Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae

The larval stages of polychaete annelids are often responsive to light and can possess one to six eyes. The early trochophore larvae of the errant annelid Platynereis dumerilii have a single pair of ventral eyespots, whereas older nectochaete larvae have an additional two pairs of dorsal eyes that w...

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Main Authors: Randel, Nadine, Bezares-Calderón, Luis A., Gühmann, Martin, Shahidi, Réza, Jékely, Gáspár
Format: Online
Language:English
Published: Oxford University Press 2013
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3687135/
id pubmed-3687135
recordtype oai_dc
spelling pubmed-36871352013-06-20 Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae Randel, Nadine Bezares-Calderón, Luis A. Gühmann, Martin Shahidi, Réza Jékely, Gáspár Integrating Genomics with Comparative Vision Research of the Invertebrates The larval stages of polychaete annelids are often responsive to light and can possess one to six eyes. The early trochophore larvae of the errant annelid Platynereis dumerilii have a single pair of ventral eyespots, whereas older nectochaete larvae have an additional two pairs of dorsal eyes that will develop into the adult eyes. Early Platynereis trochophores show robust positive phototaxis starting on the first day of development. Even though the mechanism of phototaxis in Platynereis early trochophore larvae is well understood, no photopigment (opsin) expression has yet been described in this stage. In late trochophore larvae, a rhabdomeric-type opsin, r-opsin1, expressed in both the eyespots and the adult eyes has already been reported. Here, we identify another Platynereis rhabdomeric opsin, r-opsin3, that is expressed in a single photoreceptor in the eyespots in early trochophores, suggesting that it mediates early larval phototaxis. We also show that r-opsin1 and r-opsin3 are expressed in adjacent photoreceptor cells in the eyespots in later stages, indicating that a second eyespot-photoreceptor differentiates in late trochophore larvae. Using serial transmission electron microscopy (TEM), we identified and reconstructed both photoreceptors and a pigment cell in the late larval eyespot. We also characterized opsin expression in the adult eyes and found that the two opsins co-express there in several photoreceptor cells. Using antibodies recognizing r-opsin1 and r-opsin3 proteins, we demonstrate that both opsins localize to the rhabdomere in all six eyes. In addition, we found that r-opsin1 mRNA is localized to, and translated in, the projections of the adult eyes. The specific changes we describe in opsin transcription and translation and in the cellular complement suggest that the six larval eyes undergo spectral and functional maturation during the early planktonic phase of the Platynereis life cycle. Oxford University Press 2013-07 2013-05-10 /pmc/articles/PMC3687135/ /pubmed/23667045 http://dx.doi.org/10.1093/icb/ict046 Text en © The Author 2013. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. http://creativecommons.org/licenses/by/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Randel, Nadine
Bezares-Calderón, Luis A.
Gühmann, Martin
Shahidi, Réza
Jékely, Gáspár
spellingShingle Randel, Nadine
Bezares-Calderón, Luis A.
Gühmann, Martin
Shahidi, Réza
Jékely, Gáspár
Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae
author_facet Randel, Nadine
Bezares-Calderón, Luis A.
Gühmann, Martin
Shahidi, Réza
Jékely, Gáspár
author_sort Randel, Nadine
title Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae
title_short Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae
title_full Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae
title_fullStr Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae
title_full_unstemmed Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae
title_sort expression dynamics and protein localization of rhabdomeric opsins in platynereis larvae
description The larval stages of polychaete annelids are often responsive to light and can possess one to six eyes. The early trochophore larvae of the errant annelid Platynereis dumerilii have a single pair of ventral eyespots, whereas older nectochaete larvae have an additional two pairs of dorsal eyes that will develop into the adult eyes. Early Platynereis trochophores show robust positive phototaxis starting on the first day of development. Even though the mechanism of phototaxis in Platynereis early trochophore larvae is well understood, no photopigment (opsin) expression has yet been described in this stage. In late trochophore larvae, a rhabdomeric-type opsin, r-opsin1, expressed in both the eyespots and the adult eyes has already been reported. Here, we identify another Platynereis rhabdomeric opsin, r-opsin3, that is expressed in a single photoreceptor in the eyespots in early trochophores, suggesting that it mediates early larval phototaxis. We also show that r-opsin1 and r-opsin3 are expressed in adjacent photoreceptor cells in the eyespots in later stages, indicating that a second eyespot-photoreceptor differentiates in late trochophore larvae. Using serial transmission electron microscopy (TEM), we identified and reconstructed both photoreceptors and a pigment cell in the late larval eyespot. We also characterized opsin expression in the adult eyes and found that the two opsins co-express there in several photoreceptor cells. Using antibodies recognizing r-opsin1 and r-opsin3 proteins, we demonstrate that both opsins localize to the rhabdomere in all six eyes. In addition, we found that r-opsin1 mRNA is localized to, and translated in, the projections of the adult eyes. The specific changes we describe in opsin transcription and translation and in the cellular complement suggest that the six larval eyes undergo spectral and functional maturation during the early planktonic phase of the Platynereis life cycle.
publisher Oxford University Press
publishDate 2013
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3687135/
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