Skip to main content
SpringerLink
Log in

Sequence variations in the large-subunit ribosomal RNA gene of ammonia (foraminifera, protozoa) and their evolutionary implications

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

Abstract

An unusually high divergence was observed in the ribosomal RNA genes of a free-living population of foraminifera belonging to the genusAmmonia. The sequences of a large-subunit (LSU) rDNA expansion segment D1 and flanking regions were obtained from 20 specimens namedAmmonia sp. 1 andAmmonia sp. 2. The sequence divergence between the two species averages 14%. Within each species it ranges from 0.2% to 7.1% inAmmonia sp. 1 and from 0.7% to 2.3% inAmmonia sp. 2. We did not find two specimens having identical sequences. Moreover, in opposition to the generally acaepted view, rDNA sequence variations were also found within a single individual. The variations among several rDNA copies in a single specimen ofAmmonia may reach up to 4.9%. Most of the observed variations result from multiplication of CA or TA serial repeats occurring in two particularly variable regions. For single base changes, C-T transitions are most frequently observed. We discuss the evolution of expansion segments and their use for phylogenetic studies.

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

  • Bairoch A (1989) PC/Gene, IntelliGenetics, Inc

  • Christen R (1994) Molecular phylogeny and the origin of Metazoa. In: Bengtson S (ed) Early life on earth, Nobel symposium No. 84. Columbia University Press, New York, pp 467–474

    Google Scholar 

  • Clark CG (1987) On the evolution of ribosomal RNA. J Mol Evol 25:343–350

    Article  CAS  PubMed  Google Scholar 

  • Clark CG, Tague BW, Ware VC, Gerbi SA (1984) Xenopus laevis 288 ribosomal RNA: a secondary structure and its evolutionary and functional implications. Nucleic Acids Res 12:6197–6220

    CAS  PubMed  Google Scholar 

  • De Rijk P, Van de Peer Y, Chapelle S, De Wachter R (1994) Database on the structure of large ribosomal subunit RNA. Nucleic Acids Res 22:3495–3501

    PubMed  Google Scholar 

  • Dover AG (1988) rDNA world falling to pieces. Nature 336:623–624

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1988) Phylogenees from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565

    Article  CAS  PubMed  Google Scholar 

  • Gerbi SA, Jeppesen C, Stebbins-Boaz B, Ares M Jr (1987) Evolution of eukaryotic rRNA: constraints imposed by RNA interactions. Cold Spring Harb Symp Quant Biol 11:709–719

    Google Scholar 

  • Goldstein ST, Moodley L (1993) Gametogenesis and the life cycle of the foraminiferaAmmonia beccarii (Linne) Formatepida (Cushman). J Foraminiferal Res 23:213–220

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gonzalez IL, Sylvester JE, Schmickel RD (1988) Human 28S ribosomal RNA sequences heterogeneity. Nucleic Acids Res 16: 10213–10224

    CAS  PubMed  Google Scholar 

  • Gunderson JH, Sogin ML, Wollett G, Hollingdale M, De La Cruz VF, Waters AP, Mc Cutchan TF (1987) Structurally distinct, stage-specific ribosomes occur inPlasmodium. Science 238:933–937

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hamby RK, Zimmer EA (1991) Ribosomal RNA as a phylogenetic tool in plant systematics. In: Soltis P, Soltis D, Doyle JJ (eds) Molecular systematics in plants. Routledge, Chapman and Hall, New York, pp 50–91

    Google Scholar 

  • Hancock JM, Dover GA (1988) Molecular coevolution among cryptically simple expansion segments of eukaryotic 26S/28S rRNAs. Mol Biol Evol 5:377–392

    CAS  PubMed  Google Scholar 

  • Hancock JM, Dover GA (1990) “Compensatory slippage” in the evolution of ribosomal RNA genes. Nucleic Acids Res 18:5949–5954

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Haynes JR (1992) Supposed pronounced ecophenotypy in foraminifera. J Micropaleontol 11:59–63

    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

    Article  CAS  PubMed  Google Scholar 

  • Larsen NGJ, Maidak BL, McCaughey MJ, Overbeek R, Macke TJ, Marsh TL, Woese CR (1993) The ribosomal database project. Nucleic Acids Res 21:3021–3023

    CAS  PubMed  Google Scholar 

  • Larson A, Wilson AC (1989) Patterns of ribosomal RNA evolution in salamanders. Mol Biol Evol 6:131–153

    PubMed  Google Scholar 

  • Lee JJ, Faber WW Jr, Anderson RO, Pawlowski J (1992) Life cycles of foraminifera. In: Lee JJ, Anderson RO (eds) Biology of foraminifera. Academic press, San Diego, pp 285–334

    Google Scholar 

  • Leffers H, Andersen AH (1993) The sequence of 28S ribosomal RNA varies within and between human cell lines. Nucleic Acids Res 21:1449–1455

    CAS  PubMed  Google Scholar 

  • Lenaers G, Scholin C, Bhaud Y, Saint-Hilaire D, HerzogM (1991) A molecular phylogeny of dinoflagellate protists (Pyrrhophyta) inferred from the sequence of 248 r RNA divergent domains D1 and D8. J Mol Evol 32:53–63

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Rocourt M, Pan S, Leibowitz MJ (1992) Sequence and variability of the 5.88 and 26S rRNA genes ofPneumocystis carinii. Nucleic Acids Res 20:3763–3772

    CAS  PubMed  Google Scholar 

  • Maden BE, Dent CL, Farrell TE, Garde J, McCallum F, Wakeman JA (1987) Human rRNA heterogeneity. Biochem J 246:519–527

    CAS  PubMed  Google Scholar 

  • McCutchan TF, De La Cruz VF, Lal AA, Gunderson JH, Elwood HJ, Sogin M (1988) Primary sequence of two small subunit ribosomal RNA genes fromPlasmodium falciparum. Mol Biochem Parasitol 28:63–68

    Article  CAS  PubMed  Google Scholar 

  • Michot B, Qu HL, Bachellerie JP (1990) Evolution of large-subunit rRNA structure; the diversification of divergent D3 domain among major phylogenetic groups. Eur J Biochem 188:219–229

    Article  CAS  PubMed  Google Scholar 

  • Murray JW (1991) Ecology and paleoecology of benthic foraminifera. Longman, Harlow

    Google Scholar 

  • Mylvaganam S, Denis PP (1992) Sequence heterogeneity between the two genes encoding 168 rRNA from thehalophilic archaebacteriumHaloarcula marismortui. Genetics 130:399–410

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pélandakis M, Solignac M (1993) Molecular phylogeny ofDrosophila based on ribosomal RNA sequences. J Mol Evol 37:525–543

    Article  PubMed  Google Scholar 

  • Pawlowski J, Bolivar I, Guiard-Maffia J, Gouy M (1994) Phylogenetic position of Foraminifera inferred from LSU rRNA gene sequences. Mol Biol Evol 11:929–938

    CAS  PubMed  Google Scholar 

  • Pawlowski J, Bolivar I, Fahrni J, Zaninetti L (1995) DNA analysis of “Ammonia beccarii” morphotypes: one or more species? Marine Micropaleontol 26:171–178

    Google Scholar 

  • Qu LH, Nicoloso M, Bachellerie JP (1988) Phylogenetic calibration of the 5′ terminal domain of large rRNA achieved by determining twenty eucaryotic sequences. J Mol Evol 28:113–114

    Article  CAS  PubMed  Google Scholar 

  • Rousset F, Pélandakis M, Solignac M (1991) Evolution of compensatory substitutions through G-U intermediate state inDrosophila rRNA. Proc Natl Acad Sci USA 88:10032–10036

    CAS  PubMed  Google Scholar 

  • Ruiz Linares A, Hancock JM, Dover GA (1991) Secondary structure constraints on the evolution ofDrosophila 28S ribosomal RNA expansion segments. J Mol Biol 219:381–390

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mot Biol Evol 4:406–425

    CAS  Google Scholar 

  • Schlegel M (1991) Protist evolution and phylogeny as discerned from small subunit RNA sequence comparisons. Eur J Protistol 27:207–219

    Google Scholar 

  • Sogin ML (1991) Early evolution and the origin of eukaryotes. Curr Opin Genet Dev 1:457–463

    Article  CAS  PubMed  Google Scholar 

  • Sogin ML (1994) The origin of eukaryotes and evolution into major kingdoms. In: Bengtson S (ed) Early life on earth, Nobel Symposium No. 84. Columbia U.P., New York, pp 181–192

    Google Scholar 

  • Tautz D, Hancock JM, Webb DA, Tautz C, Dover GA (1988) Complete sequences of the rRNA genes ofDrosophila melanogaster. Mol Biol Evol 5:366–376

    CAS  PubMed  Google Scholar 

  • Walton WR, Sloan BJ (1990) The genusAmmonia Brünnich, 1772: its geographic distribution and morphologic variability. J Foraminiferal Res 20:128–156

    Google Scholar 

  • Weekers PHH, Gast RJ, Fuerst PA, Byers TJ (1994) Sequence variations in small-subunit ribosomal RNAs ofHartmanella venniformis and their phylogenetic implications. Mol Biol Evol 11:684–690

    CAS  PubMed  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archae, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    CAS  PubMed  Google Scholar 

  • Zuker M (1989) On finding all suboptimal foldings of an RNA molecule. Science 244:48–52

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Palaontologie der Universität Wien, 1090, Wien, Austria

    Maria Holzmann & Werner Piller

  2. Département de Zoologie et Biologie Animale, Université de Genève, 154 route de Malagnou, 1224, Chêne-Bougeries, Switzerland

    Jan Pawlowski

Authors
  1. Maria Holzmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Werner Piller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jan Pawlowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Correspondence to: J. Pawlowski

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holzmann, M., Piller, W. & Pawlowski, J. Sequence variations in the large-subunit ribosomal RNA gene of ammonia (foraminifera, protozoa) and their evolutionary implications. J Mol Evol 43, 145–151 (1996). https://doi.org/10.1007/BF02337359

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02337359

Key words

Search

Navigation