Functional hierarchy and phenotypic suppression among Drosophila homeotic genes: the labial and empty spiracles genes

The Drosophila homeotic cluster (HOM-C) is made up of eight genes, which specify the identity of cephalic, thoracic and abdominal segments. These genes can be ordered in a hierarchy which correlates with their position along the 5'-3' transcriptional direction. When they are absent, thoracic and abdominal body segments develop the same'ground' pattern, which is thoracic-like but also includes cephalic structures (sclerotic plates). We find that these plates are specified by the homeobox gene empty spiracles (ems) which is not a member of the HOM-C and which is expressed in all body segments. ems mutations, however, only produce defects in anterior head structures and the posterior spiracles. The ems product has the potential to induce sclerotic plates but this potential is suppressed by any of the HOM-C genes, including the labial gene, which we show to be the lowest ranking of the HOM-C hierarchy. This suppression does not occur at the transcriptional or translational level because the ems function is suppressed in cells containing the ems product. Thus, this appears to be the first case of phenotypic suppression operating in normal development. We propose that ems was originally a member of the HOM-C which escaped from the complex and has also acquired new functions during evolution.