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Thermal plasticity of the miRNA transcriptome during Senegalese sole development

BACKGROUND: Several miRNAs are known to control myogenesis in vertebrates. Some of them are specifically expressed in muscle while others have a broader tissue expression but are still involved in establishing the muscle phenotype. In teleosts, water temperature markedly affects embryonic developmen...

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Autores principales: Campos, Catarina, Sundaram, Arvind YM, Valente, Luisa MP, Conceição, Luis EC, Engrola, Sofia, Fernandes, Jorge MO
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4097167/
https://www.ncbi.nlm.nih.gov/pubmed/24966054
http://dx.doi.org/10.1186/1471-2164-15-525
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author Campos, Catarina
Sundaram, Arvind YM
Valente, Luisa MP
Conceição, Luis EC
Engrola, Sofia
Fernandes, Jorge MO
author_facet Campos, Catarina
Sundaram, Arvind YM
Valente, Luisa MP
Conceição, Luis EC
Engrola, Sofia
Fernandes, Jorge MO
author_sort Campos, Catarina
collection PubMed
description BACKGROUND: Several miRNAs are known to control myogenesis in vertebrates. Some of them are specifically expressed in muscle while others have a broader tissue expression but are still involved in establishing the muscle phenotype. In teleosts, water temperature markedly affects embryonic development and larval growth. It has been previously shown that higher embryonic temperatures promoted faster development and increased size of Senegalese sole (Solea senegalensis) larvae relatively to a lower temperature. The role of miRNAs in thermal-plasticity of growth is hitherto unknown. Hence, we have used high-throughput SOLiD sequencing to determine potential changes in the miRNA transcriptome in Senegalese sole embryos that were incubated at 15°C or 21°C until hatching and then reared at a common temperature of 21°C. RESULTS: We have identified 320 conserved miRNAs in Senegalese sole, of which 48 had not been previously described in teleosts. mir-17a-5p, mir-26a, mir-130c, mir-206-3p, mir-181a-5p, mir-181a-3p and mir-199a-5p expression levels were further validated by RT- qPCR. The majority of miRNAs were dynamically expressed during early development, with peaks of expression at pre-metamorphosis or metamorphosis. Also, a higher incubation temperature (21°C) was associated with expression of some miRNAs positively related with growth (e.g., miR-17a, miR-181-5p and miR-206) during segmentation and at hatching. Target prediction revealed that these miRNAs may regulate myogenesis through MAPK and mTOR pathways. Expression of miRNAs involved in lipid metabolism and energy production (e.g., miR-122) also differed between temperatures. A miRNA that can potentially target calpain (miR-181-3p), and therefore negatively regulate myogenesis, was preferentially expressed during segmentation at 15°C compared to 21°C. CONCLUSIONS: Temperature has a strong influence on expression of miRNAs during embryonic and larval development in fish. Higher expression levels of miR-17a, miR-181-5p and miR-206-3p and down-regulation of miR-181a-3p at 21°C may promote myogenesis and are in agreement with previous studies in Senegalese sole, which reported enhanced growth at higher embryonic temperatures compared to 15°C. Moreover, miRNAs involved in lipid metabolism and energy production may also contribute to increased larval growth at 21°C compared to 15°C. Taken together, our data indicate that miRNAs may play a role in temperature-induced phenotypic plasticity of growth in teleosts. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-525) contains supplementary material, which is available to authorized users.
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spelling pubmed-40971672014-07-18 Thermal plasticity of the miRNA transcriptome during Senegalese sole development Campos, Catarina Sundaram, Arvind YM Valente, Luisa MP Conceição, Luis EC Engrola, Sofia Fernandes, Jorge MO BMC Genomics Research Article BACKGROUND: Several miRNAs are known to control myogenesis in vertebrates. Some of them are specifically expressed in muscle while others have a broader tissue expression but are still involved in establishing the muscle phenotype. In teleosts, water temperature markedly affects embryonic development and larval growth. It has been previously shown that higher embryonic temperatures promoted faster development and increased size of Senegalese sole (Solea senegalensis) larvae relatively to a lower temperature. The role of miRNAs in thermal-plasticity of growth is hitherto unknown. Hence, we have used high-throughput SOLiD sequencing to determine potential changes in the miRNA transcriptome in Senegalese sole embryos that were incubated at 15°C or 21°C until hatching and then reared at a common temperature of 21°C. RESULTS: We have identified 320 conserved miRNAs in Senegalese sole, of which 48 had not been previously described in teleosts. mir-17a-5p, mir-26a, mir-130c, mir-206-3p, mir-181a-5p, mir-181a-3p and mir-199a-5p expression levels were further validated by RT- qPCR. The majority of miRNAs were dynamically expressed during early development, with peaks of expression at pre-metamorphosis or metamorphosis. Also, a higher incubation temperature (21°C) was associated with expression of some miRNAs positively related with growth (e.g., miR-17a, miR-181-5p and miR-206) during segmentation and at hatching. Target prediction revealed that these miRNAs may regulate myogenesis through MAPK and mTOR pathways. Expression of miRNAs involved in lipid metabolism and energy production (e.g., miR-122) also differed between temperatures. A miRNA that can potentially target calpain (miR-181-3p), and therefore negatively regulate myogenesis, was preferentially expressed during segmentation at 15°C compared to 21°C. CONCLUSIONS: Temperature has a strong influence on expression of miRNAs during embryonic and larval development in fish. Higher expression levels of miR-17a, miR-181-5p and miR-206-3p and down-regulation of miR-181a-3p at 21°C may promote myogenesis and are in agreement with previous studies in Senegalese sole, which reported enhanced growth at higher embryonic temperatures compared to 15°C. Moreover, miRNAs involved in lipid metabolism and energy production may also contribute to increased larval growth at 21°C compared to 15°C. Taken together, our data indicate that miRNAs may play a role in temperature-induced phenotypic plasticity of growth in teleosts. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-525) contains supplementary material, which is available to authorized users. BioMed Central 2014-06-25 /pmc/articles/PMC4097167/ /pubmed/24966054 http://dx.doi.org/10.1186/1471-2164-15-525 Text en © Campos et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Campos, Catarina
Sundaram, Arvind YM
Valente, Luisa MP
Conceição, Luis EC
Engrola, Sofia
Fernandes, Jorge MO
Thermal plasticity of the miRNA transcriptome during Senegalese sole development
title Thermal plasticity of the miRNA transcriptome during Senegalese sole development
title_full Thermal plasticity of the miRNA transcriptome during Senegalese sole development
title_fullStr Thermal plasticity of the miRNA transcriptome during Senegalese sole development
title_full_unstemmed Thermal plasticity of the miRNA transcriptome during Senegalese sole development
title_short Thermal plasticity of the miRNA transcriptome during Senegalese sole development
title_sort thermal plasticity of the mirna transcriptome during senegalese sole development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4097167/
https://www.ncbi.nlm.nih.gov/pubmed/24966054
http://dx.doi.org/10.1186/1471-2164-15-525
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