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A G(o)-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii

BACKGROUND: The presence of photoreceptive molecules outside the eye is widespread among animals, yet their functions in the periphery are less well understood. Marine organisms, such as annelid worms, exhibit a ‘shadow reflex’, a defensive withdrawal behaviour triggered by a decrease in illuminatio...

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Autores principales: Ayers, Thomas, Tsukamoto, Hisao, Gühmann, Martin, Veedin Rajan, Vinoth Babu, Tessmar-Raible, Kristin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5904973/
https://www.ncbi.nlm.nih.gov/pubmed/29669554
http://dx.doi.org/10.1186/s12915-018-0505-8
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author Ayers, Thomas
Tsukamoto, Hisao
Gühmann, Martin
Veedin Rajan, Vinoth Babu
Tessmar-Raible, Kristin
author_facet Ayers, Thomas
Tsukamoto, Hisao
Gühmann, Martin
Veedin Rajan, Vinoth Babu
Tessmar-Raible, Kristin
author_sort Ayers, Thomas
collection PubMed
description BACKGROUND: The presence of photoreceptive molecules outside the eye is widespread among animals, yet their functions in the periphery are less well understood. Marine organisms, such as annelid worms, exhibit a ‘shadow reflex’, a defensive withdrawal behaviour triggered by a decrease in illumination. Herein, we examine the cellular and molecular underpinnings of this response, identifying a role for a photoreceptor molecule of the G(o)-opsin class in the shadow response of the marine bristle worm Platynereis dumerilii. RESULTS: We found Pdu-Go-opsin1 expression in single specialised cells located in adult Platynereis head and trunk appendages, known as cirri. Using gene knock-out technology and ablation approaches, we show that the presence of Go-opsin1 and the cirri is necessary for the shadow reflex. Consistently, quantification of the shadow reflex reveals a chromatic dependence upon light of approximately 500 nm in wavelength, matching the photoexcitation characteristics of the Platynereis Go-opsin1. However, the loss of Go-opsin1 does not abolish the shadow reflex completely, suggesting the existence of a compensatory mechanism, possibly acting through a ciliary-type opsin, Pdu-c-opsin2, with a Lambda(max) of approximately 490 nm. CONCLUSIONS: We show that a Go-opsin is necessary for the shadow reflex in a marine annelid, describing a functional example for a peripherally expressed photoreceptor, and suggesting that, in different species, distinct opsins contribute to varying degrees to the shadow reflex. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0505-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-59049732018-04-24 A G(o)-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii Ayers, Thomas Tsukamoto, Hisao Gühmann, Martin Veedin Rajan, Vinoth Babu Tessmar-Raible, Kristin BMC Biol Research Article BACKGROUND: The presence of photoreceptive molecules outside the eye is widespread among animals, yet their functions in the periphery are less well understood. Marine organisms, such as annelid worms, exhibit a ‘shadow reflex’, a defensive withdrawal behaviour triggered by a decrease in illumination. Herein, we examine the cellular and molecular underpinnings of this response, identifying a role for a photoreceptor molecule of the G(o)-opsin class in the shadow response of the marine bristle worm Platynereis dumerilii. RESULTS: We found Pdu-Go-opsin1 expression in single specialised cells located in adult Platynereis head and trunk appendages, known as cirri. Using gene knock-out technology and ablation approaches, we show that the presence of Go-opsin1 and the cirri is necessary for the shadow reflex. Consistently, quantification of the shadow reflex reveals a chromatic dependence upon light of approximately 500 nm in wavelength, matching the photoexcitation characteristics of the Platynereis Go-opsin1. However, the loss of Go-opsin1 does not abolish the shadow reflex completely, suggesting the existence of a compensatory mechanism, possibly acting through a ciliary-type opsin, Pdu-c-opsin2, with a Lambda(max) of approximately 490 nm. CONCLUSIONS: We show that a Go-opsin is necessary for the shadow reflex in a marine annelid, describing a functional example for a peripherally expressed photoreceptor, and suggesting that, in different species, distinct opsins contribute to varying degrees to the shadow reflex. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0505-8) contains supplementary material, which is available to authorized users. BioMed Central 2018-04-18 /pmc/articles/PMC5904973/ /pubmed/29669554 http://dx.doi.org/10.1186/s12915-018-0505-8 Text en © Tessmar-Raible et al. 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Ayers, Thomas
Tsukamoto, Hisao
Gühmann, Martin
Veedin Rajan, Vinoth Babu
Tessmar-Raible, Kristin
A G(o)-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii
title A G(o)-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii
title_full A G(o)-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii
title_fullStr A G(o)-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii
title_full_unstemmed A G(o)-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii
title_short A G(o)-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii
title_sort g(o)-type opsin mediates the shadow reflex in the annelid platynereis dumerilii
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5904973/
https://www.ncbi.nlm.nih.gov/pubmed/29669554
http://dx.doi.org/10.1186/s12915-018-0505-8
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