Journal of Molecular Evolution

, Volume 66, Issue 1, pp 21–35 | Cite as

The Origin and Evolution of tRNA Inferred from Phylogenetic Analysis of Structure

Article

Abstract

The evolutionary history of the two structural and functional domains of tRNA is controversial but harbors the secrets of early translation and the genetic code. To explore the origin and evolution of tRNA, we reconstructed phylogenetic trees directly from molecular structure. Forty-two structural characters describing the geometry of 571 tRNAs and three statistical parameters describing thermodynamic and mechanical features of molecules quantitatively were used to derive phylogenetic trees of molecules and molecular substructures. Trees of molecules failed to group tRNA according to amino acid specificity and did not reveal the tripartite nature of life, probably due to loss of phylogenetic signal or because tRNA diversification predated organismal diversification. Trees of substructures derived from both structural and statistical characters support the origin of tRNA in the acceptor arm and the hypothesis that the top half domain composed of acceptor and pseudouridine (TΨC) arms is more ancient than the bottom half domain composed of dihydrouridine (DHU) and anticodon arms. This constitutes the cornerstone of the genomic tag hypothesis that postulates tRNAs were ancient telomeres in the RNA world. The trees of substructures suggest a model for the evolution of the major functional and structural components of tRNA. In this model, short RNA hairpins with stems homologous to the acceptor arm of present day tRNAs were extended with regions homologous to TΨC and anticodon arms. The DHU arm was then incorporated into the resulting three-stemmed structure to form a proto-cloverleaf structure. The variable region was the last structural addition to the molecular repertoire of evolving tRNA substructures.

Keywords

tRNA Secondary structure Cladistic analysis Molecular evolution 

Supplementary material

239_2007_9050_MOESM1_ESM.pdf (431 kb)
Supplementary material

References

  1. Ancel LW, Fontana W (2000) Plasticity, evolvability, and modularity in RNA. J Exp Zool (Mol Dev Evol) 288:242–283CrossRefGoogle Scholar
  2. Billoud B, Guerrucci MA, Masselot M, Deutsch JS (2000) Cirripede phylogeny using a novel approach: molecular morphometrics. Mol Biol Evol 17:1435–1445PubMedGoogle Scholar
  3. Bloch DP, McArthur B, Mirrop S (1985) tRNA-rRNA sequence homologies: evidence for an ancient modular format shared by tRNAs and rRNAs. Biosystems 17:209–225PubMedCrossRefGoogle Scholar
  4. Bremer K (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795–803CrossRefGoogle Scholar
  5. Bull AT, Goodfellow M, Slater JH (1992) Biodiversity as a source of innovation in biotechnology. Annu Rev Microbiol 46:219–252PubMedCrossRefGoogle Scholar
  6. Caetano-Anollés G (2001) Novel strategies to study the role of mutation and nucleic acid structure in evolution. Plant Cell Tissue Org Cult 67:115–132CrossRefGoogle Scholar
  7. Caetano-Anollés G (2002a) Evolved RNA secondary structure and the rooting of the universal tree of life. J Mol Evol 54:333–345Google Scholar
  8. Caetano-Anollés G (2002b) Tracing the evolution of RNA structure in ribosomes. Nucleic Acids Res 30:2575–2587Google Scholar
  9. Caetano-Anollés G (2005) Grass evolution inferred from chromosomal rearrangements and geometrical and statistical features in RNA structure. J Mol Evol 60:635–652PubMedCrossRefGoogle Scholar
  10. Collins LJ, Moulton V, Penny D (2000) Use of RNA secondary structure for studying the evolution of RNase P and RNase MRP. J Mol Evol 51:194–2004PubMedGoogle Scholar
  11. Dick TP, Schamel WWA (1995) Molecular evolution of transfer RNA from two precursor hairpins: implications for the origin of protein synthesis. J Mol Evol 41:1–9PubMedCrossRefGoogle Scholar
  12. Di Giulio M (1992) On the origin of the transfer RNA molecule. J Theor Biol 159:199–214PubMedCrossRefGoogle Scholar
  13. Di Giulio M (1999) The non-monophyletic origin of the tRNA molecule. J Theor Biol 197:403–414PubMedCrossRefGoogle Scholar
  14. Di Giulio M (2000) The RNA world, the genetic code and the tRNA molecule. Trends Genet 16:17–18PubMedCrossRefGoogle Scholar
  15. Eigen M, Winkler-Oswatitsch R (1981) Transfer-RNA, an early gene? Naturwissenschaften 68:282–292PubMedCrossRefGoogle Scholar
  16. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  17. Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565PubMedCrossRefGoogle Scholar
  18. Fontana W (2002) Modelling ‘evo-devo’ with RNA. BioEssays 24:1164–1177PubMedCrossRefGoogle Scholar
  19. Gladyshev GP, Ershov YA (1982) Principles of the thermodynamics of biological systems. J Theor Biol 94:301–343PubMedCrossRefGoogle Scholar
  20. Goodenbour JM, Pan T (2006) Diversity of tRNA genes in eukaryotes. Nucleic Acids Res 34:6137–6146PubMedCrossRefGoogle Scholar
  21. Gultyaev PA, van Batenburg FHD, Pleij CWA (2002) Selective pressures on RNA hairpins in vivo and in vitro. J Mol Evol 54: 1–8PubMedCrossRefGoogle Scholar
  22. Higgs PG (1993) RNA secondary structure: a comparison of real and random sequences. J Phys I France 3:43–59CrossRefGoogle Scholar
  23. Higgs PG (1995) Thermodynamic properties of transfer RNA: a computational study. J Chem Soc Faraday Trans 91:2531–2540CrossRefGoogle Scholar
  24. Higgs PG (2000) RNA secondary structure: physical and computational aspects. Quarterly Rev Biophys 33:199–253CrossRefGoogle Scholar
  25. Hillis DM, Huelsenbeck JP (1992) Signal, noise, and reliability in molecular phylogenetic analyses. J Hered 83:189–195PubMedGoogle Scholar
  26. Hopfield JJ (1978) Origin of the genetic code: a testable hypothesis based on tRNA structure, sequence, and kinetic proofreading. Proc Natl Acad Sci USA 75:4334–4338PubMedCrossRefGoogle Scholar
  27. Maddison WP, Maddison DR (2003) MacClade 4: analysis of phylogeny and character evolution, version 4.06. Sinauer Associates, Sunderland, MAGoogle Scholar
  28. Maizels N, Weiner AM (1994) Phylogeny from function: evidence from the molecular fossil record that tRNA originated in replication, not translation. Proc Natl Acad Sci USA 91:6729–6734PubMedCrossRefGoogle Scholar
  29. Marck C, Kachouri-Lafond R, Lafontaine I, Westhof E, Dujon B, Grosjean H (2006) The RNA polymerase III-dependent family of genes in hemiascomycetes: comparative RNomics, decoding strategies, transcription and evolutionary implications. Nucleic Acids Res 34:1816–1835PubMedCrossRefGoogle Scholar
  30. Marlière P (1983) Computer building and folding of fictitious transfer-RNA sequences. Biochimie 65:267–273PubMedCrossRefGoogle Scholar
  31. Martinis SA, Schimmel P (1995) Small RNA oligonucleotide substrate for specific aminoacylations. In: Söll D, RajBandary V (eds) tRNA: structure, biosynthesis, and function. ASM Press, Washington, DC, pp 349–370Google Scholar
  32. Muller AWJ (2005) Thermosynthesis as energy source for the RNA world: a model for the bioenergetics of the origin of life. Biosystems 82:93–102PubMedCrossRefGoogle Scholar
  33. Nagaswamy U, Fox G (2003) RNA ligation and the origin of tRNA. Origins Life Evol B 33:199–209CrossRefGoogle Scholar
  34. Pollock D (2003) The Zuckerkandl Prize: structure and evolution. J Mol Evol 56:375–376Google Scholar
  35. Randau L, Münch R, Hohn MJ, Jahn D, Söll D (2005) Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5′- and 3′-halves. Nature 433:537–541PubMedCrossRefGoogle Scholar
  36. Rodin S, Ohno S, Rodin A (1993) Transfer RNAs with complementary anticodons: Could they reflect early evolution of discriminative genetic code adaptors? Proc Natl Acad Sci USA 90:4723–4727PubMedCrossRefGoogle Scholar
  37. Rodin S, Rodin A, Ohno S (1996) The presence of codon-anticodon pairs in the acceptor stem of tRNAs. Proc Natl Acad Sci USA 93:4537–4542PubMedCrossRefGoogle Scholar
  38. Rodin SN, Rodin AS (2006a) Origin of the genetic code: first aminoacyl-tRNA systhetases could replace isofunctional ribozymes when only the second base of codons was established. DNA Cell Biol 25:365–375Google Scholar
  39. Rodin SN, Rodin AS (2006b) Partitioning of aminoacyl-tRNA synthetases in two classes could have been coded in a strand-symmetric RNA world. DNA Cell Biol 25:617–626Google Scholar
  40. Schimmel P, Giegé R, Moras D, Yokoyama S (1993) An operational RNA code for amino acids and possible relationship to genetic code. Proc Natl Acad Sci USA 90:8763–8768PubMedCrossRefGoogle Scholar
  41. Schimmel P, Ribas de Pouplana L (1995) Transfer RNA: from minihelix to genetic code. Cell 81:983–986PubMedCrossRefGoogle Scholar
  42. Schultes EA, Bartel DP (2000) One sequence, two ribozymes: implications for the emergence of new ribozyme folds. Science 289:448–452PubMedCrossRefGoogle Scholar
  43. Schultes EA, Hraber PT, LaBean TH (1999) Estimating the contributions of selection and self-organization in RNA secondary structure. J Mol Evol 49:76–83PubMedCrossRefGoogle Scholar
  44. Selmer M, Dunham CM, Murphy FV IV, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313:1935–1942PubMedCrossRefGoogle Scholar
  45. Shi H, Moore PB (2000) The crystal structure of yeast phenylalanine tRNA at 1.93 Å resolution: a classic structure revisited. RNA 6:1091–1105PubMedCrossRefGoogle Scholar
  46. Sprinzl M, Vassilenko KS (2005) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 33:D139–D140PubMedCrossRefGoogle Scholar
  47. Steel M, Penny D (2000) Parsimony, likelihood, and the role of models in molecular phylogenetics. Mol Biol Evol 17:839–850PubMedGoogle Scholar
  48. Steffens W, Digby D (1999) mRNA have greater negative folding free energies than shuffled or codon choice randomized sequences. Nucleic Acids Res 27:1578–1584CrossRefGoogle Scholar
  49. Stegger G, Hofman H, Fortsch J, Gross HJ, Randles JW, Sanger HL, Riesner D (1984) Conformational transitions in viroids and virusoids: comparison of results from energy minimization algorithm and from experimental data. J Biomol Struct Dynam 2:543–571Google Scholar
  50. Steinberg S, Misch A, Sprinzl M (1993) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 21:3011–3015PubMedCrossRefGoogle Scholar
  51. Sun F-J, Fleurdépine S, Bousquet-Antonelli C, Caetano-Anollés G, Deragon J-M (2007) Common evolutionary trends for tRNA-derived SINE RNA structures. Trends Genet 23:26–33PubMedCrossRefGoogle Scholar
  52. Swain TD, Taylor DJ (2003) Structural rRNA characters support monophyly of raptorial limbs and paraphyly of limb specialization in water fleas. Proc R Soc London B 270:887–896CrossRefGoogle Scholar
  53. Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods), version 4.0b10. Sinauer Associates, Sunderland, MAGoogle Scholar
  54. Szathmáry E (1999) The origin of the genetic code: amino acids as cofactors in an RNA world. Trends Genet 15:223–229PubMedCrossRefGoogle Scholar
  55. Tanaka T, Kikuchi Y (2001) Origin of the cloverleaf shape of transfer RNA - the double-hairpin model: implication for the role of tRNA intron and the long extra loop. Viva Origino 29:134–142Google Scholar
  56. Wang M, Caetano-Anollés G (2006) Global phylogeny determined by the combination of protein domains in proteomes. Mol Biol Evol 23:2444–2454PubMedCrossRefGoogle Scholar
  57. Wang M, Yafremava LS, Caetano-Anollés D, Mittenthal JE, Caetano-Anollés G (2007) Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. Genome Res 17:1572–1585Google Scholar
  58. Weiner AM, Maizels N (1987) tRNA-like structures tag the 3′ ends of genomic RNA moleculesfor replication: implications for the origin of protein synthesis. Proc Natl Acad Sci USA 84:7383–7387PubMedCrossRefGoogle Scholar
  59. Weiner AM, Maizels N (1999) The genomic tag hypothesis: modern viruses as molecular fossils of ancient strategies for genomic replication, and clues regarding the origin of protein synthesis. Biol Bull 196:327–330PubMedCrossRefGoogle Scholar
  60. Widmann J, Di Giulio M, Yarus M, Knight R (2005) tRNA creation by hairpin duplication. J Mol Evol 61:524–535PubMedCrossRefGoogle Scholar
  61. Woese CR (1969) The biological significance of the genetic code. Prog Mol Subcell Biol 1:5–46Google Scholar
  62. Yusupov MM, Yusupov GZ, Baucom A, Lieberman K, Earnest TN, Cate JHD, Noller HF (2001) Crystal structure of the ribosome at 5.5 Å resolution. Science 292:883–895PubMedCrossRefGoogle Scholar
  63. Zhu W, Freeland S (2006) The standard genetic code enhances adaptive evolution of proteins. J Theor Biol 239:63–70PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Department of Crop SciencesUniversity of Illinois at Urbana-ChampaignUrbanaUSA

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