Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1980 May 10;8(9):1893–1912. doi: 10.1093/nar/8.9.1893

Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type.

R Grantham, C Gautier, M Gouy
PMCID: PMC324046  PMID: 6159596

Abstract

The poor printing of our previous Figure 2 (1) is corrected. Codon usage in mRNA sequences just published is also given. A new correspondence analysis is done, based on simultaneous comparison in all mRNA of use of the 61 codons. This analysis reinforces our claim that most genes in a genome, or genome type, have the same coding strategy; that is, they show similar choices among synonymous codons, or among degenerate bases (2). Like analysis on frequency variation in the amino acids coded reveals an entirely different pattern.

Full text

PDF
1893

Selected References

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

  1. Alton N. K., Vapnek D. Nucleotide sequence analysis of the chloramphenicol resistance transposon Tn9. Nature. 1979 Dec 20;282(5741):864–869. doi: 10.1038/282864a0. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Büchel D. E., Gronenborn B., Müller-Hill B. Sequence of the lactose permease gene. Nature. 1980 Feb 7;283(5747):541–545. doi: 10.1038/283541a0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Csordás-Tóth E., Boros I., Venetianer P. Nucleotide sequence of a secondary attachment site for bacteriophage lambda on the Escherichia coli chromosome. Nucleic Acids Res. 1979 Nov 10;7(5):1335–1341. doi: 10.1093/nar/7.5.1335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. 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]
  10. 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]
  11. 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]
  12. 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]
  13. 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]
  14. 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]
  15. Firtel R. A., Timm R., Kimmel A. R., McKeown M. Unusual nucleotide sequences at the 5' end of actin genes in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6206–6210. doi: 10.1073/pnas.76.12.6206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fox T. D. Five TGA "stop" codons occur within the translated sequence of the yeast mitochondrial gene for cytochrome c oxidase subunit II. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6534–6538. doi: 10.1073/pnas.76.12.6534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Grantham R., Gautier C. Genetic distances from mRNA sequences. Naturwissenschaften. 1980 Feb;67(2):93–94. doi: 10.1007/BF01054695. [DOI] [PubMed] [Google Scholar]
  19. Grantham R., Gautier C., Gouy M., Mercier R., Pavé A. Codon catalog usage and the genome hypothesis. Nucleic Acids Res. 1980 Jan 11;8(1):r49–r62. doi: 10.1093/nar/8.1.197-c. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. 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]
  24. 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]
  25. 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]
  26. Heffron F., McCarthy B. J., Ohtsubo H., Ohtsubo E. DNA sequence analysis of the transposon Tn3: three genes and three sites involved in transposition of Tn3. Cell. 1979 Dec;18(4):1153–1163. doi: 10.1016/0092-8674(79)90228-9. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Holland J. P., Holland M. J. The primary structure of a glyceraldehyde-3-phosphate dehydrogenase gene from Saccharomyces cerevisiae. J Biol Chem. 1979 Oct 10;254(19):9839–9845. [PubMed] [Google Scholar]
  30. Honjo T., Obata M., Yamawaki-Katoaka Y., Kataoka T., Kawakami T., Takahashi N., Mano Y. Cloning and complete nucleotide sequence of mouse immunoglobulin gamma 1 chain gene. Cell. 1979 Oct;18(2):559–568. doi: 10.1016/0092-8674(79)90072-2. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. Konkel D. A., Maizel J. V., Jr, Leder P. The evolution and sequence comparison of two recently diverged mouse chromosomal beta--globin genes. Cell. 1979 Nov;18(3):865–873. doi: 10.1016/0092-8674(79)90138-7. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Kronenberg H. M., McDevitt B. E., Majzoub J. A., Nathans J., Sharp P. A., Potts J. T., Jr, Rich A. Cloning and nucleotide sequence of DNA coding for bovine preproparathyroid hormone. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4981–4985. doi: 10.1073/pnas.76.10.4981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Lawther R. P., Nichols B., Zurawski G., Hatfield G. W. The nucleotide sequence preceding and including the beginning of the ilvE gene of the ilvGEDA operon of Escherichia coli K12. Nucleic Acids Res. 1979 Dec 20;7(8):2289–2301. doi: 10.1093/nar/7.8.2289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Marcoli R., Iida S., Bickle T. A. The DNA sequence of an IS/-flanked transposon coding for resistance to chloramphenicol and fusidic acid. FEBS Lett. 1980 Jan 28;110(1):11–14. doi: 10.1016/0014-5793(80)80011-1. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. 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]
  41. Miyata T., Hayashida H., Yasunaga T., Hasegawa M. The preferential codon usages in variable and constant regions of immunoglobulin genes are quite distinct from each other. Nucleic Acids Res. 1979 Dec 20;7(8):2431–2438. doi: 10.1093/nar/7.8.2431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Nakamura K., Inouye M. DNA sequence of the gene for the outer membrane lipoprotein of E. coli: an extremely AT-rich promoter. Cell. 1979 Dec;18(4):1109–1117. doi: 10.1016/0092-8674(79)90224-1. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Nichols B. P., Yanofsky C. Nucleotide sequences of trpA of Salmonella typhimurium and Escherichia coli: an evolutionary comparison. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5244–5248. doi: 10.1073/pnas.76.10.5244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Nishioka Y., Leder P. The complete sequence of a chromosomal mouse alpha--globin gene reveals elements conserved throughout vertebrate evolution. Cell. 1979 Nov;18(3):875–882. doi: 10.1016/0092-8674(79)90139-9. [DOI] [PubMed] [Google Scholar]
  46. Perricaudet M., Akusjärvi G., Virtanen A., Pettersson U. Structure of two spliced mRNAs from the transforming region of human subgroup C adenoviruses. Nature. 1979 Oct 25;281(5733):694–696. doi: 10.1038/281694a0. [DOI] [PubMed] [Google Scholar]
  47. Porter A. G., Barber C., Carey N. H., Hallewell R. A., Threlfall G., Emtage J. S. Complete nucleotide sequence of an influenza virus haemagglutinin gene from cloned DNA. Nature. 1979 Nov 29;282(5738):471–477. doi: 10.1038/282471a0. [DOI] [PubMed] [Google Scholar]
  48. 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]
  49. 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]
  50. Richards R. I., Shine J., Ullrich A., Wells J. R., Goodman H. M. Molecular cloning and sequence analysis of adult chicken betal globin cDNA. Nucleic Acids Res. 1979 Nov 10;7(5):1137–1146. doi: 10.1093/nar/7.5.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. 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]
  52. 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]
  53. Roskam W. G., Rougeon F. Molecular cloning and nucleotide sequence of the human growth hormone structural gene. Nucleic Acids Res. 1979 Sep 25;7(2):305–320. doi: 10.1093/nar/7.2.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. 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]
  55. 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]
  56. 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]
  57. 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]
  58. 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]
  59. 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]
  60. 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]
  61. 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]
  62. 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]
  63. 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]
  64. 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]
  65. 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]
  66. 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]
  67. 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]
  68. Tsujimoto Y., Suzuki Y. The DNA sequence of Bombyx mori fibroin gene including the 5' flanking, mRNA coding, entire intervening and fibroin protein coding regions. Cell. 1979 Oct;18(2):591–600. doi: 10.1016/0092-8674(79)90075-8. [DOI] [PubMed] [Google Scholar]
  69. 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]
  70. 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]
  71. Williamson V. M., Bennetzen J., Young E. T., Nasmyth K., Hall B. D. Isolation of the structural gene for alcohol dehydrogenase by genetic complementation in yeast. Nature. 1980 Jan 10;283(5743):214–216. doi: 10.1038/283214a0. [DOI] [PubMed] [Google Scholar]
  72. 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