Journal of Molecular Evolution

, Volume 43, Issue 3, pp 216–223 | Cite as

A relationship between GC content and coding-sequence length

  • José L. Oliver
  • Antonio Marín
Article

Abstract

Since base composition of translational stop codons (TAG, TAA, and TGA) is biased toward a low G+C content, a differential density for these termination signals is expected in random DNA sequences of different base compositions. The expected length of reading frames (DNA segments of sense codons flanked by in-phase stop codons) in random sequences is thus a function of GC content. The analysis of DNA sequences from several genome databases stratified according to GC content reveals that the longest coding sequences—exons in vertebrates and genes in prokaryotes—are GC-rich, while the shortest ones are GC-poor. Exon lengthening in GC-rich vertebrate regions does not result, however, in longer vertebrate proteins, perhaps because of the lower number of exons in the genes located in these regions. The effects on coding-sequence lengths constitute a new evolutionary meaning for compositional variations in DNA GC content.

Key words

Base composition Stop-codon density Coding-sequence length Compositional heterogeneity 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bernardi G (1989) The isochore organization of the human genome. Annu Rev Genet 23:637–661CrossRefPubMedGoogle Scholar
  2. Bernardi G (1993) The isochore organization of the human genome and its evolutionary history—a review. Gene 135:57–66PubMedGoogle Scholar
  3. Bernardi G (1995) The human genome: organization and evolutionary story. Annu Rev Genet 29:445–476CrossRefPubMedGoogle Scholar
  4. Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G, Meunier-Rotival M, Rodier F (1985) The mosaic genome of warm-blooded vertebrates. Science 228:953–958PubMedGoogle Scholar
  5. Blake C (1983) Exons—present from the beginning? Nature 306:535–537CrossRefPubMedGoogle Scholar
  6. Blake C (1985) Exons and the evolution of proteins. Int Rev Cytol 93:149–185PubMedGoogle Scholar
  7. Boldögkoi Z, Murvai J, Fodor I (1995) G and C accumulation at silent positions of codons produces additional ORFs. Trends Genet 11: 125–126PubMedGoogle Scholar
  8. Cebrat S, Dudek MR (1996) Generation of overlapping reading frames. Trends Genet 12:12CrossRefPubMedGoogle Scholar
  9. D'Onofrio G, Bernardi G (1992) A universal compositional correlation among codon positions. Gene 110:81–88CrossRefPubMedGoogle Scholar
  10. Duret L, Mouchiroud D, Gautier C (1995) Statistical analysis of vertebrate sequences reveals that long genes are scarce in GC-rich isochores. J Mol Evol 40:308–317CrossRefPubMedGoogle Scholar
  11. Fleischmann RD et al. (1995) Whole-genome random sequencing and assembly ofHaemophilus influenzae Rd. Science 269:496–512PubMedGoogle Scholar
  12. Fraser CM et al. (1995) The minimal gene complement ofMycoplasma genitalium. Science 270:397–403PubMedGoogle Scholar
  13. Guigó R, Fickett JW (1995) Distinctive sequence features in protein coding, genic non-coding, and intergenic human DNA. J Mol Biol 253:51–60CrossRefPubMedGoogle Scholar
  14. Hawkins JD (1988) A survey on imron and exon lengths. Nucleic Acids Res 16:9893–9908PubMedGoogle Scholar
  15. Höglund M, Säll T, Röhme D (1990) On the origin of coding sequences from random open reading frames. J Mol Evol 30:104–108CrossRefGoogle Scholar
  16. Holland SK, Blake CCF (1990) Proteins, exons, and molecular evolution. In: Stone EM, Schwartz RJ (eds) Intervening sequences in evolution and development. Oxford University Press, New York, p 32Google Scholar
  17. Holmquist GP (1989) Evolution of chromosome bands: molecular ecology of noncoding DNA. J Mol Evol 28:469–486PubMedGoogle Scholar
  18. Hughes AL, Hughes MK (1995) Small genomes for better flyers. Nature 377:391CrossRefPubMedGoogle Scholar
  19. Merino E, Balbás P, Puente JL, Bolivar F (1994) Antisense overlapping open reading frames in genes from bacteria to humans. Nucleic Acids Res 22:1903–1908PubMedGoogle Scholar
  20. Naora H, Miyahara K, Curnow RN (1987) Origin of non coding DNA sequences: molecular fossils of genome evolution. Proc Natl Acad Sci USA 84:6195–6199PubMedGoogle Scholar
  21. Nomura M, Sor F, Yamagishi M, Lawson M (1987) Heterogeneity of GC content within a single bacterial genome and its implications for evolution. Cold Spring Harb Symp Quant Biol 52:658–663Google Scholar
  22. Perrière G, Gouy M, Gojobori T (1994) NRSub: a non-redundant data base for theBacillus subtilis genome. Nucleic Acids Res 22:5525–5529PubMedGoogle Scholar
  23. Poole ES, Brown CM, Tate WP (1995) The identity of the base following the stop codon determines the efficiency ofin vitro translational termination inEscherichia coli. EMBO J 14:151–158PubMedGoogle Scholar
  24. Seidel HM, Pompliano DL, Knowles JR (1992) Exons as microgenes? Science 257:1489–1490PubMedGoogle Scholar
  25. Senapathy P (1986) Origin of eukaryotic introns: a hypothesis, based on codon distribution statistics in genes, and its implications. Proc Natl Acad Sci USA 83:2133–2137PubMedGoogle Scholar
  26. Senapathy P (1988) Possible evolution of splice-junction signals in eukaryotic genes from stop codons. Proc Natl Acad Sci USA 85: 1129–1133PubMedGoogle Scholar
  27. Senapathy P (1995) Introns and the origin of protein-coding genes. Science 268:1366–1367PubMedGoogle Scholar
  28. Senapathy P, Shapiro MB, Harris NL (1990) Splice junctions, branch point sites, and exons: sequence statistics, identification, and applications to genome project. Methods Enzymol 183:252–278PubMedGoogle Scholar
  29. Sharp PM, Burgess CJ, Lloyd AT, Mitchell KJ (1992) Selective use of termination codons and variations in codon choice. In: Hatfield DL, Lee BL Pirtle RM (eds) Transfer RNA in protein synthesis. CRC Press, Boca Raton, pp 398–425Google Scholar
  30. Smith MW (1988) Structure of vertebrate genes: a statistical analysis implicating selection. J Mol Evol 27:45–55CrossRefPubMedGoogle Scholar
  31. Stoehr PJ, Cameron ON (1991) The EMBL data library. Nucleic Acids Res (Suppl) 19:2227–2230Google Scholar
  32. Stoltzfus A, Spencer DF, Zuker M, Logsdon JM, Doolittle WF (1995) Introns and the origin of protein-coding genes (response). Science 268:1367–1369Google Scholar
  33. Sueoka N (1992) Directional mutation pressure, selection constraints, and genetic equilibria. J Mol Evol 34:95–114CrossRefPubMedGoogle Scholar
  34. Traut TW (1988) Do exons code for structural or functional units in proteins? Proc Natl Acad Sci USA 85:2944–2948PubMedGoogle Scholar
  35. Wahl R, Rice P, Rice CM, Kröger M (1994) ECD—a totally integrated database ofEscherichia coli K12. Nucleic Acids Res 22:3450–3455PubMedGoogle Scholar
  36. White SH, Jacobs RE (1993) The evolution of proteins from random amino acid sequences. 1. Evidence from the lengthwise distribution of amino acids in modem protein sequences. J Mol Evol 36:79–95PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1996

Authors and Affiliations

  • José L. Oliver
    • 1
  • Antonio Marín
    • 2
  1. 1.Departamento de Genética, Instituto de Biotecnologfa, Facultad de CienciasUniversidad de GranadaGranadaSpain
  2. 2.Departamento de Genética, Facultad de BiologfaUniversidad de SevillaSevillaSpain

Personalised recommendations