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Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation

To survive, organisms need to precisely respond to various environmental factors, such as light and gravity. Among these, light is so important for most life on Earth that light-response systems have become extraordinarily developed during evolution, especially in multicellular animals. A combinatio...

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Autores principales: Yaguchi, Shunsuke, Taniguchi, Yuri, Suzuki, Haruka, Kamata, Mai, Yaguchi, Junko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8830728/
https://www.ncbi.nlm.nih.gov/pubmed/35143488
http://dx.doi.org/10.1371/journal.pgen.1010033
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author Yaguchi, Shunsuke
Taniguchi, Yuri
Suzuki, Haruka
Kamata, Mai
Yaguchi, Junko
author_facet Yaguchi, Shunsuke
Taniguchi, Yuri
Suzuki, Haruka
Kamata, Mai
Yaguchi, Junko
author_sort Yaguchi, Shunsuke
collection PubMed
description To survive, organisms need to precisely respond to various environmental factors, such as light and gravity. Among these, light is so important for most life on Earth that light-response systems have become extraordinarily developed during evolution, especially in multicellular animals. A combination of photoreceptors, nervous system components, and effectors allows these animals to respond to light stimuli. In most macroscopic animals, muscles function as effectors responding to light, and in some microscopic aquatic animals, cilia play a role. It is likely that the cilia-based response was the first to develop and that it has been substituted by the muscle-based response along with increases in body size. However, although the function of muscle appears prominent, it is poorly understood whether ciliary responses to light are present and/or functional, especially in deuterostomes, because it is possible that these responses are too subtle to be observed, unlike muscle responses. Here, we show that planktonic sea urchin larvae reverse their swimming direction due to the inhibitory effect of light on the cholinergic neuron signaling>forward swimming pathway. We found that strong photoirradiation of larvae that stay on the surface of seawater immediately drives the larvae away from the surface due to backward swimming. When Opsin2, which is expressed in mesenchymal cells in larval arms, is knocked down, the larvae do not show backward swimming under photoirradiation. Although Opsin2-expressing cells are not neuronal cells, immunohistochemical analysis revealed that they directly attach to cholinergic neurons, which are thought to regulate forward swimming. These data indicate that light, through Opsin2, inhibits the activity of cholinergic signaling, which normally promotes larval forward swimming, and that the light-dependent ciliary response is present in deuterostomes. These findings shed light on how light-responsive tissues/organelles have been conserved and diversified during evolution.
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spelling pubmed-88307282022-02-11 Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation Yaguchi, Shunsuke Taniguchi, Yuri Suzuki, Haruka Kamata, Mai Yaguchi, Junko PLoS Genet Research Article To survive, organisms need to precisely respond to various environmental factors, such as light and gravity. Among these, light is so important for most life on Earth that light-response systems have become extraordinarily developed during evolution, especially in multicellular animals. A combination of photoreceptors, nervous system components, and effectors allows these animals to respond to light stimuli. In most macroscopic animals, muscles function as effectors responding to light, and in some microscopic aquatic animals, cilia play a role. It is likely that the cilia-based response was the first to develop and that it has been substituted by the muscle-based response along with increases in body size. However, although the function of muscle appears prominent, it is poorly understood whether ciliary responses to light are present and/or functional, especially in deuterostomes, because it is possible that these responses are too subtle to be observed, unlike muscle responses. Here, we show that planktonic sea urchin larvae reverse their swimming direction due to the inhibitory effect of light on the cholinergic neuron signaling>forward swimming pathway. We found that strong photoirradiation of larvae that stay on the surface of seawater immediately drives the larvae away from the surface due to backward swimming. When Opsin2, which is expressed in mesenchymal cells in larval arms, is knocked down, the larvae do not show backward swimming under photoirradiation. Although Opsin2-expressing cells are not neuronal cells, immunohistochemical analysis revealed that they directly attach to cholinergic neurons, which are thought to regulate forward swimming. These data indicate that light, through Opsin2, inhibits the activity of cholinergic signaling, which normally promotes larval forward swimming, and that the light-dependent ciliary response is present in deuterostomes. These findings shed light on how light-responsive tissues/organelles have been conserved and diversified during evolution. Public Library of Science 2022-02-10 /pmc/articles/PMC8830728/ /pubmed/35143488 http://dx.doi.org/10.1371/journal.pgen.1010033 Text en © 2022 Yaguchi et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Yaguchi, Shunsuke
Taniguchi, Yuri
Suzuki, Haruka
Kamata, Mai
Yaguchi, Junko
Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation
title Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation
title_full Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation
title_fullStr Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation
title_full_unstemmed Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation
title_short Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation
title_sort planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8830728/
https://www.ncbi.nlm.nih.gov/pubmed/35143488
http://dx.doi.org/10.1371/journal.pgen.1010033
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