Homothorax controls a binary Rhodopsin switch in Drosophila ocelli.

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 wit...

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Autores principales: Abhishek Kumar Mishra, Cornelia Fritsch, Roumen Voutev, Richard S Mann, Simon G Sprecher
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Publicado: Public Library of Science (PLoS) 2021
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Acceso en línea:https://doaj.org/article/baf113dc68824bf98ae75a7cb72c4a97
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spelling oai:doaj.org-article:baf113dc68824bf98ae75a7cb72c4a972021-12-02T20:02:44ZHomothorax controls a binary Rhodopsin switch in Drosophila ocelli.1553-73901553-740410.1371/journal.pgen.1009460https://doaj.org/article/baf113dc68824bf98ae75a7cb72c4a972021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009460https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Visual 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.Abhishek Kumar MishraCornelia FritschRoumen VoutevRichard S MannSimon G SprecherPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 7, p e1009460 (2021)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Abhishek Kumar Mishra
Cornelia Fritsch
Roumen Voutev
Richard S Mann
Simon G Sprecher
Homothorax controls a binary Rhodopsin switch in Drosophila ocelli.
description 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.
format article
author Abhishek Kumar Mishra
Cornelia Fritsch
Roumen Voutev
Richard S Mann
Simon G Sprecher
author_facet Abhishek Kumar Mishra
Cornelia Fritsch
Roumen Voutev
Richard S Mann
Simon G Sprecher
author_sort Abhishek Kumar Mishra
title Homothorax controls a binary Rhodopsin switch in Drosophila ocelli.
title_short Homothorax controls a binary Rhodopsin switch in Drosophila ocelli.
title_full Homothorax controls a binary Rhodopsin switch in Drosophila ocelli.
title_fullStr Homothorax controls a binary Rhodopsin switch in Drosophila ocelli.
title_full_unstemmed Homothorax controls a binary Rhodopsin switch in Drosophila ocelli.
title_sort homothorax controls a binary rhodopsin switch in drosophila ocelli.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/baf113dc68824bf98ae75a7cb72c4a97
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AT corneliafritsch homothoraxcontrolsabinaryrhodopsinswitchindrosophilaocelli
AT roumenvoutev homothoraxcontrolsabinaryrhodopsinswitchindrosophilaocelli
AT richardsmann homothoraxcontrolsabinaryrhodopsinswitchindrosophilaocelli
AT simongsprecher homothoraxcontrolsabinaryrhodopsinswitchindrosophilaocelli
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