Résumés
Résumé
La génétique évolutive du développement révèle une grande plasticité des mécanismes développementaux. L’exemple de bicoid, le premier morphogène connu, illustre comment un gène essentiel peut changer de fonction au cours de l’évolution. La recherche d’homologues de bicoid a montré que ce gène était spécifique des mouches et absent chez les autres insectes. En fait, il s’avère que bicoid est un gène homéotique Hox3 très dérivé (c’est-à-dire très éloigné de son gène ancestral). Au cours de l’évolution des insectes, le gène Hox3 ancestral a perdu sa fonction homéotique pour acquérir un nouveau rôle maternel et dans les annexes embryonnaires. Dans la lignée menant aux mouches, une duplication de ce nouveau gène a ensuite eu lieu, suivie d’une divergence aboutissant à la création des gènes bicoid et zerknüllt. L’analyse de l’évolution de bicoid, comme celle de nombreux autres gènes du développement, montre la nécessité d’élargir le choix des espèces modèles pour éviter les généralisations hâtives faites à partir d’un modèle particulier.
Summary
Evolutionary developmental genetics (evo-devo) reveals that the plasticity of development is so important that every developmental biology project should carefully take this point into consideration. The example of bicoid, the first discovered morphogen, illustrates how an essential gene can change its function during evolution. The search for bicoid homologues showed that this gene is surprisingly specific to flies (cyclorraphan diptera) and absent in other insects. In fact, recent studies demonstrate that bicoid is a very derived Hox3 homeotic gene. During insect evolution, the ancestral Hox3 gene lost its homeotic function and acquired new roles in oocytes and embryonic annexes. Then, in the lineage leading to modern flies, a duplication of this new gene, followed by functional divergence, led to the formation of bicoid and zerknüllt. Both genes are located within the DrosophilaHox complex; however, they have no homeotic function. Thanks to the power of Drosophila genetics, it is possible to suggest that torso and hunchback may constitute the insect primitive anterior organizer. The bicoid evolutionary history reveals several fundamental mechanisms of the evolution of developmental genes, such as changes of gene regulation, modifications of protein sequences and gene duplication. It also shows the need for studying a wider range of model organisms before generalisations can be made from data obtained with one particular species.
Parties annexes
Références
- 1. Deutsch J. Les gènes Hox et le rêve de Darwin. Med Sci 2000; 16: 205-11.
- 2. Laudet V. Vive la zoologie moléculaire! Med Sci 2002; 18: 234-6.
- 3. Brown SJ, Fellers JP, Shippy TD, et al. Sequence of the tribolium castaneum homeotic complex. The region corresponding to the Drosophila melanogaster Antennapedia complex. Genetics 2002; 160: 1067-74.
- 4. Hughes CL, Kaufman TC. Exploring the myriapod body plan: expression patterns of the ten Hox genes in a centipede. Development 2002; 129: 1225-38.
- 5. Stauber M, Prell A, Schmidt-Ott U. A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci USA 2002; 99: 274-9.
- 6. Schröder R, Sander K. A comparison of transplantable bicoid activity and partial bicoid homeobox sequences in several Drosophila and blowfly species (Calliphoridae). Roux’s Arch Dev Biol 1993; 203: 34-43.
- 7. Curtis D, Apfeld J, Lehmann R. nanos is an evolutionarily conserved organizer of anterior-posterior polarity. Development 1995; 121: 1899-910.
- 8. Shaw PJ, Salameh A, McGregor AP, Bala S, Dover GA. Divergent structure and function of the bicoid gene in Muscoidea fly species. Evol Dev 2001; 3: 251-62.
- 9. Stauber M, Jackle H, Schmidt-Ott U. The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc Natl Acad Sci USA 1999; 96: 3786-9.
- 10. Stauber M, Taubert H, Schmidt-Ott U. Function of bicoid and hunchback homologs in the basal cyclorrhaphan fly Megaselia (Phoridae). Proc Natl Acad Sci USA 2000; 97: 10844-9.
- 11. Falciani F, Hausdorf B, Schroder R, et al. Class 3 Hox genes in insects and the origin of zen. Proc Natl Acad Sci USA 1996; 93: 8479-84.
- 12. Dearden P, Grbic M, Falciani F, Akam M. Maternal expression and early zygotic regulation of the Hox3/zen gene in the grasshopper Schistocerca gregaria. Evol Dev 2000; 2: 261-70.
- 13. Damen WG, Tautz D. A Hox class 3 orthologue from the spider Cupiennius salei is expressed in a Hox-gene-like fashion. Dev Genes Evol 1998; 208: 586-90.
- 14. Telford MJ, Thomas RH. Of mites and zen: expression studies in a chelicerate arthropod confirm zen is a divergent Hox gene. Dev Genes Evol 1998; 208: 591-4.
- 15. Abzhanov A, Popadic A, Kaufman TC. Chelicerate Hox genes and the homology of arthropod segments. Evol Dev 1999; 1: 77-89.
- 16. Cook CE, Smith ML, Telford MJ, Bastianello A, Akam M. Hox genes and the phylogeny of the arthropods. Curr Biol 2001; 11: 759-63.
- 17. Schaeffer V, Killian D, Desplan C, Wimmer EA. High bicoid levels render the terminal system dispensable for Drosophila head development. Development 2000; 127: 3993-9.
- 18. Wimmer EA, Carleton A, Harjes P, Turner T, Desplan C. Bicoid-independent formation of thoracic segments in Drosophila. Science 2000; 287: 2476-9.
- 19. Bonneton F, Shaw PJ, Fazakerley C, Shi M, Dover GA. Comparison of bicoid-dependent regulation of hunchback between Musca domestica and Drosophila melanogaster. Mech Dev 1997; 66: 143-56.
- 20. Hughes CL, Kaufman TC. Hox genes and the evolution of the arthropod body plan. Evol Dev 2002; 4: 459-99.
- 21. Mouchel-Vielh E, Blin M, Rigolot C, Deutsch JS. Expression of a homologue of the fushi tarazu (ftz) gene in a cirripede crustacean. Evol Dev 2002; 4: 76-85.
- 22. Schröder R. The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 2003; 422: 621-5.