Homothorax and Extradenticle alter the transcription factor network in Drosophila ommatidia at the dorsal rim of the retina.

A narrow band of ommatidia in the dorsal periphery of the Drosophila retina called the dorsal rim area (DRA) act as detectors for polarized light. The transcription factor Homothorax (Hth) is expressed in DRA inner photoreceptors R7 and R8 and is both necessary and sufficient to induce the DRA fate, including specialized morphology and unique Rhodopsin expression. Hth expression is the result of Wingless (Wg) pathway activity at the eye margins and restriction to the dorsal eye by the selector genes of the Iroquois complex (Iro-C). However, how the DRA is limited to exactly one or two ommatidial rows is not known. Although several factors regulating the Drosophila retinal mosaic are expressed in DRA ommatidia, the role of Hth in this transcriptional network is uncharacterized. Here we show that Hth functions together with its co-factor Extradenticle (Exd) to repress the R8-specific factor Senseless (Sens) in DRA R8 cells, allowing expression of an ultraviolet-sensitive R7 Rhodopsin (Rh3). Furthermore, Hth/Exd act in concert with the transcriptional activators Orthodenticle (Otd) and Spalt (Sal), to activate expression of Rh3 in the DRA. The resulting monochromatic coupling of Rh3 between R7 and R8 in DRA ommatidia is important for comparing celestial e-vector orientation rather than wavelengths. Finally, we show that Hth expression expands to many ommatidial rows in regulatory mutants of optomotorblind (omb), a transcription factor transducing Wg signaling at the dorsal and ventral eye poles. Therefore, locally restricted recruitment of the DRA-specific factor Hth alters the transcriptional network that regulates Rhodopsin expression across ommatidia.

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