Intron-dependent evolution of chicken glyceraldehyde phosphate dehydrogenase gene (original) (raw)

Nature volume 313, pages 498–500 (1985)Cite this article

Abstract

The function of introns in the evolution of genes can be explained in at least two ways: either introns appeared late in evolution and therefore could not have participated in the construction of primordial genes, or RNA splicing and introns existed in the earliest organisms but were lost during the evolution of the modern prokaryotes. The latter alternative allows the possibility of intron participation in the formation of primordial genes before the divergence of modern prokaryotes and eukaryotes1,2. Blake3 suggested that evidence for intron-facilitated evolution of a gene might be found by comparing the borders of functional protein domains with the placement of introns. We therefore examined glyceraldehyde phosphate dehydrogenase (GAPDH), a glycolytic enzyme, because it is the first protein for which the following data are available: (1) X-ray crystallographic studies demonstrating structurally independent protein ‘domains’ which were highly conserved during the divergence of prokaryotes and eukaryotes4,5; and (2) a study of genomic organization which mapped introns in the gene6. Sequencing of the chicken GAPDH gene revealed 11 introns. We report here that sites of three of the introns (IV, VI and XI) correspond closely with the borders of the NAD-binding, catalytic and helical tail domains of the enzyme, supporting the hypothesis that introns did have a role in the evolution of primitive genes. In addition, other biochemical and structural data were used to construct a model of the intron-mediated assembly of the GAPDH gene that explains the existence of 10 introns.

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References

  1. Doolittle, W. Nature 272, 581–582 (1978).
    Article ADS Google Scholar
  2. Darnell, J. Science 202, 1257–1260 (1978).
    Article ADS CAS Google Scholar
  3. Blake, C. Nature 273, 267–268 (1978); Nature 306, 535–537 (1983).
    Article ADS Google Scholar
  4. Rossman, M., Liljas, A., Branden, C. & Banaszak, L. The Enzymes Vol. 11 (ed. Boyer, P.) 61–102 (Academic, New York, 1975).
    Article CAS Google Scholar
  5. Biesecker, G., Harris, J., Thierry, J., Walker, J. & Wonacott, A. Nature 266, 328–333 (1977).
    Article ADS CAS Google Scholar
  6. Stone, E., Rothblum, K., Kuo, T., Alvey, M. C. & Schwartz, R. J. Proc. natn. Acad. Sci. U.S.A. (in the press).
  7. Gilbert, W. Nature 271, 501 (1978).
    Article ADS CAS Google Scholar
  8. Stein, J. P., Catterall, J. F., Kristo, P., Means, A. R. & O'Malley, B. W. Cell 21, 681–687 (1980).
    Article CAS Google Scholar
  9. Barker, W., Ketcham, L. & Dayhoff, M. J. molec. Evol. 15, 113–127 (1980).
    Article ADS Google Scholar
  10. Ohkubo, H. et al. Proc. natn. Acad. Sci. U.S.A. 77, 7059–7063 (1980).
    Article ADS CAS Google Scholar
  11. Tilghman, S. M. 27th scient. Rep. Inst. Cancer Res. 125 (Fox Chase Cancer Centre, 1982).
  12. Dugaiczyk, A. et al. Biochemistry 22, 1605–1613 (1983).
    Article CAS Google Scholar
  13. Moras, D. et al. J. biol. Chem. 250, 9137–9162 (1975).
    CAS PubMed Google Scholar
  14. Harris, J. & Waters, M. The Enzymes Vol. 13 (ed. Boyer, P.) 1–49 (Academic, New York, 1976).
    Google Scholar
  15. Davidson, B. E., Sajgo, M., Noller, H. G. & Harris, J. I. Nature 216, 1181–1185 (1967).
    Article ADS CAS Google Scholar
  16. Hocking, J. & Harris, J. Experientia Suppl. 26, 121–133 (1975).
    Article Google Scholar
  17. Holland, J. & Holland, M. J. biol. Chem. 255, 2596–2605 (1980).
    CAS PubMed Google Scholar
  18. Harris, J. & Perham, R. Nature 219, 1025–1028 (1968).
    Article ADS CAS Google Scholar
  19. Nowak, K., Wolny, M. & Banas, T. FEBS Lett. 134, 143–146 (1981).
    Article CAS Google Scholar

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Authors and Affiliations

  1. Department of Cell Biology, Baylor College of Medicine, One Baylor Plaza, Houston, Texas, 77030, USA
    Edwin M. Stone, Katrina N. Rothblum & Robert J. Schwartz

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  1. Edwin M. Stone
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  2. Katrina N. Rothblum
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  3. Robert J. Schwartz
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Stone, E., Rothblum, K. & Schwartz, R. Intron-dependent evolution of chicken glyceraldehyde phosphate dehydrogenase gene.Nature 313, 498–500 (1985). https://doi.org/10.1038/313498a0

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