Summary
For each of eleven different types of nuclear genes, comparisons of the protein coding sequences were made between human, mouse and rat pairwisely, and the evolutionary rate of silent substitution, v nucl.S , was estimated. It is shown that the v nucl.S is not only very high (=5.37×10−9/site/yr), but also approximately uniform for different genes regardless of the types, which confirms our previous results (Miyata et al. 1980b). This is in sharp contrast to the rate of protein evolution which differes greatly from protein to protein. Furthermore the v nucl.S is shown to be approximately constant with respect to different divergence times, at least within a short time period (≤75 Myr). Based on these observations, we propose a new molecular clock which has several advantages over a protein clock. Using this clock, we show that the rate of amino acid replacement in the immunoglobulin Ck gene of b4 rabbit is unexpectedly high, almost comparable to the rate of silent changes. This rate may be the highest one for protein evolution that we know so far. We further examine the rate of silent substitutions in mitochondrial genes comparing mouse and rat. Surprisingly the rate is extremely high (≥35×10−9/site/yr), at least 6-times as high as the corresponding rate of nuclear genes. Based on the estimate, we discuss a possible origin of the rapid rate found in mitochondrial DNA.
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Abbreviations
- URF:
-
Unidentified reading frame
- yr:
-
Year
References
Anderson S, Bankier AT, Barrell GB, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roc BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–464
Bell GI, Pictet RL, Rutter WJ, Cordell B, Tischer E, Goodman HM (1980) Sequence of the human insulin gene. Nature 284:26–32
Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180
Bregegere F, Abastodo JP, Kvist S, Rask L, Lalanne JL, Garoff H, Cami B, Wiman K, Larhammar D, Peterson PA, Gachelin G, Kourilsky P, Dobberstein B (1981) Structure of C-terminal half of two H-2 antigens from cloned mRNA. Nature 292:78–81
Brown WM, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76: 1967–1971
Brown WM (1981) Mechanisms of evolution of animal mitochondrial DNA. Annals NY Acad Sci 361:119–134
Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: Tempo and mode of evolution. J Mol Evol 18:225–239
Chersi A, Alexander CB, Mage R (1980) Partial primary structure of the immunoglobulin light chain constant region of a single rabbit of b5 allotype. Mol Immunol 17:1515–1523
Chin WW, Kronenberg HM, Dee PC, Maloof F, Habener JF (1981) Nucleotide sequence of the mRNA encoding the pre-α-subunit of mouse thyrotropin. Proc Natl Acad Sci USA 78:5329–5333
Cooke NE, Coit D, Weiner RI, Baxter JD, Martial JA (1980) Structure of cloned DNA complementary to rat prolactin messenger RNA. J Biol Chem 255:6502–6510
Cooke NE, Coit D, Shine J, Baxter JD, Martial JA (1981) Human prolactin. J Biol Chem 256:4007–4016
Dayhoff MO (1978) In Atlas of protein sequence and structure. Dayhoff MD (ed) vol 5, suppl 3, National Biomedical Research Foundation, Silver Spring, MD
Dickerson RE (1971) The structure of cytochrome c and the rates of molecular evolution. J Mol Evol 1:26–45
Fransworth V, Goodfliesh R, Rodkey S, Hood L (1976) Immunoglobulin allotypes of rabbit kappa chains: Polymorphism of a control mechanism regulating closely linked duplicated genes? Proc Natl. Acad Sci USA 73:1293–1296
Fiddes JC, Goodman HM (1979) Isolation, cloning and sequence analysis of the cDNA for the α-subunit of human chorionic gonadotropin. Nature 281:351–356
Fitch WM, Margoliash E (1970) The usefulness of amino acid and nucleotide sequences in evolutionary studies. Evol Biol 4:76–109
Grunstein M, Schede P, Kedes L (1976) Sequence analysis and evolution of sea urchin (Lytechinus pictus andStronglyocentrotus purpuratus) histone H4 messenger RNAs. J Mol Biol 104:351–369
Hagenbuchle O, Bovey R, Young RA (1980) Tissue-specific expression of mouse α-amylase genes: Nucleotide sequence of isoenzyme mRNAs from pancreas and salivary gland. Cell 21: 179–187
Heidemann O, Auffray C, Cazenave P, Rougeon F (1981) Nucleotide sequence of constant and 3′ untranslated regions of ak immunoglobulin light chain mRNA of a homozygous b4 rabbit. Proc Natl Acad Sci USA 78:5802–5806
Heindell HC, Paddock GV, Studnicka GM, Salser WA (1978) The primary sequence of rabbit α-globin mRNA. Cell 15: 43–54
Hieter PA, Max EE, Seidmann JG, Maizel JV Jr, Leder P (1980) Cloned human and mouse kappa immunogloblin constant and J region genes conserved homology in functional segments. Cell 22:197–207
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolisms II, vol III, Academic Press, New York, pp 21–132
Jukes TH (1980) Silent nucleotide substitutions and the molecular evolutionary clock. Science 210:973–978
Kawakami T, Takahashi N, Honjo T (1980) Complete nucleotide sequence of mouse immunoglobulin μ gene and comparison with other immunoglobulin heavy chain genes. Nucleic Acids Res 8:3933–3945
Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624–626
Kimura M, Ohta T (1972) On the stochastic model for estimation of mutational distance between homologous proteins. J Mol Evol 2:87–90
Kimura M, Ohta T (1974) On some principles governing molecular evolution. Proc Natl Acad Sci USA 71:2848–2852
Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci USA 78:454–458
Konkel DA, Maizel JV Jr, Leder P (1979) The evolution and sequence comparison of two recently diverged mouse chromosomal β-globin genes. Cell 18:865–873
Lawn RM, Efstratiadis A, O'Connell C, Maniatis T (1980) The nucleotide sequence of the human β-blobin gene. Cell 21: 645–651
Li W, Gojobori T, Nei M (1981) Pseudogenes as a paradigm of neutral evolution. Nature 292:237–239
Lomedico P, Rosenthal N, Efstratiadis A, Gilbert W, Kolodner R, Tizard R (1979) The structure and evolution of the two nonallelic rat preproinsulin genes. Cell 18:545–558
MacDonald RJ, Crerar MM, Swain WF, Pictet RL, Thomas G, Rutter WJ (1980) Structure of a family of rat amylase genes. Nature 287:117–122
Martial JA, Hallewell RA, Baxter JD, Goodman HM (1979) Human growth hormone: Complementary DNA cloning and expression in bacteria. Science 205:602–607
Martin SL, Zimmer EA, Davidson WS, Wilson AC, Kan YW (1981) The untranslated regions of β-globin mRNA evolve at a functional rate in higher primates. Cell 25:737–741
Miyata T, Yasunaga T (1980) 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 16:23–36
Miyata T, Yasunaga T, Yamawaki-Kataoka Y, Obata M, Honjo T (1980a) Nucleotide sequence divergence of mouse immunoglobulin γl and γ2b genes and the hypothesis of intervening sequence-mediated domain transfer. Proc Natl Acad Sci USA 77:2143–2147
Miyata T, Yasunaga T, Nishida T (1980b) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332
Miyata T, Yasunaga T (1981) Rapidly evolving mouse α-globin related pseudo gene and its evolutionary history. Proc Natl Acad Sci USA 78:450–453
Miyata T, Hayashida H (1981) Extraordinarily high evolutionary rate of pseudogenes: Evidence for the presence of selective pressure against changes between synonymous codons. Proc Natl Acad Sci USA 78:5739–5741
Miyata T (1982) Evolutionary changes and functional constraint in DNA sequences. In: Kimura M (ed) Molecular Evolution, protein polymorphism and the neutral theory. Japan Scientific Press, Tokyo, pp 233–266
Miyata T, Hayashida H (1982) Recent divergence from a common ancestor of human IFN-α genes. Nature 295:165–168
Miyata T, Kikuno R, Ohshima Y (1982) A pseudogene cluster in the leader region of theEuglena chloroplast 16S–23S rRNA genes. Nucleic Acids Res 10:1771–1780
Nishioka Y, Leder P (1979) The complete sequence of a chromosomal mouse α-globin gene reveals elements conserved throughout vertebrate evolution. Cell 18:875–882
Nishioka Y, Leder A, Leder P (1980) Unusual α-globin-like gene that has cleanly lost both globin intervening sequences. Proc Natl Acad Sci USA 77:2806–2809
Ohta T (1974) Mutational pressure as the main cause of molecular evolution and polymorphism. Nature 252:351–354
Perler F, Efstratiadis A, Lomedico P, Gilbert W, Kolonder R, Dodgson J (1980) The evolution of genes: The chicken preproinsulin gene. Cell 20:555–566
Rabbitts TH, Forster A, Milstein CP (1981) Human immunoglobulin heavy chain genes: Evolutionary comparisons of Cμ, Cδ and Cγ genes and associated switch sequences. Nucleic Acids Res 9:4509–4524
Saccone C, Cantatore P, Gadaleta G, Gallerani R, Lanave C, Pepe G, Kroon AM (1981) The nucleotide sequence of the large ribosomal RNA gene and the adjacent tRNA genes from rat mitochondria. Nucleic Acids Res 9:4139–4148
Seeberg PH, Shine J, Martial JA, Baxter JD, Goodman HM (1977) Nucleotide sequence and amplification in bacteria of structural gene for rat growth hormone. Nature 270:486–494
Sheppard HW, Gutman GA (1981) Allelic forms of ratk chain genes: Evidence for strong selection at the level of nucleotide sequence. Proc Natl Acad Sci USA 78:7064–7068
Shine J, Seeberg PH, Martial JA, Baxter JD, Goodman HM (1977) Construction and analysis of recombinant DNA for human chorionic somatomammotropin. Nature 270:494–499
Takahata N, Kimura M (1981) A model of evolutionary base substitutions and its applications with special reference to rapid change of pseudo genes. Genetics 98:641–657
Van Ooen A, Van Den Berg J, Mantei N, Weissmann C (1979) Comparison of total sequence of a cloned rabbit β-globin gene and its flanking regions with a homologous mouse sequence. Science 206:337–344
Vanin EF, Goldberg GI, Tucker PW, Smithies O (1980) A mouse α-globin-related pseudogene lacking intervening sequences. Nature 286:222–226
Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Ann Rev Biochem 46:573–639
Wilson JT, Wilson JB, Reddy VB, Covallesco C, Ghosh PK, Riek JK, Forget BG, Weissman SM (1980) Nucleotide sequence of the coding portion of human α globin messenger RNA. J Biol Chem 255:2807–2815
Yarmush ML, Sogn JA, Kindt TJ (1979) Latent allotypes: A window to a genetic enigma. Ann Immunol Inst Pasteur 130C:143–156
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Miyata, T., Hayashida, H., Kikuno, R. et al. Molecular clock of silent substitution: At least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol 19, 28–35 (1982). https://doi.org/10.1007/BF02100221
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DOI: https://doi.org/10.1007/BF02100221