Homothorax Controls a Binary Rhodopsin Switch inDrosophilaOcelli

Abstract

Visual perception of the environment is mediated by specialized photoreceptor (PR) neurons of the eye. Each PR expresses photosensitive opsins, which are activated by a particular wavelength of light. In most insects, the visual system comprises a pair of compound eyes that are mainly associated with motion detection, color or polarized light perception and a triplet of ocelli that are thought to be critical during flight to detect horizon and movements. It is widely believed that evolutionary diversification of compound eye and ocelli in insects occurred from an ancestral visual organ around 500 million years ago. Concurrently, opsin genes were also duplicated to provide distinct spectral sensitivities to different PRs of compound eye and ocelli. In the fruit fly Drosophila melanogaster, Rhodopsin1 (Rh1) and Rh2 are closely related opsins that are originated from the duplication of a single ancestral gene. However, in the visual organs, Rh2 is uniquely expressed in ocelli whereas Rh1 is uniquely expressed in outer PRs of the compound eye. It is currently unknown how this differential expression of Rh1 and Rh2 in the two visual organs is controlled to provide unique spectral sensitivities to ocelli and compound eyes. Here, we show that Homothorax (Hth) is expressed in ocelli and confers proper rhodopsin expression. We find that Hth controls a binary rhodopsin switch in ocelli to promote Rh2 expression and repress Rh1 expression. Genetic and molecular analysis of rh1 and rh2 supports that Hth acts through their promoters to regulate rhodopsin expression in the ocelli. Finally, we also show that when ectopically expressed in the retina, hth is sufficient to induce Rh2 expression only at the outer PRs in a cell autonomous manner. We therefore propose that the diversification of rhodpsins in the ocelli and retinal outer PRs occurred by duplication of an ancestral gene, which is under the control of Homothorax.

The genome of the blind bee louse fly reveals deep convergences with its social host and illuminates Drosophila origins

“…72 Therefore, the retention of these rhodopsins in the bee louse fly could mainly be due to their unconventional functions. On the other hand, the rhodopsin Rh2, which is exclusively expressed in the ocelli and used for horizon detection in D. melanogaster 73 , is among those lost in the bee louse fly, in agreement with the loss of the ocelli. Regression of the visual system and its underlying opsin genes is common in animals inhabiting dark environments, such as fossorial mammals 74 and cavefishes, 75 representing a major example of deep convergences.…”

The genome of the blind bee louse fly reveals deep convergences with its social host and illuminates Drosophila origins

“…69 Therefore, the retention of these rhodopsins in the bee louse fly could mainly be due to their unconventional functions. On the other hand, the rhodopsin Rh2, which is exclusively expressed in the ocelli and used for horizon detection in D. melanogaster 70 , is among those lost in the bee louse fly, in agreement with the loss of the ocelli. Regression of the visual system and its underlying opsin genes is common in animals inhabiting dark environments, such as fossorial mammals 71 and cavefishes, 72 representing a major example of deep convergences.…”