Head versus trunk patterning in the Drosophila embryo; collier requirementfor formation of the intercalary segment

Whereas the segmental nature of the insect head is well established, relati vely little is known about the genetic and molecular mechanisms governing t his process. In this paper, we report the phenotypic analysis of mutations in collier (col), which encodes the Drosophila member of the COE family of HLH transcription factors and is activated at the blastoderm stage in a reg ion overlapping a parasegment (PS0: posterior intercalary and anterior mand ibular segments) and a mitotic domain, MD2. col mutant embryos specifically lack intercalary ectodermal structures. col activity is required for inter calary-segment expression both of the segment polarity genes hedgehog, engr ailed, and wingless, and of the segment identity gene cap and collar. The p arasegmental register of col activation is controlled by the combined activ ities of the head-gap genes buttonhead and empty spiracles and the pair-rul e gene even skipped; it therefore integrates inputs from both the head and trunk segmentation systems, which were previously considered as being essen tially independent. After gastrulation, positive autoregulation of col is l imited to cells of anterior PS0, Conversely, heat-pulse induced ubiquitous expression of Col leads to disruption of the head skeleton. Together, these results indicate that col is required for establishment of the PS(-1)/PS0 parasegmental border and formation of the intercalary segment. Our data sup port neither a simple combinatorial model for segmental patterning of the h ead nor a direct activation of segment polarity gene expression by head-gap genes, but rather argue for the existence of parasegment-specific second o rder regulators acting in the head, at a level similar to that of pair-rule genes in the trunk.