Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1980 Dec;77(12):7328–7332. doi: 10.1073/pnas.77.12.7328

Nucleotide sequence divergence and functional constraint in mRNA evolution.

T Miyata, T Yasunaga, T Nishida
PMCID: PMC350496  PMID: 6938980

Abstract

Comparison of about 50 pairs of homologous nucleotide sequences for different genes revealed that the substitutions between synonymous codons occurred at much higher rates than did amino acid substitutions. Furthermore, five pairs of mRNA sequences for different genes were compared in species that had diverged at the same time. The evolutionary rate of synonymous substitution was estimated to be 5.1 X 10(-9) per site per year on the average and is approximately constant among different genes. It also is suggested that this property would be suitable for a molecular clock to determine the evolutionary relationships and branching order of duplicated genes. Each functional block of the noncoding region evolves with a rate that is almost constant, regardless of the types of genes. The intervening sequence and the 5' portion of the 3' noncoding region show considerable divergence, the extent of which is almost comparable to that in the synonymous codon sites, whereas the other blocks consisting of the 5' noncoding region and the 3' portion of the 3' noncoding region are strongly conserved, showing approximatley half of the divergence of the synonymous sites. This strong sequence preservation might be due to the functional requirements for transcription and modification of mRNA.

Full text

PDF
7328

Selected References

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

  1. Bell G. I., Pictet R. L., Rutter W. J., Cordell B., Tischer E., Goodman H. M. Sequence of the human insulin gene. Nature. 1980 Mar 6;284(5751):26–32. doi: 10.1038/284026a0. [DOI] [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. Busslinger M., Portmann R., Irminger J. C., Birnstiel M. L. Ubiquitous and gene-specific regulatory 5' sequences in a sea urchin histone DNA clone coding for histone protein variants. Nucleic Acids Res. 1980 Mar 11;8(5):957–977. doi: 10.1093/nar/8.5.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cordell B., Bell G., Tischer E., DeNoto F. M., Ullrich A., Pictet R., Rutter W. J., Goodman H. M. Isolation and characterization of a cloned rat insulin gene. Cell. 1979 Oct;18(2):533–543. doi: 10.1016/0092-8674(79)90070-9. [DOI] [PubMed] [Google Scholar]
  5. Deacon N. J., Shine J., Naora H. Complete nucleotide sequence of a cloned chicken alpha-globin cDNA. Nucleic Acids Res. 1980 Mar 25;8(6):1187–1199. doi: 10.1093/nar/8.6.1187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Early P., Huang H., Davis M., Calame K., Hood L. An immunoglobulin heavy chain variable region gene is generated from three segments of DNA: VH, D and JH. Cell. 1980 Apr;19(4):981–992. doi: 10.1016/0092-8674(80)90089-6. [DOI] [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. 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]
  10. 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]
  11. Grantham R., Gautier C., Gouy M. Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type. Nucleic Acids Res. 1980 May 10;8(9):1893–1912. doi: 10.1093/nar/8.9.1893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grunstein M., Grunstein J. E. The histone H4 gene of Strongylocentrotus purpuratus: DNA and mRNA sequences at the 5' end. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1083–1092. doi: 10.1101/sqb.1978.042.01.109. [DOI] [PubMed] [Google Scholar]
  13. Grunstein M., Schedl P., Kedes L. Sequence analysis and evolution of sea urchin (Lytechinus pictus and Strongylocentrotus purpuratus) histone H4 messenger RNAs. J Mol Biol. 1976 Jun 25;104(2):351–369. doi: 10.1016/0022-2836(76)90276-x. [DOI] [PubMed] [Google Scholar]
  14. Hasegawa M., Yasunaga T., Miyata T. Secondary structure of MS2 phage RNA and bias in code word usage. Nucleic Acids Res. 1979 Dec 11;7(7):2073–2079. doi: 10.1093/nar/7.7.2073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. Jones C. W., Rosenthal N., Rodakis G. C., Kafatos F. C. Evolution of two major chorion multigene families as inferred from cloned cDNA and protein sequences. Cell. 1979 Dec;18(4):1317–1332. doi: 10.1016/0092-8674(79)90242-3. [DOI] [PubMed] [Google Scholar]
  19. Jou W. M., Verhoeyen M., Devos R., Saman E., Fang R., Huylebroeck D., Fiers W., Threlfall G., Barber C., Carey N. Complete structure of the hemagglutinin gene from the human influenza A/Victoria/3/75 (H3N2) strain as determined from cloned DNA. Cell. 1980 Mar;19(3):683–696. doi: 10.1016/s0092-8674(80)80045-6. [DOI] [PubMed] [Google Scholar]
  20. Jukes T. H., King J. L. Evolutionary nucleotide replacements in DNA. Nature. 1979 Oct 18;281(5732):605–606. doi: 10.1038/281605a0. [DOI] [PubMed] [Google Scholar]
  21. Kafatos F. C., Efstratiadis A., Forget B. G., Weissman S. M. Molecular evolution of human and rabbit beta-globin mRNAs. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5618–5622. doi: 10.1073/pnas.74.12.5618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kimura M. Evolutionary rate at the molecular level. Nature. 1968 Feb 17;217(5129):624–626. doi: 10.1038/217624a0. [DOI] [PubMed] [Google Scholar]
  23. Kimura M., Ohta T. On some principles governing molecular evolution. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2848–2852. doi: 10.1073/pnas.71.7.2848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kimura M., Ota T. On the stochastic model for estimation of mutational distance between homologous proteins. J Mol Evol. 1972 Dec 29;2(1):87–90. doi: 10.1007/BF01653945. [DOI] [PubMed] [Google Scholar]
  25. Kimura M. Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature. 1977 May 19;267(5608):275–276. doi: 10.1038/267275a0. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Leder A., Miller H. I., Hamer D. H., Seidman J. G., Norman B., Sullivan M., Leder P. Comparison of cloned mouse alpha- and beta-globin genes: conservation of intervening sequence locations and extragenic homology. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6187–6191. doi: 10.1073/pnas.75.12.6187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lerner M. R., Boyle J. A., Mount S. M., Wolin S. L., Steitz J. A. Are snRNPs involved in splicing? Nature. 1980 Jan 10;283(5743):220–224. doi: 10.1038/283220a0. [DOI] [PubMed] [Google Scholar]
  30. Lomedico P., Rosenthal N., Efstratidadis A., Gilbert W., Kolodner R., Tizard R. The structure and evolution of the two nonallelic rat preproinsulin genes. Cell. 1979 Oct;18(2):545–558. doi: 10.1016/0092-8674(79)90071-0. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. 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]
  34. Miyata T., Yasunaga T. Molecular evolution of mRNA: a method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application. J Mol Evol. 1980 Sep;16(1):23–36. doi: 10.1007/BF01732067. [DOI] [PubMed] [Google Scholar]
  35. Miyata T., Yasunaga T., Yamawaki-Kataoka Y., Obata M., Honjo T. Nucleotide sequence divergence of mouse immunoglobulin gamma 1 and gamma 2b chain genes and the hypothesis of intervening sequence-mediated domain transfer. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2143–2147. doi: 10.1073/pnas.77.4.2143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Montgomery D. L., Leung D. W., Smith M., Shalit P., Faye G., Hall B. D. Isolation and sequence of the gene for iso-2-cytochrome c in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1980 Jan;77(1):541–545. doi: 10.1073/pnas.77.1.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Nakamura K., Inouye M. DNA sequence of the Serratia marcescens lipoprotein gene. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1369–1373. doi: 10.1073/pnas.77.3.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. 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]
  41. 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]
  42. Nishioka Y., Leder A., Leder P. Unusual alpha-globin-like gene that has cleanly lost both globin intervening sequences. Proc Natl Acad Sci U S A. 1980 May;77(5):2806–2809. doi: 10.1073/pnas.77.5.2806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. 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]
  45. 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]
  46. 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]
  47. 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]
  48. Salser W. Globin mRNA sequences: analysis of base pairing and evolutionary implications. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):985–1002. doi: 10.1101/sqb.1978.042.01.099. [DOI] [PubMed] [Google Scholar]
  49. Salser W., Isaacson J. S. Mutation rates in globin genes: the genetic load and Haldane's dilemma. Prog Nucleic Acid Res Mol Biol. 1976;19:205–220. doi: 10.1016/s0079-6603(08)60919-8. [DOI] [PubMed] [Google Scholar]
  50. 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]
  51. Sanger F., Coulson A. R., Friedmann T., Air G. M., Barrell B. G., Brown N. L., Fiddes J. C., Hutchison C. A., 3rd, Slocombe P. M., Smith M. The nucleotide sequence of bacteriophage phiX174. J Mol Biol. 1978 Oct 25;125(2):225–246. doi: 10.1016/0022-2836(78)90346-7. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. 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]
  54. Seidman J. G., Leder A., Edgell M. H., Polsky F., Tilghman S. M., Tiemeier D. C., Leder P. Multiple related immunoglobulin variable-region genes identified by cloning and sequence analysis. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3881–3885. doi: 10.1073/pnas.75.8.3881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. 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]
  56. Seif I., Khoury G., Dhar R. The genome of human papovavirus BKV. Cell. 1979 Dec;18(4):963–977. doi: 10.1016/0092-8674(79)90209-5. [DOI] [PubMed] [Google Scholar]
  57. 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]
  58. 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]
  59. 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]
  60. Vanin E. F., Goldberg G. I., Tucker P. W., Smithies O. A mouse alpha-globin-related pseudogene lacking intervening sequences. Nature. 1980 Jul 17;286(5770):222–226. doi: 10.1038/286222a0. [DOI] [PubMed] [Google Scholar]
  61. Wilson A. C., Carlson S. S., White T. J. Biochemical evolution. Annu Rev Biochem. 1977;46:573–639. doi: 10.1146/annurev.bi.46.070177.003041. [DOI] [PubMed] [Google Scholar]
  62. Yamawaki-Kataoka Y., Kataoka T., Takahashi N., Obata M., Honjo T. Complete nucleotide sequence of immunoglobulin gamma2b chain gene cloned from newborn nouse DNA. Nature. 1980 Feb 21;283(5749):786–789. doi: 10.1038/283786a0. [DOI] [PubMed] [Google Scholar]
  63. Yang R. C., Wu R. BK virus DNA sequence: extent of homology with simian virus 40 DNA. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1179–1183. doi: 10.1073/pnas.76.3.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Yang R. C., Wu R. BK virus DNA: complete nucleotide sequence of a human tumor virus. Science. 1979 Oct 26;206(4417):456–462. doi: 10.1126/science.228391. [DOI] [PubMed] [Google Scholar]
  65. van Ooyen A., van den Berg J., Mantei N., Weissmann C. Comparison of total sequence of a cloned rabbit beta-globin gene and its flanking regions with a homologous mouse sequence. Science. 1979 Oct 19;206(4416):337–344. doi: 10.1126/science.482942. [DOI] [PubMed] [Google Scholar]
  66. van den Berg J., van Ooyen A., Mantei N., Schamböck A., Grosveld G., Flavell R. A., Weissmann C. Comparison of cloned rabbit and mouse beta-globin genes showing strong evolutionary divergence of two homologous pairs of introns. Nature. 1978 Nov 2;276(5683):37–44. doi: 10.1038/276037a0. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES