Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1980 Jan 11;8(1):r49–r62. doi: 10.1093/nar/8.1.197-c

Codon catalog usage and the genome hypothesis.

R Grantham, C Gautier, M Gouy, R Mercier, A Pavé
PMCID: PMC327256  PMID: 6986610

Abstract

Frequencies for each of the 61 amino acid codons have been determined in every published mRNA sequence of 50 or more codons. The frequencies are shown for each kind of genome and for each individual gene. A surprising consistency of choices exists among genes of the same or similar genomes. Thus each genome, or kind of genome, appears to possess a "system" for choosing between codons. Frameshift genes, however, have widely different choice strategies from normal genes. Our work indicates that the main factors distinguishing between mRNA sequences relate to choices among degenerate bases. These systematic third base choices can therefore be used to establish a new kind of genetic distance, which reflects differences in coding strategy. The choice patterns we find seem compatible with the idea that the genome and not the individual gene is the unit of selection. Each gene in a genome tends to conform to its species' usage of the codon catalog; this is our genome hypothesis.

Full text

PDF
r49

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beck E., Sommer R., Auerswald E. A., Kurz C., Zink B., Osterburg G., Schaller H., Sugimoto K., Sugisaki H., Okamoto T. Nucleotide sequence of bacteriophage fd DNA. Nucleic Acids Res. 1978 Dec;5(12):4495–4503. doi: 10.1093/nar/5.12.4495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bernard O., Hozumi N., Tonegawa S. Sequences of mouse immunoglobulin light chain genes before and after somatic changes. Cell. 1978 Dec;15(4):1133–1144. doi: 10.1016/0092-8674(78)90041-7. [DOI] [PubMed] [Google Scholar]
  3. Charnay P., Mandart E., Hampe A., Fitoussi F., Tiollais P., Galibert F. Localization on the viral genome and nucleotide sequence of the gene coding for the two major polypeptides of the hepatitis B surface antigen (HBs Ag). Nucleic Acids Res. 1979 Sep 25;7(2):335–346. doi: 10.1093/nar/7.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dhar R., Seif I., Khoury G. Nucleotide sequence of the BK virus DNA segment encoding small t antigen. Proc Natl Acad Sci U S A. 1979 Feb;76(2):565–569. doi: 10.1073/pnas.76.2.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Efstratiadis A., Kafatos F. C., Maniatis T. The primary structure of rabbit beta-globin mRNA as determined from cloned DNA. Cell. 1977 Apr;10(4):571–585. doi: 10.1016/0092-8674(77)90090-3. [DOI] [PubMed] [Google Scholar]
  6. Escarmis C., Sastry P. A., Billeter M. A. Determination of the first half of the coat protein cistron of bacteriophage Qbeta as an application of a mapping procedure for RNA fragments. J Biol Chem. 1978 Dec 10;253(23):8390–8399. [PubMed] [Google Scholar]
  7. Farabaugh P. J. Sequence of the lacI gene. Nature. 1978 Aug 24;274(5673):765–769. doi: 10.1038/274765a0. [DOI] [PubMed] [Google Scholar]
  8. Fiddes J. C., Goodman H. M. Isolation, cloning and sequence analysis of the cDNA for the alpha-subunit of human chorionic gonadotropin. Nature. 1979 Oct 4;281(5730):351–356. doi: 10.1038/281351a0. [DOI] [PubMed] [Google Scholar]
  9. Fiddes J. C. The nucleotide sequence of a viral DNA. Sci Am. 1977 Dec;237(6):54–67. doi: 10.1038/scientificamerican1277-54. [DOI] [PubMed] [Google Scholar]
  10. Fiers W., Contreras R., Duerinck F., Haegeman G., Iserentant D., Merregaert J., Min Jou W., Molemans F., Raeymaekers A., Van den Berghe A. Complete nucleotide sequence of bacteriophage MS2 RNA: primary and secondary structure of the replicase gene. Nature. 1976 Apr 8;260(5551):500–507. doi: 10.1038/260500a0. [DOI] [PubMed] [Google Scholar]
  11. Fiers W., Contreras R., Duerinck F., Haegmean G., Merregaert J., Jou W. M., Raeymakers A., Volckaert G., Ysebaert M., Van de Kerckhove J. A-protein gene of bacteriophage MS2. Nature. 1975 Jul 24;256(5515):273–278. doi: 10.1038/256273a0. [DOI] [PubMed] [Google Scholar]
  12. Fiers W., Contreras R., Haegemann G., Rogiers R., Van de Voorde A., Van Heuverswyn H., Van Herreweghe J., Volckaert G., Ysebaert M. Complete nucleotide sequence of SV40 DNA. Nature. 1978 May 11;273(5658):113–120. doi: 10.1038/273113a0. [DOI] [PubMed] [Google Scholar]
  13. Garel J. P. Functional adaptation of tRNA population. J Theor Biol. 1974 Jan;43(1):211–225. doi: 10.1016/s0022-5193(74)80054-8. [DOI] [PubMed] [Google Scholar]
  14. Godson G. N., Barrell B. G., Staden R., Fiddes J. C. Nucleotide sequence of bacteriophage G4 DNA. Nature. 1978 Nov 16;276(5685):236–247. doi: 10.1038/276236a0. [DOI] [PubMed] [Google Scholar]
  15. Grantham R. Viral, prokaryote and eukaryote genes contrasted by mRNA sequence indexes. FEBS Lett. 1978 Nov 1;95(1):1–11. doi: 10.1016/0014-5793(78)80041-6. [DOI] [PubMed] [Google Scholar]
  16. Grosschedl R., Schwarz E. Nucleotide sequence of the cro-cII-oop region of bacteriophage 434 DNA. Nucleic Acids Res. 1979 Mar;6(3):867–881. doi: 10.1093/nar/6.3.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gubbins E. J., Maurer R. A., Hartley J. L., Donelson J. E. Construction and analysis of recombinant DNAs containing a structural gene for rat prolactin. Nucleic Acids Res. 1979 Mar;6(3):915–930. doi: 10.1093/nar/6.3.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Guilley H., Briand J. P. Nucleotide sequence of turnip yellow mosaic virus coat protein mRNA. Cell. 1978 Sep;15(1):113–122. doi: 10.1016/0092-8674(78)90087-9. [DOI] [PubMed] [Google Scholar]
  19. Guilley H., Jonard G., Kukla B., Richards K. E. Sequence of 1000 nucleotides at the 3' end of tobacco mosaic virus RNA. Nucleic Acids Res. 1979 Apr;6(4):1287–1308. doi: 10.1093/nar/6.4.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hamlyn P. H., Browniee G. G., Cheng C. C., Gait M. J., Milstein C. Complete sequence of constant and 3' noncoding regions of an immunoglobulin mRNA using the dideoxynucleotide method of RNA sequencing. Cell. 1978 Nov;15(3):1067–1075. doi: 10.1016/0092-8674(78)90290-8. [DOI] [PubMed] [Google Scholar]
  21. Heindell H. C., Liu A., Paddock G. V., Studnicka G. M., Salser W. A. The primary sequence of rabbit alpha-globin mRNA. Cell. 1978 Sep;15(1):43–54. doi: 10.1016/0092-8674(78)90081-8. [DOI] [PubMed] [Google Scholar]
  22. Hensgens L. A., Grivell L. A., Borst P., Bos J. L. Nucleotide sequence of the mitochondrial structural gene for subunit 9 of yeast ATPase complex. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1663–1667. doi: 10.1073/pnas.76.4.1663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hulsebos T., Schoenmakers J. G. Nucleotide sequence of gene VII and of a hypothetical gene (IX) in bacteriophage M13. Nucleic Acids Res. 1978 Dec;5(12):4677–4698. doi: 10.1093/nar/5.12.4677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jonard G., Richards K., Mohier E., Gerlinger P. Nucleotide sequence at the 5' extremity of tobacco-mosaic-virus RNA. 2. The coding region (nucleotides 69-236). Eur J Biochem. 1978 Mar 15;84(2):521–531. doi: 10.1111/j.1432-1033.1978.tb12195.x. [DOI] [PubMed] [Google Scholar]
  25. Konkel D. A., Tilghman S. M., Leder P. The sequence of the chromosomal mouse beta-globin major gene: homologies in capping, splicing and poly(A) sites. Cell. 1978 Dec;15(4):1125–1132. doi: 10.1016/0092-8674(78)90040-5. [DOI] [PubMed] [Google Scholar]
  26. Marotta C. A., Wilson J. T., Forget B. G., Weissman S. M. Human beta-globin messenger RNA. III. Nucleotide sequences derived from complementary DNA. J Biol Chem. 1977 Jul 25;252(14):5040–5053. [PubMed] [Google Scholar]
  27. Martial J. A., Hallewell R. A., Baxter J. D., Goodman H. M. Human growth hormone: complementary DNA cloning and expression in bacteria. Science. 1979 Aug 10;205(4406):602–607. doi: 10.1126/science.377496. [DOI] [PubMed] [Google Scholar]
  28. McReynolds L., O'Malley B. W., Nisbet A. D., Fothergill J. E., Givol D., Fields S., Robertson M., Brownlee G. G. Sequence of chicken ovalbumin mRNA. Nature. 1978 Jun 29;273(5665):723–728. doi: 10.1038/273723a0. [DOI] [PubMed] [Google Scholar]
  29. Min Jou W., Haegeman G., Ysebaert M., Fiers W. Nucleotide sequence of the gene coding for the bacteriophage MS2 coat protein. Nature. 1972 May 12;237(5350):82–88. doi: 10.1038/237082a0. [DOI] [PubMed] [Google Scholar]
  30. Nakanishi S., Inoue A., Kita T., Nakamura M., Chang A. C., Cohen S. N., Numa S. Nucleotide sequence of cloned cDNA for bovine corticotropin-beta-lipotropin precursor. Nature. 1979 Mar 29;278(5703):423–427. doi: 10.1038/278423a0. [DOI] [PubMed] [Google Scholar]
  31. Osterman L. A. Participation of tRNA in regulation of protein biosynthesis at the translational level in eukaryotes. Biochimie. 1979;61(3):323–342. doi: 10.1016/s0300-9084(79)80126-1. [DOI] [PubMed] [Google Scholar]
  32. Post L. E., Strycharz G. D., Nomura M., Lewis H., Dennis P. P. Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit beta in Escherichia coli. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1697–1701. doi: 10.1073/pnas.76.4.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Reddy V. B., Thimmappaya B., Dhar R., Subramanian K. N., Zain B. S., Pan J., Ghosh P. K., Celma M. L., Weissman S. M. The genome of simian virus 40. Science. 1978 May 5;200(4341):494–502. doi: 10.1126/science.205947. [DOI] [PubMed] [Google Scholar]
  34. Roberts J. L., Seeburg P. H., Shine J., Herbert E., Baxter J. D., Goodman H. M. Corticotropin and beta-endorphin: construction and analysis of recombinant DNA complementary to mRNA for the common precursor. Proc Natl Acad Sci U S A. 1979 May;76(5):2153–2157. doi: 10.1073/pnas.76.5.2153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rogers J., Clarke P., Salser W. Sequence analysis of cloned cDNA encoding part of an immunoglobulin heavy chain. Nucleic Acids Res. 1979 Jul 25;6(10):3305–3321. doi: 10.1093/nar/6.10.3305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sanger F., Air G. M., Barrell B. G., Brown N. L., Coulson A. R., Fiddes C. A., Hutchison C. A., Slocombe P. M., Smith M. Nucleotide sequence of bacteriophage phi X174 DNA. Nature. 1977 Feb 24;265(5596):687–695. doi: 10.1038/265687a0. [DOI] [PubMed] [Google Scholar]
  37. Sauer R. T. DNA sequence of the bacteriophage gama cI gene. Nature. 1978 Nov 16;276(5685):301–302. doi: 10.1038/276301a0. [DOI] [PubMed] [Google Scholar]
  38. Schaffner W., Kunz G., Daetwyler H., Telford J., Smith H. O., Birnstiel M. L. Genes and spacers of cloned sea urchin histone DNA analyzed by sequencing. Cell. 1978 Jul;14(3):655–671. doi: 10.1016/0092-8674(78)90249-0. [DOI] [PubMed] [Google Scholar]
  39. Scherer G. Nucleotide sequence of the O gene and of the origin of replication in bacteriophage lambda DNA. Nucleic Acids Res. 1978 Sep;5(9):3141–3156. doi: 10.1093/nar/5.9.3141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Schwarz E., Scherer G., Hobom G., Kössel H. Nucleotide sequence of cro, cII and part of the O gene in phage lambda DNA. Nature. 1978 Mar 30;272(5652):410–414. doi: 10.1038/272410a0. [DOI] [PubMed] [Google Scholar]
  41. Seeburg P. H., Shine J., Martial J. A., Baxter J. D., Goodman H. M. Nucleotide sequence and amplification in bacteria of structural gene for rat growth hormone. Nature. 1977 Dec 8;270(5637):486–494. doi: 10.1038/270486a0. [DOI] [PubMed] [Google Scholar]
  42. Seidman J. G., Leder A., Nau M., Norman B., Leder P. Antibody diversity. Science. 1978 Oct 6;202(4363):11–17. doi: 10.1126/science.99815. [DOI] [PubMed] [Google Scholar]
  43. Seidman J. G., Max E. E., Leder P. A kappa-immunoglobulin gene is formed by site-specific recombination without further somatic mutation. Nature. 1979 Aug 2;280(5721):370–375. doi: 10.1038/280370a0. [DOI] [PubMed] [Google Scholar]
  44. Shaw D. C., Walker J. E., Northrop F. D., Barrell B. G., Godson G. N., Fiddes J. C. Gene K, a new overlapping gene in bacteriophage G4. Nature. 1978 Apr 6;272(5653):510–515. doi: 10.1038/272510a0. [DOI] [PubMed] [Google Scholar]
  45. Shine J., Seeburg P. H., Martial J. A., Baxter J. D., Goodman H. M. Construction and analysis of recombinant DNA for human chorionic somatomammotropin. Nature. 1977 Dec 8;270(5637):494–499. doi: 10.1038/270494a0. [DOI] [PubMed] [Google Scholar]
  46. Smith M., Leung D. W., Gillam S., Astell C. R., Montgomery D. L., Hall B. D. Sequence of the gene for iso-1-cytochrome c in Saccharomyces cerevisiae. Cell. 1979 Apr;16(4):753–761. doi: 10.1016/0092-8674(79)90091-6. [DOI] [PubMed] [Google Scholar]
  47. Sures I., Lowry J., Kedes L. H. The DNA sequence of sea urchin (S. purpuratus) H2A, H2B and H3 histone coding and spacer regions. Cell. 1978 Nov;15(3):1033–1044. doi: 10.1016/0092-8674(78)90287-8. [DOI] [PubMed] [Google Scholar]
  48. Sutcliffe J. G. Nucleotide sequence of the ampicillin resistance gene of Escherichia coli plasmid pBR322. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3737–3741. doi: 10.1073/pnas.75.8.3737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Tonegawa S., Maxam A. M., Tizard R., Bernard O., Gilbert W. Sequence of a mouse germ-line gene for a variable region of an immunoglobulin light chain. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1485–1489. doi: 10.1073/pnas.75.3.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Ullrich A., Shine J., Chirgwin J., Pictet R., Tischer E., Rutter W. J., Goodman H. M. Rat insulin genes: construction of plasmids containing the coding sequences. Science. 1977 Jun 17;196(4296):1313–1319. doi: 10.1126/science.325648. [DOI] [PubMed] [Google Scholar]
  51. Valenzuela P., Gray P., Quiroga M., Zaldivar J., Goodman H. M., Rutter W. J. Nucleotide sequence of the gene coding for the major protein of hepatitis B virus surface antigen. Nature. 1979 Aug 30;280(5725):815–819. doi: 10.1038/280815a0. [DOI] [PubMed] [Google Scholar]
  52. van Wezenbeek P., Schoenmakers J. G. Nucleotide sequence of the genes III, VI and I of bacteriophage M13. Nucleic Acids Res. 1979 Jun 25;6(8):2799–2818. doi: 10.1093/nar/6.8.2799. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES