Journal of Molecular Evolution

, Volume 34, Issue 1, pp 45–53 | Cite as

Exons encoding the highly conserved part of human glutaminyl-tRNA synthetase

  • Eva Kaiser
  • Dirk Eberhard
  • Rolf Knippers
Article

Summary

Aminoacyl-tRNA synthetases are important components of the genetic apparatus. In spite of common catalytic properties, synthetases with different amino acid specificities are widely diverse in their primary structures, subunit sizes, and subunit composition. However, synthetases with given amino acid specificities are well conserved throughout evolution. We have been studying the human glutaminyl-tRNA synthetase possessing a sequence of about 400 amino acid residues (the core region) that is very similar to sequences in the corresponding enzymes from bacteria and yeast. The conserved sequence appears to be essential for the basic function of the enzyme, the charging of tRNA with glutamine. As a first step to a better understanding of the evolution of this enzyme, we determined the coding region for the conserved part of the human glutaminyl-tRNA synthetase. The coding region is composed of eight exons. It appears that individual exons encode defined secondary structural elements as parts of functionally important domains of the enzyme. Evolution of the gene by assembly of individual exons seems to be a viable hypothesis; alternative pathways are discussed.

Key words

Aminoacyl-tRNA synthetases Human glutaminyl-tRNA synthetase Exon Secondary structure elements Functional domains Core region 

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References

  1. Baron M, Norman DG, Campbell ID (1991) Protein modules. Trends Biochem Sci 16:13–17Google Scholar
  2. Blake CC (1983) Exons—present from the beginning? Nature 306:535–537Google Scholar
  3. Cavalier-Smith T (1991) Intron phylogeny: anew hypothesis. Trends Genet 7:145–148Google Scholar
  4. Chou PY, Fasman GD (1978) Empirical predictions of protein conformation. Annu Rev Biochem 47:251–276Google Scholar
  5. Cusack S, Berthet-Colominas C, Härtlein M, Nassar N, Lebermann 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. Dorit RL, Schoenbach L, Gilbert W (1990) How big is the universe of exons? Science 250:1377–1382Google Scholar
  7. Eriani G, Delarue M, Poch O, Gangloff J, Moras D (1990) Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature 347:203–206Google Scholar
  8. Fett R, Knippers R (1991) The primary structure of human glutaminyl-tRNA synthetase. A highly conserved “core region,” amino acid repeat regions, and homologies with translation elongation factors. J Biol Chem 266:1448–1455Google Scholar
  9. Gilbert W (1978) Why genes in pieces? Nature 271:501Google Scholar
  10. Gilbert W (1987) The exon theory of genes. Cold Spring Harbor Symp Quant Biol 52:901–905Google Scholar
  11. Go M, Nosaka M (1987) Protein architecture and the origins of introns. Cold Spring Harbor Symp Quant Biol 52:915–924Google Scholar
  12. Godar DE, Godar DE, Garcia V, Jacobo LA, Aebi U, Yang DCH (1988) Structural organization of the multienzyme complex of mammalian aminoacyl-tRNA synthetases. Biochemistry 27:6921–6928Google Scholar
  13. Hawkins JD (1988) A survey on intron and exon length. Nucleic Acids Res 16:9893–9908Google Scholar
  14. Innis MA, Gelfand DH, Sninsky JJ, White TJ (1990) PCR protocols. A guide to methods and applications. Academic Press, New YorkGoogle Scholar
  15. Kunze N, Bittler E, Fett R, Schray B, Hameister H, Wiedorn KH, Knippers R (1990) The human QARS locus: assignment of the human gene for glutaminyl-tRNA synthetase to chromosome 1q32–42. Hum Genet 85:527–530Google Scholar
  16. Ludmerer SW, Schimmel P (1987) Gene for yeast glutamine tRNA synthetase encodes a large amino-terminal extension and provides a strong confirmation of the signature sequence for a group of the aminoacyl-tRNA synthetases. J Biol Chem 262:10801–10806Google Scholar
  17. Maniatis T, Sambrook J, Fritsch EF (1982) Molecular cloning. A laboratory handbook. Cold Spring Harbor Laboratories, Cold Spring Harbor NYGoogle Scholar
  18. Norcum MT (1989) Isolation and electron microscopic characterization of the high molecular weight mass aminoacyl-tRNA synthetase complex from murine erythroleukemia cells. J Biol Chem 264:15043–15051Google Scholar
  19. Patthy L (1987) Intron-dependent evolution: preferred types of exons and introns. FEBS Lett 214:1–7Google Scholar
  20. Rogers JH (1990) The role of introns in evolution. FEBS Lett 268:339–343Google Scholar
  21. Rould MA, Perona JJ, Söll D, Steitz TA (1989) Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNAGla and ATP at 2.8 Å resolution. Science 246:1135–1142Google Scholar
  22. Sanger F, Nicklen S, Coulsen AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467Google Scholar
  23. Schimmel P (1987) Aminoacyl-tRNA synthetases: general scheme of structure-function relationships in the polypeptides and recognition of tRNAs. Annu Rev Biochem 56:125–158Google Scholar
  24. Schimmel P (1991) Classes ofaminoacyl-tRNA synthetases and the establishment of the genetic code. Trends Biochem Sci 16:1–3Google Scholar
  25. Schray B, Thömmes P, Knippers R (1990) Glutaminyl-tRNA synthetase as a component of the high-molecular weight complex of human aminoacyl-tRNA synthetases. An immunological study. Biochim Biophys Acta 1087:226–234Google Scholar
  26. Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517Google Scholar
  27. Thömmes P, Fett R, Schray B, Kunze N, Knippers R (1988) The core region of human glutaminyl-tRNA synthetase. Homologies with the Escherichia coli and yeast enzyme. Nucleic Acids Res 16:5391–5406Google Scholar
  28. Traut TW (1988) Do exons code for structural or functional units in proteins? Proc Natl Acad Sci USA 85:2944–2948Google Scholar
  29. Uemura H, Conley J, Yamao F, Roger J, Söll D (1988) Escherichia coli glutaminyl-tRNA synthetase: a single amino acid replacement relaxes tRNA specificity. Protein Sequences & Data Anal 1:479–485Google Scholar

Copyright information

© Springer-Verlag New York Inc 1992

Authors and Affiliations

  • Eva Kaiser
    • 1
  • Dirk Eberhard
    • 2
  • Rolf Knippers
    • 1
  1. 1.Fakultät für BiologieUniversität KonstanzKonstanzGermany
  2. 2.Deutsches Krebsforschungszentrum Im Neuenheimer FeldHeidelbergGermany

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