Journal of Molecular Evolution

, Volume 43, Issue 4, pp 357–373 | Cite as

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

  • Mark S. Springer
  • Emmanuel Douzery
Article

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.

Key words

Mitochondrial 12S rRNA Secondary structure Evolutionary rates Nucleotide substitution patterns Mammalia 

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References

  1. Allard MW, Miyamoto MM (1992) Perspective: testing phylogenetic approaches with empirical data, as illustrated with the parsimony method. Mol Biol Evol 9:778–786PubMedGoogle Scholar
  2. 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 89:3972–3976PubMedGoogle Scholar
  3. 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 290:457–465PubMedGoogle Scholar
  4. 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 156:683–717CrossRefPubMedGoogle Scholar
  5. 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 37:312–322PubMedGoogle Scholar
  6. 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 37:323–330Google Scholar
  7. Arnason U, Gullberg A, Widegren B (1991) The complete nucleotide sequence of the mitochondrial DNA of the fin whale,Balaenoptera physalus. J Mol Evol 33:556–568CrossRefPubMedGoogle Scholar
  8. Arnason U, Johnsson E (1992) The complete mitochondrial DNA sequence of the harbor seal,Phoca vitulina. J Mol Evol 34:493–505PubMedGoogle Scholar
  9. Barnes LG, Domning DP, Ray CE (1985) Status of studies in fossil marine mammals. Marine Mamm Sci 1:15–53Google Scholar
  10. Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180CrossRefPubMedGoogle Scholar
  11. 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 11:593–604PubMedGoogle Scholar
  12. Carroll RL (1988) Vertebrate paleontology and evolution. WH Freeman, New YorkGoogle Scholar
  13. Catzeflis F, Aguilar J-P, Jaeger J-J (1992) Muroid rodents: phylogeny and evolution. Trends Ecol Evol 7:122–126CrossRefGoogle Scholar
  14. Chang YS, Huang FL, Lo TB (1994) The complete nucleotide sequence and gene organization of carp (Cyprinus carpio) mitochondrial genome. J Mol Evol 38:138–155CrossRefPubMedGoogle Scholar
  15. 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 336–367Google Scholar
  16. Dahlberg AE (1989) The functional role of ribosomal RNA in protein synthesis. Cell 57:525–529CrossRefPubMedGoogle Scholar
  17. Desjardins P, Morais R (1990) Sequence organization of the chicken genome. A novel gene order in higher vertebrates. J Mol Biol 212:599–634CrossRefPubMedGoogle Scholar
  18. Desjardins P, Morais R (1991) Nucleotide sequence and evolution of coding and noncoding regions of a quail mitochondrial genome. J Mol Evol 32:153–161PubMedGoogle Scholar
  19. Dixon MT, Hillis DM (1993) Ribosomal RNA secondary structure: Compensatory mutations and implications for phylogenetic analysis. Mol Biol Evol 10:256–267PubMedGoogle Scholar
  20. Domning DP (1978) Sirenia. In: Maglio VJ, Cooke HBS (eds) Evolution of east African mammals. Harvard University Press, London, pp 573–581Google Scholar
  21. 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: 1511–1518Google Scholar
  22. Douzery E, Catzeflis FM (1995) Molecular evolution of the mitochondrial 12S rRNA in Ungulata (Mammalia). J Mol Evol 41:622–636CrossRefPubMedGoogle Scholar
  23. Fox GE, Woese CR (1975) 5S RNA secondary structure. Nature 256: 505–507CrossRefPubMedGoogle Scholar
  24. 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 12:168–176PubMedGoogle Scholar
  25. 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 28:497–516PubMedGoogle Scholar
  26. Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenedc analysis of covariance by computer simulation. Syst Biol 42:265–292Google Scholar
  27. Gatesy J, Hayashi C, DeSalle R, Vrba E (1994) Rate limits for mispairing and compensatory change: the mitochondrial ribosomal DNA of antelopes. Evolution 48:188–196Google Scholar
  28. 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 9:3287–3306PubMedGoogle Scholar
  29. Graur D, Hide WA, Li W-H (1991) Is the guinea-pig a rodent? Nature 351:649–652CrossRefPubMedGoogle Scholar
  30. 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] 101:495–498Google Scholar
  31. Graur D, Higgins DG (1994) Molecular evidence for the inclusion of cetaceans within the order Artiodactyla. Mol Biol Evol 11:357–364PubMedGoogle Scholar
  32. Gutell RR (1994) Collection of small subunit (16S- and 16S-like) ribosomal RNA structures. Nucleic Acids Res 22:3502–3507PubMedGoogle Scholar
  33. Gutell RR, Larsen N, Woese CR (1994) Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev 58:10–26PubMedGoogle Scholar
  34. 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 20:5785–5795PubMedGoogle Scholar
  35. Gutell RR, Weiser B, Woese C, Noller HF (1985) Comparative anatomy of 16-S-like ribosomal RNA. Prog Nucleic Acid Res 32: 155–215Google Scholar
  36. Hedges SB (1994) Molecular evidence for the origin of birds. Proc Natl Acad Sci USA 91:2621–2624PubMedGoogle Scholar
  37. Hedges SB, Hass CA, Maxson LR (1993) Relations of fish and tetrapods. Nature 363:501–502CrossRefPubMedGoogle Scholar
  38. 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 130:433–449PubMedGoogle Scholar
  39. Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244CrossRefPubMedGoogle Scholar
  40. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Quart Rev Biol 66:411–453CrossRefPubMedGoogle Scholar
  41. 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 33:209–215Google Scholar
  42. Holley RW, Apgar J, Everett GA, Madison JT, Marquisee M, Merrill SH, Penswick JR, Zamir A (1965) Structure of a ribonucleic acid. Science 147:1462–1465PubMedGoogle Scholar
  43. Janke A, Feldmaier-Fuchs G, Thomas WK, von Haesler A, Paabo S (1994) The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137:243–256PubMedGoogle Scholar
  44. 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 83–100Google Scholar
  45. Kraus F, Miyamoto MM (1991) Rapid cladogenesis among the pecoran ruminants: evidence from mitochondrial DNA sequences. Syst Zool 40:117–130Google Scholar
  46. 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)Google Scholar
  47. Lento GM, Hickson RE, Chambers GK, Penny D (1995) Use of spectral analysis to test hypotheses on the origin of pinnipeds. Mol Biol Evol 12:28–52PubMedGoogle Scholar
  48. Levitt M (1969) Detailed molecular model for transfer ribonucleic acid. Nature 224:759–763PubMedGoogle Scholar
  49. Luckett WP, Hartenberger J-L (1993) Monophyly or polyphyly of the order Rodentia: possible conflict between morphological and molecular interpretations. J Mamm Evol 1:127–147Google Scholar
  50. MacFadden BJ (1992) Fossil horses: systematics, paleobiology, and evolution of the family Equidae. Cambridge University Press, New YorkGoogle Scholar
  51. Madison JT, Everett GA, Kung KK (1966) On the nucleotide sequence of yeast tyrosine transfer RNA. Cold Spring Harb Symp Quant Biol 31:409–416PubMedGoogle Scholar
  52. 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 433–505Google Scholar
  53. Martin AP (1995) Metabolic rate and directional nucleotide substitution in animal mitochondrial DNA. Mol Biol Evol 12:1124–1131PubMedGoogle Scholar
  54. Miyamoto MM, Kraus F, Ryder OA (1990) Phylogeny and evolution of antlered deer determined from mitochondrial DNA sequences. Proc Natl Acad Sci USA 87:6127–6131PubMedGoogle Scholar
  55. 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 211:135–145CrossRefPubMedGoogle Scholar
  56. 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 16:10363PubMedGoogle Scholar
  57. Noller HF (1991) Ribosomal RNA and translation. Ann Rev Biochem 60:191–227PubMedGoogle Scholar
  58. Noller HF (1993) tRNA-rRNA interactions and peptidyl transferase. FASEB J 7:87–89PubMedGoogle Scholar
  59. Novacek MJ (1993) Reflections on higher mammalian phylogenetics. J Mamm Evol 1:3–30Google Scholar
  60. Nowak RM, Paradiso JL (1983) Walker's mammals of the world. Johns Hopkins University Press, BaltimoreGoogle Scholar
  61. Pettigrew JD (1986) Flying primates? Megabats have the advanced pathway from eye to midbrain. Science 231:1304–1306PubMedGoogle Scholar
  62. Pettigrew JD (1994) Flying DNA. Curr Biol 4:277–280CrossRefPubMedGoogle Scholar
  63. Philippe H, Douzery E (1994) The pitfalls of molecular phylogeny based on four species as illustrated by the Cetacea/Artiodactyla relationships. J Mamm Evol 2:133–152Google Scholar
  64. 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 8:143–151PubMedGoogle Scholar
  65. RajBhandary UL, Stuart A, Faulkner RD, Chang SH, Khorana HG (1966) Nucleotide sequence studies on yeast phenylalanine sRNA. Cold Spring Harb Symp Quant Biol 31:425–434PubMedGoogle Scholar
  66. Roe BA, Ma DP, Wilson RK, Wong IF (1985) The complete nucleotide sequence of theXenopus laevis mitochondrial genome. J Biol Chem 260: 9759–9774PubMedGoogle Scholar
  67. 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 129–145Google Scholar
  68. 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: 487–491PubMedGoogle Scholar
  69. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467PubMedGoogle Scholar
  70. Sibley CG, Ahlquist JE (1984) The phylogeny of the hominoid primates, as indicated by DNA-DNA hybridization. J Mol Evol 20: 2–15CrossRefPubMedGoogle Scholar
  71. Simmons NB (1994) The case for chiropteran monophyly. Am Museum Novitates 3103: 1–54Google Scholar
  72. Smith AB (1989) RNA sequence data in phylogenetic reconstruction: testing the limits of its resolution. Cladistics 5: 321–344Google Scholar
  73. Springer MS, Hollar LJ, Burk A (1995) Compensatory substitutions and the evolution of the mitochondrial 12S rRNA gene in mammals. Mol Biol Evol 12: 1138–1150PubMedGoogle Scholar
  74. 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: 149–166Google Scholar
  75. 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: 85–115Google Scholar
  76. 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: 487–495CrossRefPubMedGoogle Scholar
  77. Szalay FS (1994) Evolutionary history of the marsupials and an analysis of osteological characters. Cambridge University Press, New YorkGoogle Scholar
  78. Tanhauser S (1985) Evolution of mitochondrial DNA: patterns and rate of change. PhD dissertation, University of Florida, GainesvilleGoogle Scholar
  79. 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: 556–560PubMedGoogle Scholar
  80. Turner DH, Sugimoto N, Freier SM (1988) RNA structure prediction. Annu Rev Biophys Chem 17: 167–192CrossRefGoogle Scholar
  81. 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: 4853–4858PubMedGoogle Scholar
  82. Vawter L, Brown WM (1993) Rates and patterns of base change in the small subunit ribosomal RNA gene. Genetics 134: 597–608PubMedGoogle Scholar
  83. Wheeler WC, Honeycutt RL (1988) Paired sequence difference in ribosomal RNAs: evolutionary and phylogenetic implications. Mol Biol Evol 5: 90–96PubMedGoogle Scholar
  84. 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: 621–669PubMedGoogle Scholar
  85. 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: 2275–2293PubMedGoogle Scholar
  86. 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 203–214Google Scholar
  87. Xu X, Arnason U (1994) The complete mitochondrial DNA sequence of the horse, Equus caballus: extensive heteroplasmy of the control region. Gene 148: 357–362PubMedGoogle Scholar
  88. 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 134–147Google Scholar
  89. 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: 417–424PubMedGoogle Scholar
  90. Zwieb C, Glotz C, Brimacombe R (1981) Secondary structure comparisons between small subunit ribosomal RNA molecules from six different species. Nucleic Acids Res 9: 3621–3640PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1996

Authors and Affiliations

  • Mark S. Springer
    • 1
  • Emmanuel Douzery
    • 2
  1. 1.Department of BiologyUniversity of CaliforniaRiversideUSA
  2. 2.Laboratoire de PaleontologieInstitut des Sciences de l'EvolutionMontpellierFrance

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