Journal of Molecular Evolution

, Volume 27, Issue 3, pp 228–235

Evolution of tropomyosin functional domains: Differential splicing and genomic constraints

  • S. Colote
  • J. Sri Widada
  • C. Ferraz
  • F. Bonhomme
  • J. Marti
  • J. -P. Liautard
Article

Summary

We have cloned and determined the nucleotide sequence of a complementary DNA (cDNA) encoded by a newly isolated human tropomyosin gene and expressed in liver. Using the leastsquare method of Fitch and Margoliash, we investigated the nucleotide divergences of this sequence and those published in the literature, which allowed us to clarify the classification and evolution of the tropomyosin genes expressed in vertebrates. Tropomyosin undergoes alternative splicing on three of its nine exons. Analysis of the exons not involved in differential splicing showed that the four human tropomyosin genes resulted from a duplication that probably occurred early, at the time of the amphibian radiation. The study of the sequences obtained from rat and chicken allowed a classification of these genes as one of the types identified for humans.

The divergence of exons 6 and 9 indicates that functional pressure was exerted on these sequences, probably by an interaction with proteins in skeletal muscle and perhaps also in smooth muscle; such a constraint was not detected in the sequences obtained from nonmuscle cells. These results have led us to postulate the existence of a protein in smooth muscle that may be the counterpart of skeletal muscle troponin.

We show that different kinds of functional pressure were exerted on a single gene, resulting in different evolutionary rates and different convergences in some regions of the same molecule.

Codon usage analysis indicates that there is no strict relationship between tissue types (and hence the tRNA precursor pool) and codon usage. G+C content is characteristic of a gene and does not change significantly during evolution. These results are in good agreement with an isochore composition of the genome, and thus suggest a similar chromosomal environment in chicken, rat, and human.

Key words

Tropomyosin Differential splicing Evolution Isochore Codon usage Sequence convergence Functional constraints 

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References

  1. Alonso S, Minty A, Bourlet Y, Buckingham M (1986) Comparison of three actin-sequences in the mouse; evolutionary relationships between the actin genes of warm-blooded vertebrates. J Mol Evol 23:11–22Google Scholar
  2. Bernardi G, Bernardi G (1985) Codon usage and genome composition. J Mol Biol 22:363–365Google Scholar
  3. Bernardi G, Bernardi G (1986) Compositional constraints and genome evolution. J Mol Evol 24:1–11Google Scholar
  4. Bernardi G, Olofsson B, Filipski J, Salinas J, Cuny G, Meunier-Rotival M, Rodier F (1985) The mosaic genome of warmblooded vertebrates. Science 228:953–958Google Scholar
  5. Berstein B, Bambourg J (1982) Tropomyosin binding to F-actin protects the F-actin from disassembly by actin depolymerising factor. Cell Motil 2:1–8Google Scholar
  6. Cavadore JC, Berta P, Axelrud-Cavadore C, Haiech J (1985) Calcium binding of arterial tropomyosin: involvement in the thin filament regulation of smooth muscle. Biochemistry 24:5216–5221Google Scholar
  7. Cooper H, Feurstein N, Noda M, Bassin R (1985) Suppression of tropomyosin synthesis, a common biochemical feature of oncogenesis by structurally diverse retroviral oncogenes. Mol Cell Biol 5:972–983Google Scholar
  8. Cote G, Lewis W, Pato M, Smillie L (1978) Platelet tropomyosin: lack of binding to skeletal muscle troponin and correlation with sequence. FEBS Lett 94:131–135Google Scholar
  9. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284Google Scholar
  10. Flach J, Lidquester G, Berish S, Hickam K, Devlin R (1986) Analysis of tropomyosin cDNAs isolated from skeletal and smooth muscle mRNA. Nucleic Acids Res 14:9193–9211Google Scholar
  11. Giometti C, Anderson L (1984) Tropomyosin heterogeneity in human cells. J Biol Chem 259:14113–14120Google Scholar
  12. Helfman D, Cheley S, Kuismanen E, Finn L, Yamawaki-Kataoka Y (1986) Non muscle and muscle tropomyosin isoforms are expressed from a single gene by alternative RNA splicing and polyadenylation. Mol Cell Biol 6:3582–3595Google Scholar
  13. Helfman D, Faramisco J, Ricci W, Hughes S (1984) Isolation and sequence of a cDNA clone that contains the entire coding region for chicken smooth muscle tropomyosin. J Biol Chem 259:14136–14143Google Scholar
  14. Hendricks M, Weintraub H (1981) Tropomyosin is decreased in transformed cells. Proc Natl Acad Sci USA 78:5633–5637Google Scholar
  15. Leavitt J, Latter G, Lutomski L, Goldstein D, Burbeck S (1986) Tropomyosin isoform switching in tumorigenic human fibroblast. Mol Cell Biol 6:2721–2726Google Scholar
  16. MacLeod A (1982) Distinct α-tropomyosin mRNA sequences in chicken skeletal muscle. Eur J Biochem 126:293–297Google Scholar
  17. MacLeod A, Houlker C, Reinach F, Smillie L, Talbot K, Modi G, Walsh F (1985) A muscle-type tropomyosin in human fibroblasts: evidence for expression by an alternative RNA splicing mechanism. Proc Natl Acad Sci USA 82:7835–7839Google Scholar
  18. MacLeod A, Houlker C, Reinach F, Talbot K (1986) The mRNA and RNA-copy pseudogenes encoding TM30 nm a human cytoskeletal tropomyosin. Nucleic Acids Res 14:8413–8426Google Scholar
  19. MacLeod A, Talbot K, Smillie L, Houlker C (1987) Characterisation of a cDNA defining a gene family encoding TM30 pl a human fibroblast tropomyosin. J Mol Biol 194:1–10Google Scholar
  20. Maxam AM, Gilbert W (1980) Sequencing of end-labelled DNA with base specific cleavage reactions. Methods Enzymol 65:499–560Google Scholar
  21. McLachlan A, Stewart M (1975) Tropomyosin coiled-coil interactions: evidence for an unstaggered structure. J Mol Biol 98:293–304Google Scholar
  22. Paulin D, Perreau J, Jakob H, Jacob F, Yaniv M (1979) Tropomyosin synthesis accompanies formation of actin filaments in embryonal carcinoma cells induced to differentiate by hexamethylene bisacetamide. Proc Natl Acad Sci USA 76:1891–1895Google Scholar
  23. Reinach F, MacLeod A (1986) Tissue-specific expression of the human tropomyosin gene involved in the generation of the trk oncogene. Nature 322:648–650Google Scholar
  24. Ruiz-Opazo N, Weinberger J, Nadal-Ginard B (1985) Comparison of α-tropomyosin sequences from smooth and striated muscle. Nature 315:67–70Google Scholar
  25. Sanger F, Niclen S, Coulson A (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467Google Scholar
  26. Smillie L (1979) Structure and function of tropomyosins from muscle and non-muscle sources. Trends Biochem Sci 4:151–155Google Scholar
  27. Staden R (1982) An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res 10:2951–2960Google Scholar
  28. Stossel T, Chaponnier C, Ezzell R, Hartwig J, Janmey P, Kwiatkosky D, Lind S, Smith D, Southwick, Yin H, Zaner K (1985) Nonmuscle actin-binding proteins. Annu Rev Cell Biol 1:353–402Google Scholar

Copyright information

© Springer-Verlag New York Inc 1988

Authors and Affiliations

  • S. Colote
    • 1
  • J. Sri Widada
    • 1
  • C. Ferraz
    • 1
  • F. Bonhomme
    • 2
  • J. Marti
    • 3
  • J. -P. Liautard
    • 1
  1. 1.INSERM U-249, CRBM du CNRSUniversité de Montpellier IMontpellierFrance
  2. 2.Institut des Sciences de l'Évolution, CNRS UA 327USTL pl. E. BataillonMontpellierFrance
  3. 3.INSERM U-65Institut de Biologie Bd Henri IVMontpellierFrance

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