3 MATERNAL COORDINATE SYSTEMS COOPERATE IN THE PATTERNING OF THE DROSOPHILA HEAD

In contrast to the segmentation of the embryonic trunk region which ha s been extensively studied, relatively little is known about the devel opment and segmentation of the Drosophila head, Proper development of the cephalic region requires the informational input of three of the f our maternal coordinate systems. Head-specific gene expression is set up in response to a complex interaction between the maternally provide d gene products and zygotically expressed genes. Several zygotic genes involved in head development have recently been characterized. A gene tic analysis suggests that the segmentation of the head may use a mech anism different from the one acting in the trunk. The two genes of the sloppy paired locus (slp1 and slp2) are also expressed in the embryon ic head. slp1 plays a predominant role in head formation while slp2 is largely dispensible. A detailed analysis of the sip head phenotype su ggests that slp is important for the development of the mandibular seg ment as well as two adjacent pregnathal segments (antennal and ocular) . Our analysis of regulatory interactions of slp with maternal and zyg otic genes suggests that it behaves like a gap gene. Thus, phenotype a nd regulation of sip support the view that slp acts as a head-specific gap gene in addition to its function as a pair-rule and segment polar ity gene in the trunk. We show that all three maternal systems active in the cephalic region are required for proper sip expression and that the different systems cooperate in the patterning of the head. The te rminal and anterior patterning system appear to be closely linked. Thi s cooperation is likely to involve a direct interaction between the bc d morphogen and the terminal system. Low levels of terminal system act ivity seem to potentiate bcd as an activator of sip, whereas high leve ls down-regulate bcd rendering it inactive. Our analysis suggests that dorsal, the morphogen of the dorsoventral system, and the head-specif ic gap gene empty spiracles act as repressor and corepressor in the re gulation of sip. We discuss how positional information established ind ependently along two axes can act in concert to control gene regulatio n in two dimensions.