Precision of Hunchback Expression in the Drosophila Embryo

SummaryActivation of the gap gene hunchback (hb) by the maternal Bicoid gradient is one of the most intensively studied gene regulatory interactions in animal development. Most efforts to understand this process have focused on the classical Bicoid target enhancer located immediately upstream of the P2 promoter [ 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11 and 12]. However, hb is also regulated by a recently identified distal shadow enhancer as well as a neglected “stripe” enhancer, which mediates expression in both central and posterior regions of cellularizing embryos [ 13 and 14]. Here, we employ BAC transgenesis and quantitative imaging methods to investigate the individual contributions of these different enhancers to the dynamic hb expression pattern. These studies reveal that the stripe enhancer is crucial for establishing the definitive border of the anterior Hb expression pattern, just beyond the initial border delineated by Bicoid. Removal of this enhancer impairs dynamic expansion of hb expression and results in variable cuticular defects in the mesothorax (T2) due to abnormal patterns of segmentation gene expression. The stripe enhancer is subject to extensive regulation by gap repressors, including Kruppel, Knirps, and Hb itself. We propose that this repression helps ensure precision of the anterior Hb border in response to variations in the Bicoid gradient.

► The Hunchback (Hb) embryonic pattern is produced via the action of three enhancers ► The “stripe” enhancer is critical for production of the final, refined Hb border ► This enhancer is regulated via general activation and carved out by gap repressors ► It is unexpectedly autorepressed, which restricts expression to the boundary region