Iroquois Complex Genes Induce Co-Expression of rhodopsins in Drosophila

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Abstract
The Drosophila eye is a mosaic that results from the stochastic distribution of two ommatidial subtypes. Pale and yellow ommatidia can be distinguished by the expression of distinct rhodopsins and other pigments in their inner photoreceptors (R7 and R8), which are implicated in color vision. The pale subtype contains ultraviolet (UV)-absorbing Rh3 in R7 and blue-absorbing Rh5 in R8. The yellow subtype contains UV-absorbing Rh4 in R7 and green-absorbing Rh6 in R8. The exclusive expression of one rhodopsin per photoreceptor is a widespread phenomenon, although exceptions exist. The mechanisms leading to the exclusive expression or to co-expression of sensory receptors are currently not known. We describe a new class of ommatidia that co-express rh3 and rh4 in R7, but maintain normal exclusion between rh5 and rh6 in R8. These ommatidia, which are localized in the dorsal eye, result from the expansion of rh3 into the yellow-R7 subtype. Genes from the Iroquois Complex (Iro-C) are necessary and sufficient to induce co-expression in yR7. Iro-C genes allow photoreceptors to break the “one receptor–one neuron” rule, leading to a novel subtype of broad-spectrum UV- and green-sensitive ommatidia. Most sensory systems follow the rule “one receptor molecule per receptor cell.” For example, photoreceptors in the fly eye and cones in the human eye each express only one light-sensitive rhodopsin. Rhodopsins are G-coupled protein receptors, a class of ancient signaling molecules that mediate not just vision but also the sense of smell, the inflammatory response, and other physiological processes. However, the mechanisms that regulate mutual exclusion of receptor genes in the visual and olfactory systems are poorly understood. Each ommatidium in the fly eye consists of eight photoreceptors (R1–R8); six of which mediate broad-spectrum motion vision (R1–R6) and two that mediate color vision (R7 and R8). We identified a new class of photoreceptors in the fly retina that violates the one rhodopsin–one receptor rule. This subset of ommatidia, located in the dorsal third of the eye, co-expresses two ultraviolet-sensitive rhodospins (rh3 and rh4) in R7, while maintaining discrimination between green and blue opsins in R8. We took advantage of the genetic tools offered by the fruit fly to show that this co-expression depends on the Iroquois Complex (Iro-C) genes that are both necessary and sufficient to allow the two ultraviolet-sensitive rhosopsins to be expressed in the same R7 cell. These results shed new light on the mechanisms regulating co-expression of rhodopsins in the eye, and may well have implications for regulating co-expression in olfactory receptors and other G-protein coupled systems.