Skip to main content
SpringerLink
Log in

Secondary structure and patterns of evolution among mammalian mitochondrial 12S rRNA molecules

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

Abstract

Forty-nine complete 12S ribosomal RNA (rRNA) gene sequences from a diverse assortment of mammals (one monotreme, 11 marsupials, 37 placentals), including 11 new sequences, were employed to establish a “core” secondary structure model for mammalian 12S rRNA. Base-pairing interactions were assessed according to the criteria of potential base-pairing as well as evidence for base-pairing in the form of compensatory mutations. In cases where compensatory evidence was not available among mammalian sequences, we evaluated evidence among other vertebrate 12S rRNAs. Our results suggest a core model for secondary structure in mammalian 12S rRNAs with deletions as well as additions to the Gutell (1994:Nucleic Acids Res. 22) models forBos andHomo. In all, we recognize 40 stems, 34 of which are supported by at least some compensatory evidence within Mammalia. We also investigated the occurrence and conservation in mammalian 12S rRNAs of nucleotide positions that are known to participate in the decoding site inE. coli. Twenty-four nucleotide positions known to participate in the decoding site inE. coli also occur among mammalian 12S rRNAs and 17 are invariant for the same base as inE. coli. Patterns of nucleotide substitution were assessed based on our secondary structure model. Transitions in loops become saturated by approximately 10–20 million years. Transitions in stems, in turn, show partial saturation at 20 million years but divergence continues to increase beyond 100 million years. Transversions accumulate lin early beyond 100 million years in both stems and loops although the rate of accumulation of transversions is three- to fourfold higher in loops. Presumably, this difference results from constraints to maintain pairing in stems.

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

  • Allard MW, Miyamoto MM (1992) Perspective: testing phylogenetic approaches with empirical data, as illustrated with the parsimony method. Mol Biol Evol 9:778–786

    CAS  PubMed  Google Scholar 

  • Allard MW, Miyamoto MM, Jarecki L, Kraus F, Tennant MR (1992) DNA systematics and evolution of the artiodactyl family Bovidae. Proc Natl Acad Sci USA 89:3972–3976

    CAS  PubMed  Google Scholar 

  • Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    CAS  PubMed  Google Scholar 

  • Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717

    Article  CAS  PubMed  Google Scholar 

  • Arnason U, Gullberg A (1993) Comparison between the complete mtDNA sequences of the blue and the fin whale, two species that can hybridize in nature. J Mol Evol 37:312–322

    CAS  PubMed  Google Scholar 

  • Amason U, Gullberg A, Johnsson E, Ledje C (1993) The nucleotide sequence of the mitochondrial DNA molecule of the grey seal,Halichoerus grypus, and a comparison with mitochondrial sequences of other true seals. J Mol Evol 37:323–330

    Google Scholar 

  • Arnason U, Gullberg A, Widegren B (1991) The complete nucleotide sequence of the mitochondrial DNA of the fin whale,Balaenoptera physalus. J Mol Evol 33:556–568

    Article  CAS  PubMed  Google Scholar 

  • Arnason U, Johnsson E (1992) The complete mitochondrial DNA sequence of the harbor seal,Phoca vitulina. J Mol Evol 34:493–505

    CAS  PubMed  Google Scholar 

  • Barnes LG, Domning DP, Ray CE (1985) Status of studies in fossil marine mammals. Marine Mamm Sci 1:15–53

    Google Scholar 

  • Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Adachi J, Yano T, Hasegawa M (1994) Phylogenetic place of guinea pigs: no support of the rodent-polyphyly hypothesis from maximum-likelihood analyses of multiple protein sequences. Mol Biol Evol 11:593–604

    CAS  PubMed  Google Scholar 

  • Carroll RL (1988) Vertebrate paleontology and evolution. WH Freeman, New York

    Google Scholar 

  • Catzeflis F, Aguilar J-P, Jaeger J-J (1992) Muroid rodents: phylogeny and evolution. Trends Ecol Evol 7:122–126

    Article  Google Scholar 

  • Chang YS, Huang FL, Lo TB (1994) The complete nucleotide sequence and gene organization of carp (Cyprinus carpio) mitochondrial genome. J Mol Evol 38:138–155

    Article  CAS  PubMed  Google Scholar 

  • Coppens Y, Maglio VJ, Madden CT, Beden M (1978) Proboscidea. In: Maglio VJ, Cooke HBS (eds) Evolution of east African mammals. Harvard University Press, London, pp 336–367

    Google Scholar 

  • Dahlberg AE (1989) The functional role of ribosomal RNA in protein synthesis. Cell 57:525–529

    Article  CAS  PubMed  Google Scholar 

  • Desjardins P, Morais R (1990) Sequence organization of the chicken genome. A novel gene order in higher vertebrates. J Mol Biol 212:599–634

    Article  CAS  PubMed  Google Scholar 

  • Desjardins P, Morais R (1991) Nucleotide sequence and evolution of coding and noncoding regions of a quail mitochondrial genome. J Mol Evol 32:153–161

    CAS  PubMed  Google Scholar 

  • Dixon MT, Hillis DM (1993) Ribosomal RNA secondary structure: Compensatory mutations and implications for phylogenetic analysis. Mol Biol Evol 10:256–267

    CAS  PubMed  Google Scholar 

  • Domning DP (1978) Sirenia. In: Maglio VJ, Cooke HBS (eds) Evolution of east African mammals. Harvard University Press, London, pp 573–581

    Google Scholar 

  • Douzery E (1993) Evolutionary relationships among Cetacea based on the sequence of the mitochondrial 12S rRNA gene: possible paraphyly of toothed-whales (odontocetes) and long separate evolution of sperm whales (Physeteridae). CR Acad Sci III 316: 1511–1518

    CAS  Google Scholar 

  • Douzery E, Catzeflis FM (1995) Molecular evolution of the mitochondrial 12S rRNA in Ungulata (Mammalia). J Mol Evol 41:622–636

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Frye MS, Hedges SB (1995) Monophyly of the order Rodentia inferred from mitochondrial DNA sequences of the genes for 12S rRNA, 16S rRNA, and tRNA-valine. Mol Biol Evol 12:168–176

    CAS  PubMed  Google Scholar 

  • Gadaleta G, Pepe G, De Candia G, Quagliariello C, Sibisa E, Saccone C (1989) The complete nucleotide sequence of theRattus norvegicus mitochondrial genome: cryptic signals revealed by comparative sequence analysis between vertebrates. J Mol Evol 28:497–516

    CAS  PubMed  Google Scholar 

  • Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenedc analysis of covariance by computer simulation. Syst Biol 42:265–292

    Google Scholar 

  • Gatesy J, Hayashi C, DeSalle R, Vrba E (1994) Rate limits for mispairing and compensatory change: the mitochondrial ribosomal DNA of antelopes. Evolution 48:188–196

    Google Scholar 

  • Glotz C, Zwieb C, Brimacombe R (1981) 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

    CAS  PubMed  Google Scholar 

  • Graur D, Hide WA, Li W-H (1991) Is the guinea-pig a rodent? Nature 351:649–652

    Article  CAS  PubMed  Google Scholar 

  • Graur D, Hide WA, Zarkikh A, Li W-H (1992) The biochemical phylogeny of guinea pigs and gundis and the paraphyly of the order Rodentia. Comp Biochem Physiol [B] 101:495–498

    CAS  Google Scholar 

  • Graur D, Higgins DG (1994) Molecular evidence for the inclusion of cetaceans within the order Artiodactyla. Mol Biol Evol 11:357–364

    CAS  PubMed  Google Scholar 

  • Gutell RR (1994) Collection of small subunit (16S- and 16S-like) ribosomal RNA structures. Nucleic Acids Res 22:3502–3507

    CAS  PubMed  Google Scholar 

  • Gutell RR, Larsen N, Woese CR (1994) Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev 58:10–26

    CAS  PubMed  Google Scholar 

  • Gutell RR, Power A, Hertz GZ, Putz J, Stormo GD (1992) Identifying constraints on the higher-order structure of RNA: continued development and application of comparative sequence analysis methods. Nucleic Acids Res 20:5785–5795

    CAS  PubMed  Google Scholar 

  • Gutell RR, Weiser B, Woese C, Noller HF (1985) Comparative anatomy of 16-S-like ribosomal RNA. Prog Nucleic Acid Res 32: 155–215

    CAS  Google Scholar 

  • Hedges SB (1994) Molecular evidence for the origin of birds. Proc Natl Acad Sci USA 91:2621–2624

    CAS  PubMed  Google Scholar 

  • Hedges SB, Hass CA, Maxson LR (1993) Relations of fish and tetrapods. Nature 363:501–502

    Article  CAS  PubMed  Google Scholar 

  • Herr W, Chapman NM, Noller HF (1979) Mechanism of ribosomal subunit association: discrimination of specific sites in 16S RNA essential for association activity. J Mol Biol 130:433–449

    CAS  PubMed  Google Scholar 

  • Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244

    Article  CAS  PubMed  Google Scholar 

  • Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Quart Rev Biol 66:411–453

    Article  CAS  PubMed  Google Scholar 

  • Hixson JE, Brown WM (1986) A comparison of small ribosomal RNA genes from the mitochondrial DNA of the great apes and humans: sequence, structure, evolution, and phylogenetic implications. Mol Biol Evol 33:209–215

    Google Scholar 

  • Holley RW, Apgar J, Everett GA, Madison JT, Marquisee M, Merrill SH, Penswick JR, Zamir A (1965) Structure of a ribonucleic acid. Science 147:1462–1465

    CAS  PubMed  Google Scholar 

  • Janke A, Feldmaier-Fuchs G, Thomas WK, von Haesler A, Paabo S (1994) The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137:243–256

    CAS  PubMed  Google Scholar 

  • Kim SH (1979) Crystal structure of yeast tRNA-phe and general structural features of other tRNAs. In: Schimmel PR, Soll D, Abelson IN (eds) Transfer RNA: structure, properties, and recognition. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 83–100

    Google Scholar 

  • Kraus F, Miyamoto MM (1991) Rapid cladogenesis among the pecoran ruminants: evidence from mitochondrial DNA sequences. Syst Zool 40:117–130

    Google Scholar 

  • Lavergne A, Douzery E, Stichler T, Catzeflis FM, Springer MS (1996) Interordinal mammalian relationships: evidence for paenungulate monophyly is provided by complete mitochondrial 12S rRNA sequences. Mol Phylogenet Evol (in press)

  • Lento GM, Hickson RE, Chambers GK, Penny D (1995) Use of spectral analysis to test hypotheses on the origin of pinnipeds. Mol Biol Evol 12:28–52

    CAS  PubMed  Google Scholar 

  • Levitt M (1969) Detailed molecular model for transfer ribonucleic acid. Nature 224:759–763

    CAS  PubMed  Google Scholar 

  • Luckett WP, Hartenberger J-L (1993) Monophyly or polyphyly of the order Rodentia: possible conflict between morphological and molecular interpretations. J Mamm Evol 1:127–147

    Google Scholar 

  • MacFadden BJ (1992) Fossil horses: systematics, paleobiology, and evolution of the family Equidae. Cambridge University Press, New York

    Google Scholar 

  • Madison JT, Everett GA, Kung KK (1966) On the nucleotide sequence of yeast tyrosine transfer RNA. Cold Spring Harb Symp Quant Biol 31:409–416

    CAS  PubMed  Google Scholar 

  • Marshall LG, Case JA, Woodburne MO (1990) Phylogenetic relationships of the families of marsupials. In: Genoways HH (ed) Current mammalogy, vol 2. Plenum Press, New York, pp 433–505

    Google Scholar 

  • Martin AP (1995) Metabolic rate and directional nucleotide substitution in animal mitochondrial DNA. Mol Biol Evol 12:1124–1131

    CAS  PubMed  Google Scholar 

  • Miyamoto MM, Kraus F, Ryder OA (1990) Phylogeny and evolution of antlered deer determined from mitochondrial DNA sequences. Proc Natl Acad Sci USA 87:6127–6131

    CAS  PubMed  Google Scholar 

  • Moazed D, Noller HF (1990) Binding of tRNA to the ribosomal A and P sites protects two distinct sets of nucleotides in 16S rRNA. J Mol Biol 211:135–145

    Article  CAS  PubMed  Google Scholar 

  • Nagae Y, Fujii H, Yoneyama Y, Goto Y, Okazaki T (1988) Nucleotide sequences of theRana catesbeiana mitochondrial small (12S) and large (16S) ribosomal RNA genes. Nucleic Acids Res 16:10363

    CAS  PubMed  Google Scholar 

  • Noller HF (1991) Ribosomal RNA and translation. Ann Rev Biochem 60:191–227

    CAS  PubMed  Google Scholar 

  • Noller HF (1993) tRNA-rRNA interactions and peptidyl transferase. FASEB J 7:87–89

    CAS  PubMed  Google Scholar 

  • Novacek MJ (1993) Reflections on higher mammalian phylogenetics. J Mamm Evol 1:3–30

    Google Scholar 

  • Nowak RM, Paradiso JL (1983) Walker's mammals of the world. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Pettigrew JD (1986) Flying primates? Megabats have the advanced pathway from eye to midbrain. Science 231:1304–1306

    CAS  PubMed  Google Scholar 

  • Pettigrew JD (1994) Flying DNA. Curr Biol 4:277–280

    Article  CAS  PubMed  Google Scholar 

  • Philippe H, Douzery E (1994) The pitfalls of molecular phylogeny based on four species as illustrated by the Cetacea/Artiodactyla relationships. J Mamm Evol 2:133–152

    Google Scholar 

  • Poldermans B, Bakker H, Van Knippenberg PH (1980) Studies on the function of two adjacent N6,N6 dimethyladenosines near the 3′ end of 16S ribosomal RNA ofEscherichia coli. IV. The effects of the methylgroups on ribosomal subunit interactions. Nucleic Acids Res 8:143–151

    CAS  PubMed  Google Scholar 

  • RajBhandary UL, Stuart A, Faulkner RD, Chang SH, Khorana HG (1966) Nucleotide sequence studies on yeast phenylalanine sRNA. Cold Spring Harb Symp Quant Biol 31:425–434

    CAS  PubMed  Google Scholar 

  • Roe BA, Ma DP, Wilson RK, Wong IF (1985) The complete nucleotide sequence of theXenopus laevis mitochondrial genome. J Biol Chem 260: 9759–9774

    CAS  PubMed  Google Scholar 

  • Rowe T (1993) Phylogenetic systematics and the early history of mammals. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal phylogeny. Springer-Verlag, New York, pp 129–145

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sibley CG, Ahlquist JE (1984) The phylogeny of the hominoid primates, as indicated by DNA-DNA hybridization. J Mol Evol 20: 2–15

    Article  CAS  PubMed  Google Scholar 

  • Simmons NB (1994) The case for chiropteran monophyly. Am Museum Novitates 3103: 1–54

    Google Scholar 

  • Smith AB (1989) RNA sequence data in phylogenetic reconstruction: testing the limits of its resolution. Cladistics 5: 321–344

    Google Scholar 

  • Springer MS, Hollar LJ, Burk A (1995) Compensatory substitutions and the evolution of the mitochondrial 12S rRNA gene in mammals. Mol Biol Evol 12: 1138–1150

    CAS  PubMed  Google Scholar 

  • Springer MS, Kirsch JAW (1993) A molecular perspective on the phylogeny of placental mammals based on mitochondrial 12S rDNA sequences, with special reference to the problem of the Paenungulata. J Mamm Evol 1: 149–166

    Google Scholar 

  • Springer MS, Westerman M, Kirsch JAW (1994) Relationships among orders and families of marsupials based on 12S ribosomal DNA sequences and the timing of the marsupial radiation. J Mamm Evol 2: 85–115

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Szalay FS (1994) Evolutionary history of the marsupials and an analysis of osteological characters. Cambridge University Press, New York

    Google Scholar 

  • Tanhauser S (1985) Evolution of mitochondrial DNA: patterns and rate of change. PhD dissertation, University of Florida, Gainesville

    Google Scholar 

  • Tapprich WE, Hill WE (1986) Involvement of bases 787–795 ofEscherichia coli 16S ribosomal RNA in ribosomal subunit association. Proc Natl Acad Sci USA 83: 556–560

    CAS  PubMed  Google Scholar 

  • Turner DH, Sugimoto N, Freier SM (1988) RNA structure prediction. Annu Rev Biophys Chem 17: 167–192

    Article  CAS  Google Scholar 

  • Tzeng C-S, Shen S-C, Huang P-C (1992) The complete nucleotide sequences of theCrossostoma lacustre mitochondrial genome: conservation and variations among vertebrates. Nucleic Acids Res 20: 4853–4858

    CAS  PubMed  Google Scholar 

  • Vawter L, Brown WM (1993) Rates and patterns of base change in the small subunit ribosomal RNA gene. Genetics 134: 597–608

    CAS  PubMed  Google Scholar 

  • Wheeler WC, Honeycutt RL (1988) Paired sequence difference in ribosomal RNAs: evolutionary and phylogenetic implications. Mol Biol Evol 5: 90–96

    CAS  PubMed  Google Scholar 

  • Woese CR, Gutell R, Gupta R, Noller HF (1983) Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids. Microbiol Rev 47: 621–669

    CAS  PubMed  Google Scholar 

  • Woese CR, Magrum LJ, Gupta R, Siegel RB, Stahl DA, Kop J, Crawford N, Brosius J, Gutell R, Hogan JJ, Noller HF (1980) Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence. Nucleic Acids Res 8: 2275–2293

    CAS  PubMed  Google Scholar 

  • Wool IG, Endo Y, Chan Y-L, Gluck A (1990) Structure, function, and evolution of mammalian ribosomes. In: Hill WE, Dahlbert A, Garrett RA, Moore PB, Schlessinger D, Warner JR (eds) The ribosome: structure, function, and evolution. American Society for Microbiology, Washington, DC, pp 203–214

    Google Scholar 

  • Xu X, Arnason U (1994) The complete mitochondrial DNA sequence of the horse, Equus caballus: extensive heteroplasmy of the control region. Gene 148: 357–362

    CAS  PubMed  Google Scholar 

  • Yonath A, Bennett W, Weinstein S, Wittman HG (1990) Crystallography and image reconstructions of ribosomes. In: Hill WE, Dahlberg A, Garrett RA, Moore PB, Schlessinger D, Warner JR (eds) The ribosome: structure, function, and evolution. American Society for Microbiology, Washington, DC, pp 134–147

    Google Scholar 

  • Zachau HG, Dotting D, Feldmann H, Melchers F, Karau W (1966) Serine specific transfer ribonucleic acids. XIV. Comparison of nucleotide sequences and secondary structure models. Cold Spring Harb Symp Quant Biol 31: 417–424

    CAS  PubMed  Google Scholar 

  • Zwieb C, Glotz C, Brimacombe R (1981) Secondary structure comparisons between small subunit ribosomal RNA molecules from six different species. Nucleic Acids Res 9: 3621–3640

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of California, 92521, Riverside, CA, USA

    Mark S. Springer

  2. Laboratoire de Paleontologie, Institut des Sciences de l'Evolution, URA 327 CNRS, Place E. Bataillon, F-34 095, Montpellier, Cedex 05, France

    Emmanuel Douzery

Authors
  1. Mark S. Springer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emmanuel Douzery
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Correspondence to: M. S. Springer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Springer, M.S., Douzery, E. Secondary structure and patterns of evolution among mammalian mitochondrial 12S rRNA molecules. J Mol Evol 43, 357–373 (1996). https://doi.org/10.1007/BF02339010

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02339010

Key words

Search

Navigation