Muscles in the Drosophila second thoracic segment are patterned independently of autonomous homeotic gene function

Abstract

Background: In Drosophila, segment-specific muscle pattern is thought to be determined by the autonomous function of homeotic selector genes in the mesoderm in combination with inductive cues from the developing epidermis and nervous system. Here, we have examined the roles of homeotic genes in the patterning of the somatic muscles of the thoracic segments of Drosophila. Results: We determined the expression patterns of homeoproteins in the mesoderm of the thoracic segments during embryonic and adult development. We found that, unlike the mesoderm of the first and third thoracic segments which express Sex combs reduced and Antennapedia (Antp), respectively, the mesoderm of the second thoracic segment does not express any known homeotic selector gene of the Antp or bithorax complex. In animals homozygous for Antp null mutations, the muscles of the second thoracic segment were affected in the embryo, probably as an indirect consequence of its requirement in the ectoderm. Animals that specifically lacked Antp function in the mesoderm, but expressed the gene in the epidermis, developed with a normal muscle pattern in the second thoracic segment. Furthermore, specific ectopic expression of Antp and other homeotic selector genes in the mesoderm of the second thoracic segment respecified its muscle pattern, indicating that these genes are not required autonomously during muscle development in this segment. Finally, we showed that Antp continues to be expressed in the mesoderm of the homeotically transformed third thoracic segment in the 'four-winged fly', and suggest that this is a likely reason for the failure of flight muscle development in the transformed segment. Conclusions: We present a model for muscle development in the second thoracic segment whereby mesodermal properties are specified entirely by induction, in contrast to muscle development in other segments, where autonomous function for homeotic selector genes is also required.