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Comparison of three actin-coding sequences in the mouse; Evolutionary relationships between the actin genes of warm-blooded vertebrates

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Summary

We have determined the sequences of three recombinant cDNAs complementary to different mouse actin mRNAs that contain more than 90% of the coding sequences and complete or partial 3′ untranslated regions (3′UTRs): pAM 91, complementary to the actin mRNA expressed in adult skeletal muscle (αsk actin); pAF 81, complementary to an actin mRNA that is accumulated in fetal skeletal muscle and is the major transcript in adult cardiac muscle (αc actin); and pAL 41, identified as complementary to a β nonmuscle actin mRNA on the basis of its 3′UTR sequence. As in other species, the protein sequences of these isoforms are highly (>93%) conserved, but the three mRNAs show significant divergence (13.8–16.5%) at silent nucleotide positions in their coding regions. A nucleotide region located toward the 5′ end shows significantly less divergence (5.6–8.7%) among the three mouse actin mRNAs; a second region, near the 3′ end, also shows less divergence (6.9%), in this case between the mouse β and αsk actin mRNAs. We propose that recombinational events between actin sequences may have homogenized these regions. Such events distort the calculated evolutionary distances between sequences within a species. Codon usage in the three actin mRNAs is clearly different, and indicates that there is no strict relation between the tissue type, and hence the tRNA precursor pool, and codon usage in these and other muscle mRNAs examined. Analysis of codon usage in these coding sequences in different vertebrate species indicates two tendencies: increases in bias toward the use of G and C in the third codon position in paralogous comparisons (in the order αc), and in orthologous comparisons (in the order chicken < rodent < man). Comparison of actin-coding sequences between species was carried out using the Perler method of analysis. As one moves backward in time, changes at silent sites first accumulate rapidly, then begin to saturate after −(30–40) million years (MY), and actually decrease between −400 and −500 MY. Replacements or silent substitutions therefore cannot be used as evolutionary clocks for these sequences over long periods. Other phenomena, such as gene conversion or isochore compartmentalization, probably distort the estimated divergence time.

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References

  • Arnold HH, Krauskopf M, Siddiqui MAQ (1983) The nucleotide sequence of myosin light chain (L-2A) mRNA from embryonic chicken cardiac muscle tissue. Nucleic Acids Res 11: 1123–1131

    PubMed  Google Scholar 

  • Bagshaw CR (1982) Muscle contraction. In: Brammar WJ, Edidin M (eds) Outline studies in biology. Chapman and Hall, London New York, pp 30–38

    Google Scholar 

  • Baltimore D (1981) Gene conversion: some implications for immunoglobulin genes. Cell 24:592–594

    PubMed  Google Scholar 

  • Bergsma DJ, Chang KS, Schwartz RJ (1985) Novel chicken actin gene: third cytoplasmic isoform. Mol Cell Biol 5:1151–1162

    PubMed  Google Scholar 

  • 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 228:953–958

    PubMed  Google Scholar 

  • Bernstein LB, Mount SM, Weiner AM (1983) Pseudogenes for human small nuclear RNA U3 appear to arise by integration of self-primed reverse transcripts of the RNA into new chromosomal sites. Cell 32:461–472

    PubMed  Google Scholar 

  • Buckingham ME, Minty AJ (1983) Contractile protein genes. In: Maclean N, Gregory SP, Flavell RA (eds) Eukaryotic genes: their structure, activity and regulation, vol 21. Butterworths, London, pp 365–395

    Google Scholar 

  • Challberg MD, Englund PT (1980) Specific labelling of 3′-termini with T4 DNA polymerase. Methods Enzymol 65:39–43

    PubMed  Google Scholar 

  • Chang KS, Rothblum KN, Schwartz RJ (1985) The complete sequence of the chicken α-cardiac actin gene: a highly conserved vertebrate gene. Nucleic Acids Res 13:1223–1249

    PubMed  Google Scholar 

  • Claverie JM (1984) A common philosophy and FORTRAN 77 software package for implementing and searching sequence databases. Nucleic Acids Res 12:397–407

    PubMed  Google Scholar 

  • Cleveland DW, Lopata MA, MacDonald RJ, Cowan NJ, Rutter WJ, Kirschner MW (1980) Number and evolutionary conservation of α-and β-tubulin and cytoplasmic β-and γ-actin genes using specific cloned cDNA probes. Cell 20:95–105

    PubMed  Google Scholar 

  • Cooke NE, Coit D, Shine J, Baxter JD, Martial JA (1981) Human prolactin: cDNA structural analysis and evolutionary comparisons. J Biol Chem 256:4007–4016

    PubMed  Google Scholar 

  • Czosnek H, Nudel U, Mayer Y, Barker PE, Pravtcheva DD, Ruddle FH, Yaffě D (1983) The genes coding for the cardiac muscle actin, the skeletal muscle actin and the cytoplasmic β-actin are located on three different mouse chromosomes. EMBO J 2:1977–1979

    PubMed  Google Scholar 

  • Davidson EH, Britten RJ (1973) Organization, transcription and regulation in the animal genome. Rev Biol 48:565–613

    Google Scholar 

  • Dickerson RE (1971) The structure of cytochrome c and the rates of molecular evolution. J Mol Evol 1:26–45

    PubMed  Google Scholar 

  • Domdey H, Wiebauer K, Klapthor H, Arnold HH (1983) Sequence analysis of the cloned mRNA coding for glyceraldehyde-3-phosphate dehydrogenase from chicken heart muscle. Eur J Biochem 131:129–135

    PubMed  Google Scholar 

  • Engel JN, Gunning PW, Kedes LM (1981) Isolation and characterization of human actin genes. Proc Natl Acad Sci USA 78:4674–4678

    PubMed  Google Scholar 

  • Fields S, Winter G (1981) Nucleotide sequence heterogeneity and sequence rearrangements in influenza virus cDNA. Gene 15:207–214

    PubMed  Google Scholar 

  • Fornwald JA, Kuncio G, Peng I, Ordahl CP (1982) The complete nucleotide sequence of the chick α-actin gene and its evolutionary relationship to the actin gene family. Nucleic Acids Res 10:3861–3876

    PubMed  Google Scholar 

  • Fyrberg EA, Bond BJ, Hershey ND, Mixter KS, Davidson N (1981) The actin genes ofDrosophila: Protein coding regions are highly conserved but intron positions are not. Cell 24: 107–116

    PubMed  Google Scholar 

  • Gallwitz D, Seidel R (1980) Molecular cloning of the actin gene from yeastSaccharomyces cerevisiae. Nucleic Acids Res 8: 1043–1059

    PubMed  Google Scholar 

  • Gunning P, Ponte P, Blau H, Kedes L (1983) α-Skeletal and α-cardiac actin genes are coexpressed in adult human skeletal muscle and heart. Mol Cell Biol 3:1985–1995

    PubMed  Google Scholar 

  • Gunning P, Ponte P, Kedes L, Hickey RJ, Skoultchi A (1984a) Expression of human cardiac actin in mouse L cells: A sarcomeric actin associates with a non muscle cytoskeleton. Cell 36:709–715

    PubMed  Google Scholar 

  • Gunning P, Ponte P, Kedes L, Eddy R, Shows T (1984b) Chromosomal location of the coexpressed human skeletal and cardiac actin genes. Proc Natl Acad Sci USA 81:1813–1817

    PubMed  Google Scholar 

  • Hamada H, Petrino MG, Kakunaga T (1982) Molecular structure and evolutionary origin of human cardiac actin gene. Proc Natl Acad Sci USA 79:5901–5905

    PubMed  Google Scholar 

  • Hanauer A, Levin M, Heilig R, Daegelen D, Kahn A, Mandel JL (1983) Isolation and characterization of cDNA clones for human skeletal muscle α actin. Nucleic Acids Res 11: 3503–3516

    PubMed  Google Scholar 

  • Hastings KEM, Emerson CP Jr (1983) Codon usage in muscle genes and liver genes. J Mol Evol 19:214–218

    PubMed  Google Scholar 

  • Humphries SE, Whittall R, Minty A, Buckingham ME, Williamson R (1981) There are approximately 20 actin genes in the human genome. Nucleic Acids Res 9:4895–4908

    PubMed  Google Scholar 

  • Kost TA, Theodorakis N, Hugues SH (1983) The nucleotide sequence of the chick cytoplasmic β-actin gene. Nucleic Acids Res 11:8287–8301

    PubMed  Google Scholar 

  • Kvist S, Brégégère F, Rask L, Cami B, Garoff H, Daniel F, Wiman K, Larhammar D, Abastado JP, Gachelin G, Peterson PA, Dobberstein B, Kourilsky P (1981) cDNA clone coding for part of a mouse H-2d major histocompatibility antigen. Proc Natl Acad Sci USA 78:2772–2776

    PubMed  Google Scholar 

  • Mahdavi V, Periasamy M, Nadal-Ginard B (1982) Molecular characterization of two myosin heavy chain genes expressed in the adult heart. Nature 297:659–664

    PubMed  Google Scholar 

  • Maxam AM, Gilbert W (1980) Sequencing of end-labelled DNA with base specific cleavage reactions. Methods Enzymol 65: 499–560

    PubMed  Google Scholar 

  • Mayer Y, Czosnek H, Zeelon PE, Yaffě D, Nudel U (1984) Expression of the genes coding for the skeletal muscle and cardiac actins in the heart. Nucleic Acids Res 12:1087–1100

    PubMed  Google Scholar 

  • McKenna MG (1969) The origin and early differentiation of therian mammals. Ann NY Acad Sci 167:217–240

    Google Scholar 

  • McKenna MG (1975) In: Luckett WP, Szalay FS (eds) Phylogeny of the primates. Plenum Press, New York, p 21

    Google Scholar 

  • Minty AJ, Caravatti M, Robert B, Cohen A, Daubas P, Weydert A, Gros F, Buckingham ME (1981) Mouse actin mRNAs. Construction and characterization of a recombinant plasmid molecule containing a complementary DNA transcript of mouse α-actin mRNA. J Biol Chem 256:1008–1014

    PubMed  Google Scholar 

  • Minty AJ, Alonso S, Caravatti M, Buckingham ME (1982) A fetal skeletal muscle actin mRNA in the mouse and its identity with cardiac actin mRNA. Cell 30:185–192

    PubMed  Google Scholar 

  • Minty AJ, Alonso S, Guénet JL, Buckingham ME (1983) Number and organization of actin-related sequences in the mouse genome. J Mol Biol 167:77–101

    PubMed  Google Scholar 

  • Moore GW, Goodman M, Callahan C, Holmquist R, Moise H (1976) Stochastic versus augmented maximum parsimony method for estimating superimposed mutations in the divergent evolution of protein sequences. Methods tested on cytochrome c amino acid sequences. J Mol Biol 105:15–37

    PubMed  Google Scholar 

  • Moos M, Gallwitz D (1982) Structure of a human β-actin related pseudogene which lacks intervening sequences. Nucleic Acids Res 10:7843–7849

    PubMed  Google Scholar 

  • Nabeshima YI, Fujii-Kuriyama Y, Muramatsu M, Ogata K (1984) Alternative transcription and two modes of splicing result in two myosin light chains from one gene. Nature 308: 333–338

    PubMed  Google Scholar 

  • Ng R, Abelson J (1980) Isolation and sequence of the gene for actin inSaccharomyces cerevisiae. Proc Natl Acad Sci USA 77:3912–3916

    PubMed  Google Scholar 

  • Nudel U, Zakut R, Shani M, Neuman S, Levy Z, Yaffě D (1983) The nucleotide sequence of the rat cytoplasmic β-actin gene. Nucleic Acids Res 11:1759–1771

    PubMed  Google Scholar 

  • Nudel U, Calvo JM, Shani M, Levy Z. (1984) The nucleotide sequence of a rat myosin light chain 2 gene. Nucleic Acids Res 12:7175–7186

    PubMed  Google Scholar 

  • Ordahl CP, Cooper TA (1983) Strong homology in promoter and 3′ untranslated regions of chick and rat α-actin genes. Nature 303:348–349

    PubMed  Google Scholar 

  • Periasamy M, Strehler EE, Garfinkel LI, Gubits RM, Ruiz-Opazo N, Nadal-Ginard B (1984) Fast skeletal muscle myosin light chains 1 and 3 are produced from a single gene by a combined process of differential RNA transcription and splicing. J Biol Chem 259:13595–13604

    PubMed  Google Scholar 

  • Perler F, Efstratiadis A, Lomedico P, Gilbert W, Kolodner R, Dodgson J (1980) The evolution of genes: the chicken preproinsulin gene. Cell 20:555–566

    PubMed  Google Scholar 

  • Pollard TD, Weihing RR (1974) Actin and myosin and cell movement. CRC Crit Rev Biochem 2:1–65

    PubMed  Google Scholar 

  • Ponte P, Gunning P, Blau H, Kedes L (1983) Human actin genes are single copy for α-skeletal and α-cardiac actin but multicopy for β-and γ-cytoskeletal genes: 3′ Untranslated regions are isotype specific but are conserved in evolution. Mol Cell Biol 3:1783–1791

    PubMed  Google Scholar 

  • Ponte P, Ng SY, Engel J, Gunning P, Kedes L (1984) Evolutionary conservation in the untranslated regions of actin mRNAs: DNA sequence of a human beta-actin cDNA. Nucleic Acids Res 12:1687–1696

    PubMed  Google Scholar 

  • Robert B, Weydert A, Caravatti M, Minty A, Cohen A, Daubas P, Gros F, Buckingham ME (1982) cDNA recombinant plasmid complementary to mRNAs for light chains 1 and 3 of mouse skeletal muscle myosin. Proc Natl Acad Sci USA 79: 2437–2441

    PubMed  Google Scholar 

  • Robert B, Daubas P, Akimenko MA, Cohen A, Garner I, Guénet JL, Buckingham ME (1984) A single locus in the mouse encodes both myosin light chains 1 and 3, a second locus corresponds to a related pseudogene. Cell 39:129–140

    PubMed  Google Scholar 

  • Robert B, Barton P, Minty A, Daubas P, Weydert A, Bonhomme F, Catalan J, Chazottes D, Guénet JL, Buckingham ME (1985) Investigation of genetic linkage between myosin and actin genes using an interspecific mouse back-cross. Nature 314: 181–183

    PubMed  Google Scholar 

  • Romero-Herrera AE, Lehman H, Joysey KA, Friday AE (1973) Molecular evolution of myoglobin and the fossil record: a phylogenetic synthesis. Nature 246:389–395

    PubMed  Google Scholar 

  • Sanger F, Coulson AR (1978) The use of thin acrylamide gels for DNA sequencing. FEBS Lett 87:107–110

    PubMed  Google Scholar 

  • Slightom JL, Blechl AE, Smithies O (1980) Human fetalGγ-andAγ genes: Complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell 21:627–638

    PubMed  Google Scholar 

  • Staden R, McLachlan AD (1982) Codon preference and its use in identifying protein coding regions in long DNA sequences. Nucleic Acids Res 10:141–156

    PubMed  Google Scholar 

  • Ueyama H, Hamada H, Battula N, Kakunaga T (1984) Structure of a human smooth muscle actin gene (aortic type) with a unique intron site. Mol Cell Biol 4:1073–1078

    PubMed  Google Scholar 

  • Vandekerckhove J, Weber K (1979) The complete amino acid sequence of actins from bovine aorta, bovine heart, bovine fast skeletal muscle and rabbit slow skeletal muscle. Differentiation 14:123–133

    PubMed  Google Scholar 

  • Vandekerckhove J, Weber K (1984) Chordate muscle actins differ distinctly from invertebrate muscle actins. The evolution of the different vertebrate muscle actins. J Mol Biol 179: 391–413

    PubMed  Google Scholar 

  • Vandekerckhove J, De Couet HG, Weber K (1983) In: dos Remedios CG, Barden JA (eds) Actin: structure and function in muscle and non-muscle cells. Academic, Sydney, Australia, pp. 241–248

    Google Scholar 

  • Vandekerckhove J, Bugaisky G, Buckingham ME (1986) J Biol Chem, in press

  • Volckaert G, Tavernier J, Derynck R, Devos R, Fiers W (1981) Molecular mechanisms of nucleotide sequence rearrangements in cDNA clones of human fibroblast interferon mRNA. Gene 15:215–233

    PubMed  Google Scholar 

  • Wain-Hobson S, Nussinov R, Brown RJ, Sussman JL (1981) Preferential codon usage in genes. Gene 13:355–364

    PubMed  Google Scholar 

  • Weydert A, Daubas P, Caravatti M, Minty AJ, Bugaisky G, Cohen A, Robert B, Buckingham ME (1983) Identification of a recombinant plasmid coding for an adult fast myosin heavy chain from mouse skeletal muscle: detection of a sequential accumulation of mRNAs encoding different myosin heavy chain isoforms during skeletal muscle development in vivo. J Biol Chem 258:13867–13874

    PubMed  Google Scholar 

  • Weydert A, Daubas P, Lazaridis I, Barton P, Garner I, Leader DP, Bonhomme F, Catalan J, Simon D, Guénet JL, Gros F, Buckingham ME (1985) Genes for skeletal muscle myosin heavy chains are clustered and are not located on the same chromosome as a cardiac myosin heavy chain gene. Proc Natl Acad Sci USA 82: 7183–7187

    PubMed  Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    PubMed  Google Scholar 

  • Zakut R, Shani M, Givol D, Neuman S, Yaffě D, Nudel U (1982) The nucleotide sequence of the rat skeletal muscle actin gene. Nature 298:857–859

    PubMed  Google Scholar 

  • Zimmer EA, Martin SL, Beverly SM, Kan YW, Wilson AC (1980) Rapid duplication and loss of genes coding for the α chains of hemoglobin. Proc Natl Acad Sci USA 77:2158–2162

    PubMed  Google Scholar 

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Alonso, S., Minty, A., Bourlet, Y. et al. Comparison of three actin-coding sequences in the mouse; Evolutionary relationships between the actin genes of warm-blooded vertebrates. J Mol Evol 23, 11–22 (1986). https://doi.org/10.1007/BF02100994

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  • DOI: https://doi.org/10.1007/BF02100994

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