy de Lanversin

    Present address: Laboratoire de Génétique et Biologie Cellulaires, C.N.R.S., Centre Universitaire de Luminy, F-13288, Marseille Cedex 9, France

Authors and Affiliations

  1. Department of Biology, University of Windsor, N9B 3P4, Windsor, Ontario, Canada

    Guy de Lanversin & Data T. N. Pillay

  2. Laboratoire de Génétique et Biologie Cellulaires, C.N.R.S., Centre Universitaire de Luminy, F-13288, Marseille Cedex 9, France

    Bernard Jacq

Authors
  1. Guy de Lanversin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Data T. N. Pillay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bernard Jacq
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Lanversin, G., Pillay, D.T.N. & Jacq, B. Sequence studies on the soybean chloroplast 16S–23S rDNA spacer region. Plant Mol Biol 10, 65–82 (1987). https://doi.org/10.1007/BF00014187

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00014187

Key words

Search

Navigation