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Gene expression profiling of trout muscle during flesh quality recovery following spawning

BACKGROUND: Sexual maturation causes loss of fish muscle mass and deterioration of fillet quality attributes that prevent market success. We recently showed that fillet yield and flesh quality recover in female trout after spawning. To gain insight into the molecular mechanisms regulating flesh qual...

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Autores principales: Ahongo, Yéléhi-Diane, Le Cam, Aurélie, Montfort, Jérôme, Bugeon, Jérôme, Lefèvre, Florence, Rescan, Pierre-Yves
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8725336/
https://www.ncbi.nlm.nih.gov/pubmed/34983401
http://dx.doi.org/10.1186/s12864-021-08228-3
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author Ahongo, Yéléhi-Diane
Le Cam, Aurélie
Montfort, Jérôme
Bugeon, Jérôme
Lefèvre, Florence
Rescan, Pierre-Yves
author_facet Ahongo, Yéléhi-Diane
Le Cam, Aurélie
Montfort, Jérôme
Bugeon, Jérôme
Lefèvre, Florence
Rescan, Pierre-Yves
author_sort Ahongo, Yéléhi-Diane
collection PubMed
description BACKGROUND: Sexual maturation causes loss of fish muscle mass and deterioration of fillet quality attributes that prevent market success. We recently showed that fillet yield and flesh quality recover in female trout after spawning. To gain insight into the molecular mechanisms regulating flesh quality recovery, we used an Agilent-based microarray platform to conduct a large-scale time course analysis of gene expression in female trout white muscle from spawning to 33 weeks post-spawning. RESULTS: In sharp contrast to the situation at spawning, muscle transcriptome of female trout at 33 weeks after spawning was highly similar to that of female trout of the same cohort that did not spawn, which is consistent with the post-spawning flesh quality recovery. Large-scale time course analysis of gene expression in trout muscle during flesh quality recovery following spawning led to the identification of approximately 3340 unique differentially expressed genes that segregated into four major clusters with distinct temporal expression profiles and functional categories. The first cluster contained approximately 1350 genes with high expression at spawning and downregulation after spawning and was enriched with genes linked to mitochondrial ATP synthesis, fatty acid catabolism and proteolysis. A second cluster of approximately 540 genes with transient upregulation 2 to 8 weeks after spawning was enriched with genes involved in transcription, RNA processing, translation, ribosome biogenesis and protein folding. A third cluster containing approximately 300 genes upregulated 4 to 13 weeks after spawning was enriched with genes encoding ribosomal subunits or regulating protein folding. Finally, a fourth cluster that contained approximately 940 genes with upregulation 8 to 24 weeks after spawning, was dominated by genes encoding myofibrillar proteins and extracellular matrix components and genes involved in glycolysis. CONCLUSION: Overall, our study indicates that white muscle tissue restoration and flesh quality recovery after spawning are associated with transcriptional changes promoting anaerobic ATP production, muscle fibre hypertrophic growth and extracellular matrix remodelling. The generation of the first database of genes associated with post-spawning muscle recovery may provide insights into the molecular and cellular mechanisms controlling muscle yield and fillet quality in fish and provide a useful list of potential genetic markers for these traits. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-08228-3.
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spelling pubmed-87253362022-01-06 Gene expression profiling of trout muscle during flesh quality recovery following spawning Ahongo, Yéléhi-Diane Le Cam, Aurélie Montfort, Jérôme Bugeon, Jérôme Lefèvre, Florence Rescan, Pierre-Yves BMC Genomics Research BACKGROUND: Sexual maturation causes loss of fish muscle mass and deterioration of fillet quality attributes that prevent market success. We recently showed that fillet yield and flesh quality recover in female trout after spawning. To gain insight into the molecular mechanisms regulating flesh quality recovery, we used an Agilent-based microarray platform to conduct a large-scale time course analysis of gene expression in female trout white muscle from spawning to 33 weeks post-spawning. RESULTS: In sharp contrast to the situation at spawning, muscle transcriptome of female trout at 33 weeks after spawning was highly similar to that of female trout of the same cohort that did not spawn, which is consistent with the post-spawning flesh quality recovery. Large-scale time course analysis of gene expression in trout muscle during flesh quality recovery following spawning led to the identification of approximately 3340 unique differentially expressed genes that segregated into four major clusters with distinct temporal expression profiles and functional categories. The first cluster contained approximately 1350 genes with high expression at spawning and downregulation after spawning and was enriched with genes linked to mitochondrial ATP synthesis, fatty acid catabolism and proteolysis. A second cluster of approximately 540 genes with transient upregulation 2 to 8 weeks after spawning was enriched with genes involved in transcription, RNA processing, translation, ribosome biogenesis and protein folding. A third cluster containing approximately 300 genes upregulated 4 to 13 weeks after spawning was enriched with genes encoding ribosomal subunits or regulating protein folding. Finally, a fourth cluster that contained approximately 940 genes with upregulation 8 to 24 weeks after spawning, was dominated by genes encoding myofibrillar proteins and extracellular matrix components and genes involved in glycolysis. CONCLUSION: Overall, our study indicates that white muscle tissue restoration and flesh quality recovery after spawning are associated with transcriptional changes promoting anaerobic ATP production, muscle fibre hypertrophic growth and extracellular matrix remodelling. The generation of the first database of genes associated with post-spawning muscle recovery may provide insights into the molecular and cellular mechanisms controlling muscle yield and fillet quality in fish and provide a useful list of potential genetic markers for these traits. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-08228-3. BioMed Central 2022-01-04 /pmc/articles/PMC8725336/ /pubmed/34983401 http://dx.doi.org/10.1186/s12864-021-08228-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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
Ahongo, Yéléhi-Diane
Le Cam, Aurélie
Montfort, Jérôme
Bugeon, Jérôme
Lefèvre, Florence
Rescan, Pierre-Yves
Gene expression profiling of trout muscle during flesh quality recovery following spawning
title Gene expression profiling of trout muscle during flesh quality recovery following spawning
title_full Gene expression profiling of trout muscle during flesh quality recovery following spawning
title_fullStr Gene expression profiling of trout muscle during flesh quality recovery following spawning
title_full_unstemmed Gene expression profiling of trout muscle during flesh quality recovery following spawning
title_short Gene expression profiling of trout muscle during flesh quality recovery following spawning
title_sort gene expression profiling of trout muscle during flesh quality recovery following spawning
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8725336/
https://www.ncbi.nlm.nih.gov/pubmed/34983401
http://dx.doi.org/10.1186/s12864-021-08228-3
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