Hox Enhancers Exploit the Regulatory Landscape of Drosophila Legs to Pattern Leg-Specific Sense-Organs

Hox genes are involved in the patterning of animal body plans at multiple levels of the pattern formation hierarchy. Early expression of Hox genes in different domains along the Drosophila embryonic anterior-posterior (A-P) axis establishes positional identity. However, several reports provide evidence that later in development, differential Hox gene expression within organ fields fine-tunes patterning of animal body parts. Regulation of Hox gene expression within organ fields during later stages of development is complex and understudied. We have investigated the regulation of the Hox genes Sex combs reduced (Scr) and Ultrabithorax (Ubx) within developing legs of the first and third thoracic segments (T1 and T3), respectively. Scr and Ubx are broadly expressed at low-levels throughout leg development. However, we have previously shown that, in addition, elevated levels of Scr and Ubx expression in defined domains are required to establish leg-specific sense-organs, the transverse bristle rows (TBRs) and sex combs bristles (SCB). We have identified an enhancer of Scr, the Scr-E, that directs this spatially-restricted elevated expression. Furthermore, we have found that the gene regulatory network that is initially involved in development of the leg along its three-axes is exploited by this enhancer, to pattern T1 leg-specific sense organs. We show that Distal-less (Dll), one of the earliest genes that mark the leg primordia, activates elevated expression of Scr in a segment-specific manner through the Scr-E enhancer. Analysis of the events involved in regulation of differential Hox gene expression within organ fields will provide comprehensive insight into the mechanisms through which Hox genes shape the distinctive morphologies of animal body parts.