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Secondary structure and phylogeny of the chloroplast 23S rRNA gene from the brown alga Pylaiella littoralis

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Abstract

The entire nucleotide sequence of a 23S rRNA gene from the brown alga Pylaiella littoralis (L.) Kjellm has been determined. The predicted length of the 23S rRNA is 2948 nucleotides, including the 4.5S rRNA-like region at the 3′ end of the molecule. The putative transcript has been folded into a secondary structure by comparison to existing structure models, and the predicted helical regions were inspected by identifying compensatory downstream base changes. The 23S rRNA secondary structure presented here has features that are unique to P. littoralis (no other chromophyte or red algal 23S rRNA sequences are yet available), but has none of the features specific to the chloroplast rRNAs of green plants and green algae. The Pylaiella sequence was aligned with analogous plastidial and eubacterial gene sequences, and the alignment was used to construct a phylogenetic tree. The plastidial sequences formed a coherent cluster closely associated with the 23S rRNA of the cyanobacterium Anacystis nidulans. Within the plastid group, the P. littoralis sequence was most closely related to that of Euglena gracilis confirming earlier analyses based upon 16S rRNA sequences.

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References

  1. Assali NE, Mache R, Loiseaux-de Goër S: Evidence for a composite phylogenetic origin of the plastid genome of the brown alga Pylaiella littoralis (L) Kjellm. Plant Mol Biol 15: 307–315 (1990).

    PubMed  Google Scholar 

  2. Assali NE, Martin WF, Somerville CC, Loiseaux-de Goër S: Evolution of the Rubisco operon from prokaryotes to algae: structure and analysis of the rbcS gene of the brown alga Pylaiella littoralis. Plant Mol Biol 17: 853–863 (1991).

    PubMed  Google Scholar 

  3. Assali NE, Loiseaux-de Goër S: Sequence and phylogeny of the psaB gene of the brown alga Pylaiella littoralis. J Phycol 28: 209–213 (1992).

    Article  Google Scholar 

  4. Boczar BA, Delaney TP, Cattolico RA: Gene for the ribulose-1,5-bisphosphate carboxylase small subunit protein of the marine chromophyte Olisthodiscus luteus is similar to that of a chemoautotrophic bacterium. Proc Natl Acad Sci USA 86: 4996–4999 (1989).

    PubMed  Google Scholar 

  5. Brosius J, Dull TS, Noller HF: Complete nucleotide sequence of a 23S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 77: 201–204 (1980).

    PubMed  Google Scholar 

  6. Dalmon J, Loiseaux S, Bazetoux S: Heterogeneity of plastid DNA of two species of brown algae. Plant Sci Lett 29: 243–253 (1983).

    Google Scholar 

  7. Douglas SE, Doolittle WF: Complete nucleotide sequence of the 23S rRNA gene of the cyanobacterium, Anacystis nidulans. Nucl Acids Res 12: 3373–3386 (1984).

    PubMed  Google Scholar 

  8. Douglas SE, Durnford DG, Morden CW: Nucleotide sequence of the gene for the large subunit of ribulose-1,5 bisphosphate carboxylase/oxygenase from Cryptomonas Φ: evidence, supporting the polyphyletic origin of plastids. J Phycol 26: 500–508 (1990).

    Article  Google Scholar 

  9. Douglas SE, Turner S: Molecular evidence for the origin of plastids from a cyanobacterium-like ancestor. J Mol Evol 33: 267–273 (1991).

    PubMed  Google Scholar 

  10. Edwards K, Kossel H: The rRNA operon from Zea mays chloroplasts: nucleotide sequence of 23S rDNA and its homology with E. coli 23S rDNA. Nucl Acids Res 9: 2853–2869 (1981).

    PubMed  Google Scholar 

  11. Felsenstein J: Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791 (1985).

    Google Scholar 

  12. Fukunaga M, Horie I, Mifuchi I: Nucleotide sequence of a 23S ribosomal RNA gene from Leptospira interrogans serovar canicola strain Moulton. Nucl Acids Res 17: 2123 (1989).

    PubMed  Google Scholar 

  13. Gibbs S: The evolution of algal chloroplasts. In: Weissner W, Robinson DG, Starr RC (eds) Experimental phycology I, pp. 145–157. Springer-Verlag, Berlin (1990).

    Google Scholar 

  14. Green CJ, Stewart GC, Hollis MA, Vold BS, Bott KF: Nucleotide sequence of the Bacillus subtilis ribosomal RNA operon, rrnB. Gene 37: 261–266 (1985).

    Article  PubMed  Google Scholar 

  15. Gutell RR, Fox GE: A compilation of large subunit RNA sequences presented in a structural format. Nucl Acids Res 16 (supp): r175-r269 (1988).

    PubMed  Google Scholar 

  16. Höpfl P, Ludwig W, Schleifer KH: Complete nucleotide sequence of a 23S ribosomal RNA gene from Rhodobacter capsulatus. Nucl Acids Res 16: 2343 (1988).

    PubMed  Google Scholar 

  17. Höpfl P, Ludwig W, Schleifer KH, Larsen N: The 23S ribosomal RNA higher-order structure of Pseudomonas cepacia and other prokaryotes. Eur J Biochem 185: 355–364 (1989).

    PubMed  Google Scholar 

  18. Höpfl P, Ulrich N, Hartmann RK, Ludwig W, Schleifer KH: Complete nucleotide sequence of a 23S ribosomal RNA gene from Thermus thermophilus HB. Nucl Acids Res 16: 9043 (1988).

    PubMed  Google Scholar 

  19. Kimura M: A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111–120 (1980).

    PubMed  Google Scholar 

  20. Kop J, Wheaton V, Gupta R, Woese CR, Noller HF: Complete nucleotide sequence of a 23S ribosomal RNA gene from Bacillus stearothermophilus. DNA 3: 347–357 (1984).

    PubMed  Google Scholar 

  21. Kostrzewa M, Valentin K, Maid U, Radetzky R, Zetsche K: Structure of the Rubisco operon from the multicellular red alga Antithamnion spec. Curr Genet 18: 465–469 (1990).

    Article  PubMed  Google Scholar 

  22. Loiseaux-de Goër S, Markowicz Y, Dalmon J, Audren H: Physical maps of the two circular plastid DNA molecules of the brown alga Pylaiella littoralis (L.) Kjellm. Location of the rRNA genes and of several protein coding regions on both molecules. Curr Genet 14: 155–162 (1988).

    Google Scholar 

  23. Loiseaux-de Goër S, Markowicz Y, Somerville CC: Ribosomal RNA genes and pseudogenes of the bimolecular plastid genome of the brown alga Pylaiella littoralis (L.) Kjellm. In: Mache R, Stutz E, Subramanian (eds) The translational apparatus of photosynthetic organelles, pp. 19–29. NATO ASI series H55. Springer-Verlag, Berlin (1991).

    Google Scholar 

  24. Maerz M, Wolters J, Hofmann CJB, Sitte P, Maier UG: Plastid DNA from Pyrenomonas salina (Cryptophyceae): physical map, genes, and evolutionary implications. Curr Genet 21: 73–81 (1992).

    Article  PubMed  Google Scholar 

  25. Markowicz Y, Loiseaux-de Goër S, Mache R: Presence of a 16S rRNA pseudogene in the bimolecular plastid genome of the primitive brown alga Pylaiella littoralis. Evolutionary implications. Curr Genet 14: 599–608 (1988).

    PubMed  Google Scholar 

  26. Markowicz Y, Mache R, Loiseaux-de Goër S: Sequence of the plastid rDNA spacer region of the brown alga Pylaiella littoralis (L.) Kjellm. Evolutionary significance. Plant Mol Biol 10: 465–469 (1988).

    Google Scholar 

  27. Markowicz Y, Loiseaux-de Goër S: Plastid genomes of Rhodophyta and Chromophyta constitute a distinct lineage which differs from that of chlorophyta and have a composite phylogenetic orgin, perhaps like that of Euglenophyta. Curr Genet 20: 427–430 (1991).

    Article  PubMed  Google Scholar 

  28. Martin WF, Somerville CC, Loiseaux-de Goër S: Molecular phylogenies of plastid origins and algal evolution. Review J Mol Evol (1992), in press.

  29. Martin WF, Jouannic S, Loiseaux-de Goër S: Phylogenetic origin of atpB and atpE genes of the brown alga Pylaiella littoralis (submitted).

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

    Article  PubMed  Google Scholar 

  31. Regensburger A, Ludwig W, Frank R, Blöcker H, Schleifer KH: Complete nucleotide sequence of a 23S ribosomal RNA gene from Micrococcus luteus. Nucl Acids Res 16: 2344 (1988).

    PubMed  Google Scholar 

  32. Saiki RK, Gelfand DH, Stoffel S, Sharf SJ, Higuchi R, Horn GT, Mullis KB, Elrich HA: Primer directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491 (1988).

    PubMed  Google Scholar 

  33. Saitou N, Nei M: The neighbor joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425 (1987).

    PubMed  Google Scholar 

  34. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  35. Somerville CC, Jouannic S, Loiseaux-de Goër S: Sequence, proposed secondary structure and phylogenetic analysis of the chloroplast 5S rDNA of the brown alga Pylaiella littoralis (L.) Kjellm. J Mol Evol 34: 246–253 (1992).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  37. Toschka HY, Höpfl P, Ludwig W, Schleifer KH, Ulbrich N, Erdmann VA: Complete nucleotide sequence of a 23S ribosomal RNA gene from Pseudomonas aeruginosa. Nucl Acids Res 15: 7182 (1987).

    PubMed  Google Scholar 

  38. Valentin K, Zetsche K: The genes of both subunits of ribulose-1,5-bisphosphate carboxylase constitute an operon on the plastome of a red alga. Curr Genet 16: 203–209 (1989).

    PubMed  Google Scholar 

  39. Valentin K, Zetsche K: Rubisco genes indicate a close phylogenetic relation between the plastids of Chromophyta and Rhodophyta. Plant Mol Biol 15: 575–584 (1990).

    Article  PubMed  Google Scholar 

  40. Valentin K, Zetsche K: Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: Evidence for a polyphyletic origin of the plastids. Mol Gen Genet 222: 425–430 (1990).

    PubMed  Google Scholar 

  41. Yamada T, Shimaji M: An intron in the 23S rRNA gene of the Chlorella chloroplasts: complete nucleotide sequence of the 23S rRNA gene. Curr Genet 11: 347–352 (1987).

    PubMed  Google Scholar 

  42. Yepiz-Plascencia GM, Jenkins ME, Hallick RB: Nucleotide sequence of the Euglena gracilis chloroplast 23S rRNA gene of the rrnc operon. Nucl Acids Res 16: 9340 (1988).

    PubMed  Google Scholar 

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Author notes

  1. Charles C. Somerville

    Present address: Technical Resources Inc., c/o U.S. Environmental Protection Agency Environmental Research Laboratory, 1 Sabine Island Drive, 32561-5299, Gulf Breeze, FL, USA

Authors and Affiliations

  1. Centre d'Etudes Océanologiques et de Biologie Marine, CNRS-UPR 4601, BP 74, 29680, Roscoff Cedex, France

    Charles C. Somerville, Stefan Jouannic, Bernard Kloareg & Susan Loiseaux-de Goër

  2. Institut für Genetik-Biocentrum, Technische Universität Braunschweig, Postfach 3329, 3300, Braunschweig, Germany

    William F. Martin

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  1. Charles C. Somerville
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  5. Susan Loiseaux-de Goër
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Somerville, C.C., Jouannic, S., Martin, W.F. et al. Secondary structure and phylogeny of the chloroplast 23S rRNA gene from the brown alga Pylaiella littoralis . Plant Mol Biol 21, 779–787 (1993). https://doi.org/10.1007/BF00027111

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  • DOI: https://doi.org/10.1007/BF00027111

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