Antagonistic action of Bicoid and the repressor Capicua determines the spatial limits of Drosophila head gene expression domains

Bicoid (Bcd) is the anterior determinant in Drosophila. Accordingly, loss of Bcd causes loss of head and thorax and their replacement with posterior structures. bcd mRNA is maternally deposited at the anterior pole and Bcd forms an anterior-to-posterior (AP) concentration gradient. The expression of a series of zygotic head genes is thought to be differentially regulated by distinct threshold concentrations of the Bcd gradient. Thereby Bcd functions as a morphogen, instructing fields of cells to take on specific fates. Here, we show that spatial limits of anterior genes are also set in the absence of a Bcd gradient and depend on factors of the maternal terminal system. The receptor tyrosine kinase Torso (Tor), a key component of this system, is active in the pole regions of the embryo. Its activity downregulates the maternally deposited repressor Capicua (Cic), leaving high Cic activity in the central regions and decreasingly lower Cic activities toward the poles. We show that the positions of posterior boundaries of Bcd target genes are dependent not only on Bcd, but also on Tor-mediated Cic activity. The results indicate that Cic can mediate repression through distinct binding sites within a Bcd responsive enhancer and that gene activation by Bcd is antagonized by Cic. The activating and repressive effects of Bcd and Cic, respectively, are integrated by the Bcd target gene enhancer. We conclude that the spatial domains of head gene expression are determined by Bcd in concert with Tor-dependent repressors.