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Ion channel profiling of the Lymnaea stagnalis ganglia via transcriptome analysis

BACKGROUND: The pond snail Lymnaea stagnalis (L. stagnalis) has been widely used as a model organism in neurobiology, ecotoxicology, and parasitology due to the relative simplicity of its central nervous system (CNS). However, its usefulness is restricted by a limited availability of transcriptome d...

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Autores principales: Dong, Nancy, Bandura, Julia, Zhang, Zhaolei, Wang, Yan, Labadie, Karine, Noel, Benjamin, Davison, Angus, Koene, Joris M., Sun, Hong-Shuo, Coutellec, Marie-Agnès, Feng, Zhong-Ping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7789530/
https://www.ncbi.nlm.nih.gov/pubmed/33407100
http://dx.doi.org/10.1186/s12864-020-07287-2
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author Dong, Nancy
Bandura, Julia
Zhang, Zhaolei
Wang, Yan
Labadie, Karine
Noel, Benjamin
Davison, Angus
Koene, Joris M.
Sun, Hong-Shuo
Coutellec, Marie-Agnès
Feng, Zhong-Ping
author_facet Dong, Nancy
Bandura, Julia
Zhang, Zhaolei
Wang, Yan
Labadie, Karine
Noel, Benjamin
Davison, Angus
Koene, Joris M.
Sun, Hong-Shuo
Coutellec, Marie-Agnès
Feng, Zhong-Ping
author_sort Dong, Nancy
collection PubMed
description BACKGROUND: The pond snail Lymnaea stagnalis (L. stagnalis) has been widely used as a model organism in neurobiology, ecotoxicology, and parasitology due to the relative simplicity of its central nervous system (CNS). However, its usefulness is restricted by a limited availability of transcriptome data. While sequence information for the L. stagnalis CNS transcripts has been obtained from EST libraries and a de novo RNA-seq assembly, the quality of these assemblies is limited by a combination of low coverage of EST libraries, the fragmented nature of de novo assemblies, and lack of reference genome. RESULTS: In this study, taking advantage of the recent availability of a preliminary L. stagnalis genome, we generated an RNA-seq library from the adult L. stagnalis CNS, using a combination of genome-guided and de novo assembly programs to identify 17,832 protein-coding L. stagnalis transcripts. We combined our library with existing resources to produce a transcript set with greater sequence length, completeness, and diversity than previously available ones. Using our assembly and functional domain analysis, we profiled L. stagnalis CNS transcripts encoding ion channels and ionotropic receptors, which are key proteins for CNS function, and compared their sequences to other vertebrate and invertebrate model organisms. Interestingly, L. stagnalis transcripts encoding numerous putative Ca(2+) channels showed the most sequence similarity to those of Mus musculus, Danio rerio, Xenopus tropicalis, Drosophila melanogaster, and Caenorhabditis elegans, suggesting that many calcium channel-related signaling pathways may be evolutionarily conserved. CONCLUSIONS: Our study provides the most thorough characterization to date of the L. stagnalis transcriptome and provides insights into differences between vertebrates and invertebrates in CNS transcript diversity, according to function and protein class. Furthermore, this study provides a complete characterization of the ion channels of Lymnaea stagnalis, opening new avenues for future research on fundamental neurobiological processes in this model system. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-020-07287-2.
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spelling pubmed-77895302021-01-07 Ion channel profiling of the Lymnaea stagnalis ganglia via transcriptome analysis Dong, Nancy Bandura, Julia Zhang, Zhaolei Wang, Yan Labadie, Karine Noel, Benjamin Davison, Angus Koene, Joris M. Sun, Hong-Shuo Coutellec, Marie-Agnès Feng, Zhong-Ping BMC Genomics Research Article BACKGROUND: The pond snail Lymnaea stagnalis (L. stagnalis) has been widely used as a model organism in neurobiology, ecotoxicology, and parasitology due to the relative simplicity of its central nervous system (CNS). However, its usefulness is restricted by a limited availability of transcriptome data. While sequence information for the L. stagnalis CNS transcripts has been obtained from EST libraries and a de novo RNA-seq assembly, the quality of these assemblies is limited by a combination of low coverage of EST libraries, the fragmented nature of de novo assemblies, and lack of reference genome. RESULTS: In this study, taking advantage of the recent availability of a preliminary L. stagnalis genome, we generated an RNA-seq library from the adult L. stagnalis CNS, using a combination of genome-guided and de novo assembly programs to identify 17,832 protein-coding L. stagnalis transcripts. We combined our library with existing resources to produce a transcript set with greater sequence length, completeness, and diversity than previously available ones. Using our assembly and functional domain analysis, we profiled L. stagnalis CNS transcripts encoding ion channels and ionotropic receptors, which are key proteins for CNS function, and compared their sequences to other vertebrate and invertebrate model organisms. Interestingly, L. stagnalis transcripts encoding numerous putative Ca(2+) channels showed the most sequence similarity to those of Mus musculus, Danio rerio, Xenopus tropicalis, Drosophila melanogaster, and Caenorhabditis elegans, suggesting that many calcium channel-related signaling pathways may be evolutionarily conserved. CONCLUSIONS: Our study provides the most thorough characterization to date of the L. stagnalis transcriptome and provides insights into differences between vertebrates and invertebrates in CNS transcript diversity, according to function and protein class. Furthermore, this study provides a complete characterization of the ion channels of Lymnaea stagnalis, opening new avenues for future research on fundamental neurobiological processes in this model system. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-020-07287-2. BioMed Central 2021-01-06 /pmc/articles/PMC7789530/ /pubmed/33407100 http://dx.doi.org/10.1186/s12864-020-07287-2 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research Article
Dong, Nancy
Bandura, Julia
Zhang, Zhaolei
Wang, Yan
Labadie, Karine
Noel, Benjamin
Davison, Angus
Koene, Joris M.
Sun, Hong-Shuo
Coutellec, Marie-Agnès
Feng, Zhong-Ping
Ion channel profiling of the Lymnaea stagnalis ganglia via transcriptome analysis
title Ion channel profiling of the Lymnaea stagnalis ganglia via transcriptome analysis
title_full Ion channel profiling of the Lymnaea stagnalis ganglia via transcriptome analysis
title_fullStr Ion channel profiling of the Lymnaea stagnalis ganglia via transcriptome analysis
title_full_unstemmed Ion channel profiling of the Lymnaea stagnalis ganglia via transcriptome analysis
title_short Ion channel profiling of the Lymnaea stagnalis ganglia via transcriptome analysis
title_sort ion channel profiling of the lymnaea stagnalis ganglia via transcriptome analysis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7789530/
https://www.ncbi.nlm.nih.gov/pubmed/33407100
http://dx.doi.org/10.1186/s12864-020-07287-2
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