Head and thoracic transformations caused by ectopic expression of Antennapedia during Drosophila development

Abstract

Segmental identity in Drosophila is controlled by the activities of the homeotic genes. One such gene is Antennapedia, which is required for the proper development of the thoracic segments. Alteration of Antennapedia expression either in mutants, or artificially using an inducible promoter, can lead to alterations of segmental identity. In this report, we present the consequences of ectopic expression of the Antennapedia gene under the control of a heat-shock promoter, at distinct stages throughout Drosophila development. In young embryos, up to the stage of germ-band retraction, the ubiquitous expression of the Antennapedia protein causes a range of effects throughout the embryo, including failure of head involution, induction of extra denticles on the dorsal surface of the head and disruption of the prothoracic denticle belts. In older embryos, it results in larval lethality. Heat shocks during larval development can lead to defects in leg formation, but no alterations in leg identity have been observed. However, clear transformations of head towards second (meso-) thoracic segment can be induced in early third instar larvae. There is a distal-to-proximal temporal response to ectopic Antennapedia expression in the antennal disc, as evidenced by successive transformations of the arista, third antennal segment, second antennal segment and occiput towards their corresponding leg and dorsal thoracic structures. Overproduction of Antennapedia protein during the pupal stage is generally lethal. Comparison of the homeotic transformations in, and Western analysis of, different lines suggests that a relatively large amount of Antennapedia protein is required to cause antenna-to-leg transformations, and further argues that, in general, developmental programmes in the insect are well buffered against the effects of ectopic homeotic gene expression. Immunodetection of Scr and Antp protein also allows us to interpret the results in light of the hypothesis that the various selector genes compete with one another to control not only their own expression, but also that of downstream genes. The role of Antennapedia in imaginal disc determination is also discussed.