Skip to main content
Log in

Phylogenetic calibration of the 5′ terminal domain of large rRNA achieved by determining twenty eucaryotic sequences

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

Due to their high information content and their particular mode of variation, large rRNA molecules potentially represent powerful indicators of phylogenetic relationships. Even partial sequences may suffice to generate reliable estimations, provided they correspond to well-chosen portions of the molecule. We have systematically analyzed a specific portion of the large rRNA (the region extending over nearly 400 nucleotides from the 5′ end) as a general index of eucaryotic phylogeny. By means of fast and direct rRNA sequencing, we have determined the sequence of this region for 20 additional eucaryotes, including several representatives of each vertebrate class, an invertebrate metazoan (mussel), a fungus (Schizosaccharomyces pombe), and three higher plants. Comparative treatment of these new data and previously reported rRNA sequences shows that this region can serve as an indicator of eucaryotic phylogeny for evaluating both long-range and short-range relationships. Its conservative domains appear to possess a rather uniform rate of nucleotide changes in all the eucaryotic lineages analyzed and the phylogenetic tree we derived agrees with classical views.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Auffray C, Rougeon F (1980) Purification of mouse immunoglobin heavy-chain messenger RNA from total myeloma tumour RNA. Eur J Biochem 107:303–314

    Google Scholar 

  • Baroin A, Perasso R, Qu LH, Brugerolle G, Bachellerie JP, Adoutte A (1988) A partial phylogeny of the unicellular eucaryotes based on a rapid sequencing of a portion of 28S ribosomal RNA. Proc Natl Acad Sci USA 85 (in press)

  • Bobrova VK, Troitsky AV, Ponomarev AG, Antonov AS (1987) Low-molecular-weight rRNAs sequences and plant phylogeny reconstruction: nucleotide seqeunces of chloroplast 4.5S rRNA fromAcorus calamus (Araceae) andLigularia calthifolia (Asteracea). Plant Syst Evol 156:13–27

    Google Scholar 

  • Branlant C, Krol A, Machatt MA, Pouyet J, Ebel JP, Edwards K, Kossell H (1981) Primary and secondary structures ofEscherichia coli MRE 600 23S ribosomal RNA. Comparison with models of secondary structure for maize chloroplast 23S rRNA and for large portions of mouse and human 16S mitochondrial rRNAs. Nucleic Acids Res 9:4303–4324

    Google Scholar 

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

    Google Scholar 

  • Chan YL, Olvera J, Wool IG (1983) The structure of rat 28S ribosomal RNA inferred from the sequence of nucleotides in a gene. Nucleic Acids Res 11:7819–7831

    Google Scholar 

  • Ellis RE, Sulston JE, Coulson AR (1986) The rDNA ofC. elegans: sequence and structure. Nucleic Acids Res 14:2345–2364

    Google Scholar 

  • Erdman VA, Wolters J (1986) Collection of published 5S, 5.8S and 4.5S ribosomal RNA sequences. Nucleic Acids Res 14:r1-r59

    Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284

    Google Scholar 

  • Georgiev OI, Nikolaev N, Hadjioloy AA, Skryabin KG, Zakharyev VM, Bayev AA (1981) The structure of the yeast ribosomal RNA genes 4. Complete sequence of the 25S rRNA gene fromSaccharomyces cerevisiae. Nucleic Acids Res 9:6953–6958

    Google Scholar 

  • Gerbi SA (1985) Evolution of ribosomal DNA. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 419–517

    Google Scholar 

  • Gonzalez IL, Gorski JL, Campen TJ, Dorney DJ, Erickson JM, Sylvester JE, Schmickel RD (1985) Variation among human 28S ribosomal RNA genes. Proc Natl Acad Sci USA 82:7666–7670

    Google Scholar 

  • Goodman M, Czeluzniak J, Moore GW, Romero-Herrera E, Matsuda G (1979) Fitting the gene lineage into its species lineage, a parsimony strategy illustrated by cladograms constructed from globin sequences. Syst Zool 28:132–163

    Google Scholar 

  • Goodman M, Weiss ML, Czeluzniak J (1982) Molecular evolution above the species level: branching pattern, rates and mechanisms. Syst Zool 31:376–399

    Google Scholar 

  • Guthrie C (1986) Finding functions for small nuclear RNAs in yeast. Trends Biochem Sci 11:430–434

    Google Scholar 

  • Hadjiolov AA, Georgiev OI, Nosikov VV, Yavachev LP (1984) Primary and secondary structure of rat 28S ribosomal RNA. Nucleic Acids Res 12:3677–3693

    Google Scholar 

  • Hasegawa M, Iida Y, Yano T, Takaiwa F, Iwabuchi M (1985) Phylogenetic relationships among eucaryotic kingdoms inferred from ribosomal RNA sequences. J Mol Evol 22:32–38

    Google Scholar 

  • Hassouna N, Michot B, Bachellerie JP (1984) The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eucaryotes. Nucleic Acids Res 12:3563–3583

    Google Scholar 

  • Hickey LJ, Doyle JA (1977) Early Cretaceous fossil evidence for angiosperm evolution. Bot Rev 43:3–104

    Google Scholar 

  • Hindenach BR, Stafford DW (1984) Nucleotide sequence of the 18S–26S rRNA intergene region of the sea urchin. Nucleic Acids Res 12:1737–1747

    Google Scholar 

  • Hori H, Osawa S (1979) Evolutionary change in 5S RNA secondary structure and a phylogenetic tree of 54 5S RNA species. Proc Natl Acad Sci USA 76:381–385

    Google Scholar 

  • Hori H, Osawa S (1986) Evolutionary change in 5S rRNA secondary structure and a phylogenetic tree of 352 5S rRNA species. BioSystems 19:163–172

    Google Scholar 

  • Hori H, Lim BK, Osawa S (1985) Evolution of green plants as deduced from 5S rRNA sequences. Proc Natl Acad Sci USA 82:820–823

    Google Scholar 

  • Huysmans E, Dams E, Vandenberghe A, De Wachter R (1983) The nucleotide sequences of the 5S rRNAs of four mushrooms and their use in studying the phylogenetic position of basidiomycetes among the eucaryotes. Nucleic Acids Res 11:2871–2880

    Google Scholar 

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

    Google Scholar 

  • Kaufer NF, Simanis V, Nurse P (1985) Fission yeastSchizosaccharomyces pombe correctly excises a mammalian RNA transcript intervening sequence. Nature 318:78–80

    Google Scholar 

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

    Google Scholar 

  • Küntzel H, Heidrich M, Piechulla B (1981) Phylogenetic tree derived from bacterial, cytosol and organelle 5S rRNA sequences. Nucleic Acids Res 9:1451–1461

    Google Scholar 

  • Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82:6955–6959

    Google Scholar 

  • Lazar E, Haendler B, Jacob M (1983) Two 5S genes are expressed in chicken somatic cells. Nucleic Acids Res 11:7735–7741

    Google Scholar 

  • Le Meur M, Glanville N, Mandel JL, Gerlinger P, Palmiter R, Chambon P (1981) The ovalbumin gene family: hormonal control of X and Y gene transcription and mRNA accumulation. Cell 23:561–571

    Google Scholar 

  • Lempereur L (1986) Le ARN de la petite sous-unité ribosomique, conformation et mode d'évolution structurale de la région 5′ chez les eucaryotes. PhD Thesis, Université Paul-Sabatier, Toulouse no. 26

    Google Scholar 

  • Maxam AM, Gilbert W (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol 65:499–560

    Google Scholar 

  • Michot B, Bachellerie JP (1987) Comparisons of large subunit rRNAs reveal some eucaryote-specific elements of secondary structure. Biochimie 69:11–23

    Google Scholar 

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

    Google Scholar 

  • Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal rate in cellular genomes. J Mol Evol 4:74–86

    Google Scholar 

  • Otsuka T, Nomiyama H, Yoshida H, Kubita T, Kuhara S, Sakaki T (1983) Complete nucleotide sequence of the 26S rRNA gene ofPhysarum polycephalum: its significance in gene evolution. Proc Natl Acad Sci USA 80:3163–3167

    Google Scholar 

  • Ozaki T, Hoshikawa Y, Iida Y, Iwabuchi M (1984) Sequence analysis of the transcribed and 5′ non-transcribed regions of the rRNA gene inDictyostelium discoideum, Nucleic Acids Res 12:4171–4184

    Google Scholar 

  • Pace NR, Olsen GJ, Woese CR (1986) Ribosomal RNA phylogeny and the primary lines of evolutionary descent. Cell 45:325–326

    Google Scholar 

  • Qu LH (1986) Structuration et évolution de l'ARN ribosomique 28S chez les eucaryotes. Etude systématique de la région 5′ terminale. PhD Thesis (Doctorat d'Etat), Université Paul-Sabatier, Toulouse no. 1273

    Google Scholar 

  • Qu LH, Michot B, Bachellerie JP (1983) Improved methods for structure probing in large RNAs: a rapid “heterologous” sequencing approach is coupled to the direct mapping of nuclease accessible sites. Application to the 5′ terminal domain of eucaryotic 28S rRNA. Nucleic Acids Res 11:5903–5920

    Google Scholar 

  • Qu LH, Hardman N, Gill L, Chappell L, Nicoloso M, Bachellerie JP (1986) Phylogeny of helminths determined by rRNA sequence comparison. Mol Biochem. Parasitol 20:93–99

    Google Scholar 

  • Rafalski JA, Wiewiorowski M, Soll D, (1982) Organization and nucleotide sequence of nuclear 5S rRNA genes in yellow lupin (Lupinus luteus). Nucleic Acids Res 10:7635–7641

    Google Scholar 

  • Salim M, Maden BEH (1981) Nucleotide sequence ofXenopus laevis 18S ribosomal RNA inferred from gene sequence. Nature 291:205–208

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467

    Google Scholar 

  • Sogin ML, Miotto K Miller L (1986) Primary structure of theNeurospora crassa small subunit rRNA coding region. Nucleic Acids Res 14:9540

    Google Scholar 

  • Takaiwa F, Oono K, Iida Y, Sugiura M (1985) The complete nucleotide sequence of a rice 25S rRNA gene. Gene 37:255–259

    Google Scholar 

  • Veldman GM, Klootwijk J, De Regt VCHF, Planta RJ, Branlant C, Krol A, Ebel JP (1981) The primary and secondary structure of yeast 26S rRNA. Nucleic Acids Res 9:6935–6952

    Google Scholar 

  • Ware VC, Tague BW, Clark CG, Gourse RL, Brand RC, Gerbi S (1983) Sequence analysis of 28S ribosomal DNA from the amphibianXenopus laevis. Nucleic Acids Res 11:7795–7817

    Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    Google Scholar 

  • Wolters J, Erdman VA (1986) Cladistic analysis of 5S rRNA and 16S rRNA secondary and primary structure. The evolution of eucaryotes and their relation to archaebacteria. J Mol Evol 24:152–166

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Qu, LH., Nicoloso, M. & Bachellerie, JP. Phylogenetic calibration of the 5′ terminal domain of large rRNA achieved by determining twenty eucaryotic sequences. J Mol Evol 28, 113–124 (1988). https://doi.org/10.1007/BF02143502

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02143502

Key words

Navigation