Mediation of Drosophila head development by gap-like segmentation genes

The first phase of embryonic development in Drosophila consists of the elaboration and interpretation of maternally encoded information that specifies spatial pattern in the embryo. The product of the maternal gene bicoid (bcd) is thought to organize the anterior pattern of the embryo. Although the bcd transcript is localized at the anterior pole of the egg the bcd protein forms a stable concentration gradient through the anterior two thirds of the embryo. The graded distribution of bcd protein defines position along the anterior-posterior axis of the embryo through the spatially restricted activation of subordinate targets such as the gap gene hunchback (hb). In vitro manipulation of specific bcd protein binding sites has shown that the gradient of bcd protein can in principle define more than one discrete domain of spatially restricted gene activation in the head of the embryo, depending on the affinity of the available binding sites for the bcd protein. Genetic analysis has indicated the need for at least one additional zygotic segmentation gene to mediate bcd function in portions of the head that lie anterior to the hb domain. The missing gene activity is expected to be activated in response to higher levels of bcd protein than are required for hb activation. We report here that three previously identified zygotic genes buttonhead (btd), empty spiracles (ems) and orthodenticle (otd) may behave like gap genes that mediate bcd function in the embryonic head.