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Transcriptional Assessment by Microarray Analysis and Large-Scale Meta-analysis of the Metabolic Capacity of Cardiac and Skeletal Muscle Tissues to Cope With Reduced Nutrient Availability in Gilthead Sea Bream (Sparus aurata L.)

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Abstract

The effects of nutrient availability on the transcriptome of cardiac and skeletal muscle tissues were assessed in juvenile gilthead sea bream fed with a standard diet at two feeding levels: (1) full ration size and (2) 70 % satiation followed by a finishing phase at the maintenance ration. Microarray analysis evidenced a characteristic transcriptomic profile for each muscle tissue following changes in oxidative capacity (heart > red skeletal muscle > white skeletal muscle). The transcriptome of heart and secondly that of red skeletal muscle were highly responsive to nutritional changes, whereas that of glycolytic white skeletal muscle showed less ability to respond. The highly expressed and nutritionally regulated genes of heart were mainly related to signal transduction and transcriptional regulation. In contrast, those of white muscle were enriched in gene ontology (GO) terms related to proteolysis and protein ubiquitination. Microarray meta-analysis using the bioinformatic tool Fish and Chips (http://fishandchips.genouest.org/index.php) showed the close association of a representative cluster of white skeletal muscle with some of cardiac and red skeletal muscle, and many GO terms related to mitochondrial function appeared to be common links between them. A second round of cluster comparisons revealed that mitochondria-related GOs also linked differentially expressed genes of heart with those of liver from cortisol-treated gilthead sea bream. These results show that mitochondria are among the first responders to environmental and nutritional stress stimuli in gilthead sea bream, and functional phenotyping of this cellular organelle is highly promising to obtain reliable markers of growth performance and well-being in this fish species.

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Acknowledgments

This work was funded by the EU seventh Framework Programme by the AQUAEXCEL (Aquaculture Infrastructures for Excellence in European Fish Research, FP7/2007-2012; grant agreement no. 262336) project. Additional funding was obtained from the Generalitat Valenciana (research grant PROMETEO 2010/006) and the Spanish Government through AQUAGENOMICS project (Consolider-Ingenio-2010 Programme).

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Authors and Affiliations

  1. Nutrigenomics and Fish Growth Endocrinology Group, Instituto de Acuicultura Torre de la Sal (IATS–CSIC), Castellón, Spain

    Josep A. Calduch-Giner & Jaume Pérez-Sánchez

  2. INRA, UR1037 LPGP Fish Physiology and Genomics, Rennes, France

    Yann Echasseriau & Patrick Prunet

  3. Departament de Fisiologia i Immunologia, Facultat de Biologia, Universitat de Barcelona and Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Spain

    Diego Crespo & Josep V. Planas

  4. INSERM, UMR 1064, Nantes, France

    Daniel Baron

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  1. Josep A. Calduch-Giner
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  4. Daniel Baron
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  7. Jaume Pérez-Sánchez
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Correspondence to Jaume Pérez-Sánchez.

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Supplemental Table A1

Datasets included in the bioinformatic meta-analysis tool Fish and Chips. (DOCX 53 kb)

Supplemental Table A2

Genes differentially expressed by restricted ration size in white skeletal muscle. Genes sharing the enriched GO terms “protein ubiquitination”, “proteolysis”, or “ubiquitin-dependent protein catabolic process” are highlighted in bold. (DOCX 28 kb)

Supplemental Table A3

Genes differentially expressed by restricted ration size in red skeletal muscle. (DOCX 19 kb)

Supplemental Table A4

Genes differentially expressed by restricted ration size in cardiac muscle. Genes sharing the enriched GO terms “regulation of transcription”, “signal transduction”, or “signaling pathway” are highlighted in bold. (DOCX 46 kb)

Supplemental Table A5

Overlapping annotated genes between clusters in the first and second round of cluster comparison. (DOCX 38 kb)

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Calduch-Giner, J.A., Echasseriau, Y., Crespo, D. et al. Transcriptional Assessment by Microarray Analysis and Large-Scale Meta-analysis of the Metabolic Capacity of Cardiac and Skeletal Muscle Tissues to Cope With Reduced Nutrient Availability in Gilthead Sea Bream (Sparus aurata L.). Mar Biotechnol 16, 423–435 (2014). https://doi.org/10.1007/s10126-014-9562-3

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