Abstract
IT is generally accepted that the specific function of a gene depends on its coding sequence. The three paired-box and homeobox genes paired (prd), gooseberry (gsb) and gooseberry neuro (gsbn) have distinct developmental functions in Drosophila embryogenesis1–5. During the syncytial blastoderm stage, the pair-rule gene prd4,6 activates segment-polarity genes, such as gsb7, wingless (wg)9 and engrailed (en), in segmentally repeated stripes8. After germ-band extension, gsb maintains the expression of wg, which in turn specifies the denticle pattern by repressing a default state of ubiquitous denticle formation in the ventral epidermis9. In addition, gsb activates gsbn5, which is expressed mainly in the central nervous system2,3, suggesting that gsbn is involved in neural development. Here we show that, despite the functional difference and the considerably diverged coding sequence of these genes, their proteins have conserved the same function. The finding that the essential difference between genes may reside in their cis-regulatory regions exemplifies an important evolutionary mechanism of how function diversifies after gene duplication.
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References
Noll, M. Curr. Opin. Genet. Dev. 3, 595–605 (1993).
Bopp, D., Burri, M., Baumgartner, S., Frigerio, G. & Noll, M. Cell 47, 1033–1040 (1986).
Baumgartner, S., Bopp, D., Burri, M. & Noll, M. Genes Dev. 1, 1247–1267 (1987).
Gutjahr, T., Frei, E. & Noll, M. Development 117, 609–623 (1993).
Gutjahr, T., Patel, N. H., Li, X., Goodman, C. S. & Noll, M. Development 118, 21–31 (1993).
Kilchherr, F., Baumgartner, S., Bopp, D., Frei, E. & Noll, M. Nature 321, 493–499 (1986).
Bopp, D., Jamet, E., Baumgartner, S., Burri, M. & Noll, M. EMBO J. 8, 3447–3457 (1989).
Ingham, P. W. & Martínez-Arias, A. Cell 68, 221–235 (1992).
Li, X. & Noll, M. EMBO J. 12, 4499–4509 (1993).
Struhl, G. Nature 318, 677–680 (1985).
Ish-Horowicz, D. & Pinchin, S. M. Cell 51, 405–415 (1987).
Morrissey, D., Askew, D., Raj, L. & Weir, M. Genes Dev. 5, 1684–1696 (1991).
Manoukian, A. S. & Krause, H. M. Genes Dev. 6, 1740–1751 (1992).
Manoukian, A. S. & Krause, H. M. Development 118, 785–796 (1993).
Frasch, M., Hoey, T., Rushiow, C., Doyle, H. & Levine, M. EMBO J. 6, 749–759 (1987).
Doe, C. Q., Smouse, D. & Goodman, C. S. Nature 333, 376–378 (1988).
Patel, N. H., Schafer, B., Goodman, C. S. & Holmgren, R. Genes Dev. 3, 890–904 (1989).
Li, X., Gutjahr, T. & Noll, M. EMBO J. 12, 1427–1436 (1993).
Frigerio, G., Burri, M., Bopp, D., Baumgartner, S. & Noll, M. Cell 47, 735–746 (1986).
Côté, S. et al. EMBO J. 6, 2793–2801 (1987).
Bejsovec, A. & Martínez-Arias, A. Development 113, 471–485 (1991).
Hoey, T. & Levine, M. Nature 332, 858–861 (1988).
Jacob, F. Science 196, 1161–1166 (1977).
Thomas, K. R. & Capecchi, M. R. Nature 346, 847–850 (1990).
McMahon, A. P. & Bradley, A. Cell 62, 1073–1085 (1990).
Joyner, A. L., Herrup, K., Auerbach, B. A., Davis, C. A. & Rossant, J. Science 251, 1239–1243 (1991).
Lohnes, D. et al. Cell 73, 643–658 (1993).
Wieschaus, E. & Nüsslein-Volhard, C. in Drosophila, a Practical Approach (ed. Roberts, D. B.), 199–227 (IRL Press, Oxford, 1986).
Dambly-Chaudière, C. et al. Cell 69, 159–172 (1992).
Rubin, G. M. & Spradling, A. C. Science 218, 348–353 (1982).
DiNardo, S. & O'Farrell, P. H. Genes Dev. 1, 1212–1225 (1987).
van den Heuvel, M., Nusse, R., Johnston, P. & Lawrence, P. A. Cell 59, 739–749 (1989).
Hidalgo, A. Mech. Dev. 35, 77–87 (1991).
Klemenz, R., Weber, U. & Gehring, W. J. Nucleic Acids Res. 15, 3947–3959 (1987).
Maxam, A. M. & Gilbert, W. Proc. natn. Acad. Sci. U.S.A. 74, 560–564 (1977).
Stanojevic, D., Hoey, T. & Levine, M. Nature 341, 331–335 (1989).
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Li, X., Noll, M. Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions. Nature 367, 83–87 (1994). https://doi.org/10.1038/367083a0
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DOI: https://doi.org/10.1038/367083a0
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