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

Abstract

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 evector 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. KEY WORDS: Drosophila, Retina, Patterning INTRODUCTIONThe ability of both vertebrates and invertebrates to detect the evector orientation of polarized light has been studied in great detail (for reviews, see Nilsson and Warrant, 1999;Wehner, 2001). The celestial pattern of polarized skylight provides an important orientation cue for navigating insects, such as honeybees, desert ants or monarch butterflies (reviewed by Rossel, 1993;Wehner, 2003). Ommatidia in the dorsal rim area (DRA) of the compound eye display important morphological specializations (Labhart and Meyer, 1999), making them potent polarization detectors (Hardie, 1985;Labhart et al., 1984;Stalleicken et al., 2006). The combination of behavioral experiments with molecular genetic tools in Drosophila confirmed that the DRA is both necessary and sufficient for polarization vision (Wehner and Strasser, 1985 et al., 2012). The retinal mosaic of Drosophila represents an excellent model for cell-fate specification in sensory epithelia (Johnston et al., 2011). However, although important progress has been made towards understanding the specification of DRA ommatidia (Tomlinson, 2003;Wernet et al., 2003), the network of transcription factors involved remains unclear.The Drosophila compound eye consists of ~800 unit eyes (ommatidia), each containing eight photoreceptor neurons (R1-8), pigment, cone, an...

The evolutionary diversity of insect retinal mosaics: common design principles and emerging molecular logic

“…Localized specification of Drosophila DRA ommatidia results from combining positional information provided by ‘dorsal selector genes’ in the retina (the transcription factors of the Iroquois complex, Iro-C ) with a diffusible signal emanating from the head cuticle all around the eye (Wingless, Wg; Figure 3C). As a result, the homeodomain transcription factor Homothorax (Hth) becomes expressed in DRA R7 and R8 cells (Figure 3D), where it is both necessary and sufficient to induce DRA fate by modulating the retinal transcriptional network in inner PRs together with Spalt [43,44,47,48]. …”

Modality-specific circuits for skylight orientation in the fly visual system

“…Importantly, a sharp boundary exists between polarization-sensitive DRA ommatidia and color-sensitive non-DRA ommatidia ( Figure 1B) 24,26,30 . This strict division is already detectable during mid-pupal stages, where DRA inner photoreceptors express the transcription factor Homothorax (Hth) that, when over-expressed, is sufficient to transform the entire retinal mosaic into a homogeneous field of DRA ommatidia ( Figure 1C) 26,31,34 . Interestingly, R8 cells in DRA ommatidia (here referred to as DRA.R8) resemble R7 cells in that they express an R7 Rhodopsin (Rh3), and down-regulate the crucial R8-specific transcription factor Senseless (Sens) around mid-pupation 26,31 .…”

“…This strict division is already detectable during mid-pupal stages, where DRA inner photoreceptors express the transcription factor Homothorax (Hth) that, when over-expressed, is sufficient to transform the entire retinal mosaic into a homogeneous field of DRA ommatidia ( Figure 1C) 26,31,34 . Interestingly, R8 cells in DRA ommatidia (here referred to as DRA.R8) resemble R7 cells in that they express an R7 Rhodopsin (Rh3), and down-regulate the crucial R8-specific transcription factor Senseless (Sens) around mid-pupation 26,31 . Furthermore, only in the DRA, R8 axons target to the deeper medulla layer M6, known to be the R7 target layer across the medulla 32 , whereas non-DRA R8 always terminate in layer M3 19 .…”

Generation and Evolution of Neural Cell Types and Circuits: Insights from the Drosophila Visual System

“…These species have lost the stochastic distribution of ommatidial types observed in many other species. Presumably, these specialized regions contain photoreceptors that exhibit novel properties, perhaps combining features of dorsal polarized light detectors of the Drosophila dorsal rim area (140, 141, 144) with properties of normal color-sensitive ventral photoreceptors. Little is known about what might have changed in the processing circuitry downstream of such changes to the retina, and this uncertainty provides opportunities for future research.…”