학술논문

Homothorax controls a binary Rhodopsin switch in Drosophila ocelli.
Document Type
Article
Source
PLoS Genetics. 7/27/2021, Vol. 17 Issue 7, p1-20. 20p.
Subject
*PHOTORECEPTORS
*RHODOPSIN
*VISUAL perception
*DROSOPHILA
*DROSOPHILA melanogaster
*SPECTRAL sensitivity
Language
ISSN
1553-7390
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, color or polarized light detection, and a triplet of ocelli that are thought to be critical during flight to detect horizon and movements. It is widely believed that the 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 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. Author summary: Sensory perception of light is mediated by specialized photoreceptor neurons of the eye. Each photoreceptor expresses unique photopigments called opsins and they are sensitive to particular wavelengths of light. In insects, ocelli and compound eyes are the main photosensory organs and they express different opsins. It is believed that opsins were duplicated during evolution to provide specificity to ocelli and the compound eye and this is corelated with their distinct functions. We show that Homothorax acts to control a binary Rhodopsin switch in the fruit fly Drosophila melanogaster to promote Rhodopsin 2 expression and represses Rhodopsin 1 expression in the ocelli. Genetic and molecular analysis showed that Homothorax acts through the promoters of rhosopsin 1 and rhosopsin 2 and controls their expression in the ocelli. We also show that Hth binding sites in the promoter region of rhodopsin 1 and rhodopsin 2 are conserved between different Drosophila species. We therefore proposed that Hth may have acted as a critical determinant during evolution which was required to provide specificity to the ocelli and compound eye by regulating a binary Rhodopsin switch in the ocelli. [ABSTRACT FROM AUTHOR]