Advertisement

Journal of Molecular Evolution

, Volume 34, Issue 6, pp 471–477 | Cite as

Statistical evidence for remnants of the primordial code in the acceptor stem of prokaryotic transfer RNA

  • W. Möller
  • G.M.C. Janssen
Article

Summary

The specificity of interaction of amino acids with triplets in the acceptor helix stem of tRNA was investigated by means of a statistical analysis of 1400 tRNA sequences. The imprint of a prototypic genetic code at position 3–5 of the acceptor helix was detected, but only for those major amino acids, glycine, alanine, aspartic acid, and valine, that are formed by spark discharges of simple gases in the laboratory. Although remnants of the code at position 3–5 are typical for tRNAs of archaebacteria, eubacteria, and chloroplasts, eukaryotes do not seem to contain this code, and mitochondria take up an intermediary position. A duplication mechanism for the transposition of the original 3–5 code toward its present position in the anticodon stern of tRNA is proposed. From this viewpoint, the mode of evolution of mRNA and functional ribosomes becomes more understandable.

Key words

Transfer RNA Acceptor helix stem Primordial code Statistics 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Amons R, Van Agthoven A, Pluijms W, Möller W, Higo K, Itoh T, Osawa S (1977) A comparison of the amino-terminal sequence of the L7/L 12-type proteins of Artemia salina and Saccharomyces cerevisiae. FEBS Lett 81:308–310Google Scholar
  2. Auer J, Lechner K, Böck A (1989) Gene organization and structure of two transcriptional units from Methanococcus coding for ribosomal proteins and elongation factors. Can J Microbiol 35:200–204Google Scholar
  3. Burbaum JJ, Schimmel P (1991) Structural relationships and the classification of aminoacyl-tRNA synthetases. J Biol Chem 266:16965–16968Google Scholar
  4. Crick FHC (1968) The origin of the genetic code. J Mol Biol 38:367–379Google Scholar
  5. Cusack S, Berthet-Colominas C, Härtlein M, Nassar N, Leberman, R (1990) A second class of synthetase structure revealed by X-ray analysis of Escherichia coli seryl-tRNA synthetase at 2.5 Å. Nature 347:249–255Google Scholar
  6. Darnell JE, Doolittle WF (1986) Speculations on the early course of evolution. Proc Natl Acad Sci USA 83:1271–1275Google Scholar
  7. De Duve C (1988) The second genetic code. Nature 333:117–118Google Scholar
  8. Eigen M, Schuster P (1978) The hypercycle: a principle of natural self-organization; part C: the realistic hypercycle. Naturwissenschaften 65:341–369Google Scholar
  9. Eigen M, Winkler-Oswatitsch R (1981a) Transfer-RNA, an early gene? Naturwissenschaften 68:282–292Google Scholar
  10. Eigen M, Winkler-Oswatitsch R (1981b) Transfer-RNA: the early adaptor Naturwissenschaften 68:217–228Google Scholar
  11. Eriani G, Delarue M, Poch O, Gangloff J, Moras D (1990) Partition of tRNA synthetases ito two classes based on mutually exclusive sets of sequence motifs. Nature 347:203–206Google Scholar
  12. Goodman HM, Olson MV, Hall BD (1977) Nucleotide sequence of a mutant eukaryotic gene: the yeast tyrosine-inserting ochre suppressor SUP4-o. Proc Natl Acad Sci USA 74:5453–5457Google Scholar
  13. Goodman R (1964) Modern statistics. Arc Books, New YorkGoogle Scholar
  14. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849–857Google Scholar
  15. Hou YM, Schimmel P (1988) A simple structural feature is a major determinant of the identity of a transfer RNA. Nature 333:140–145Google Scholar
  16. Inoue T, Orgel LE (1983) A nonenzymatic RNA polymerase model. Science 219:859–862Google Scholar
  17. Joyce GF (1989) RNA evolution and the origin of life. Nature 338:217–224Google Scholar
  18. Jukes TH, Osawa S (1991) Recent evidence for evolution of the genetic code. In: Osawa S, Honjo T (eds) Evolution of life. Springer, Tokyo, pp 79–95Google Scholar
  19. Jungck JR (1978) The genetic code as a periodic table. J Mol Evol 11:211–224Google Scholar
  20. Kim SH, Suddath FL, Quigley GJ, McPherson A, Sussman JL, Wang A, Seeman NC, Rich A (1974) The three-dimensional structure of transfer RNA. Science 185:435–440Google Scholar
  21. Kvenvolden KA, Lawless J, Pering K, Peterson E, Flores J, Ponnamperuma C, Kaplan IR, Moore C (1970) Evidence for extraterrestrial amino acids and hydrocarbons in the Murchison meteorite. Nature 288:923–926Google Scholar
  22. Matheson AT, Möller W, Amons R, Yaguchi M (1980) Comparative studies on the structure of ribosomal proteins with emphasis on the alanine-rich, acidic ribosomal ‘A’ protein. In: Chambliss G, Craven GR, Davies J, Davis K, Kahan L, Nomura M (eds) Ribosomes; structure, function and genetics. University Park Press, Baltimore, pp 297–332Google Scholar
  23. Miller SL (1986) Current status of the prebiotic synthesis of small molecules. Chem Scr 26B:5–11Google Scholar
  24. Möller W, Janssen GMC (1990) Transfer RNAs for primordial amino acids contain remnants of a primitive code at position 3 to 5. Biochimie 72:361–368Google Scholar
  25. Musier-Forsyth K, Scaringe S, Usman N, Schimmel P (1991a) Enzymatic aminoacylation of single stranded RNA with an RNA cofactor. Proc Natl Acad Sci USA 88:209–213Google Scholar
  26. Musier-Forsyth K, Usman N, Scaringe S, Doudna J, Green R, Schimmel P (1991b) Specificity for aminoacylation of an RNA helix: an unpaired, exocyclic amino group in the minor groove. Science 253:784–786Google Scholar
  27. Ramirez C, Shimmin LC, Newton CH, Matheson AT, Denis PP (1989) Structure and evolution of the L11, L1, L10 and L12 equivalent ribosomal proteins in eubacteria, archaebacteria and eukaryotes. Can J Microbiol 35:234–244Google Scholar
  28. Rould MA, Perona JJ, Söll D, Steitz TA (1989) Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNAgln and ATP at 2.8 Å resolution. Science 246:1135–1142Google Scholar
  29. Schopf JW, Packer BM (1987) Early archean (3.3-billion to 3.5-billion-year-old) microfossils from Warrawoona group, Australia. Science 237:70–72Google Scholar
  30. Shimmin LC, Newton CH, Ramirez C, Yee J, Downing WL, Louie KA, Matheson AT, Dennis PP (1989) Organization of genes encoding L11, L1, L10 and L12 equivalent: ribosomal proteins in eubacteria, archaebacteria and eukaryotes. Can J Microbiol 35:164–170Google Scholar
  31. Sprinzl M, Hartmann T, Weber J, Blank J, Zeidler R (1989) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 17:r1-r172Google Scholar
  32. Valenzuela P, Venegas A, Weinberg F, Bishop R, Rutter WJ (1978) Structure of yeast phenylalanine-tRNA genes: an intervening DNA segment within the region coding for the tRNA. Proc Natl Acad Sci USA 75:190–194Google Scholar
  33. Vidal G (1984) The oldest eukaryotic cells. Sci Am 250:32–41Google Scholar
  34. Winkler-Oswatitsch R, Dress A, Eigen M (1986) Comparative sequence analysis, exemplified with tRNA and 5S rRNA. Chem Scr 26B:59–66Google Scholar
  35. Woese CR (1989) Bacterial evolution. Microbiol Rev 51(2):221–271Google Scholar
  36. Wong JTF (1988) Evolution of the genetic code. Microbiol Sci 5:174–181Google Scholar
  37. Yarus M (1988) A specific amino acid binding site composed of RNA. Science 240:1751–1758Google Scholar

Copyright information

© Springer-Verlag New York Inc 1992

Authors and Affiliations

  • W. Möller
    • 1
  • G.M.C. Janssen
    • 1
  1. 1.Department of Medical BiochemistryState University of LeidenRA LeidenThe Netherlands

Personalised recommendations