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RNA-seq of muscle from pigs divergent in feed efficiency and product quality identifies differences in immune response, growth, and macronutrient and connective tissue metabolism

BACKGROUND: Feed efficiency (FE) is an indicator of efficiency in converting energy and nutrients from feed into a tissue that is of major environmental and economic significance. The molecular mechanisms contributing to differences in FE are not fully elucidated, therefore the objective of this stu...

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Autores principales: Horodyska, Justyna, Wimmers, Klaus, Reyer, Henry, Trakooljul, Nares, Mullen, Anne Maria, Lawlor, Peadar G., Hamill, Ruth M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6211475/
https://www.ncbi.nlm.nih.gov/pubmed/30384851
http://dx.doi.org/10.1186/s12864-018-5175-y
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author Horodyska, Justyna
Wimmers, Klaus
Reyer, Henry
Trakooljul, Nares
Mullen, Anne Maria
Lawlor, Peadar G.
Hamill, Ruth M.
author_facet Horodyska, Justyna
Wimmers, Klaus
Reyer, Henry
Trakooljul, Nares
Mullen, Anne Maria
Lawlor, Peadar G.
Hamill, Ruth M.
author_sort Horodyska, Justyna
collection PubMed
description BACKGROUND: Feed efficiency (FE) is an indicator of efficiency in converting energy and nutrients from feed into a tissue that is of major environmental and economic significance. The molecular mechanisms contributing to differences in FE are not fully elucidated, therefore the objective of this study was to profile the porcine Longissimus thoracis et lumborum (LTL) muscle transcriptome, examine the product quality from pigs divergent in FE and investigate the functional networks underpinning the potential relationship between product quality and FE. RESULTS: RNA-Seq (n = 16) and product quality (n = 40) analysis were carried out in the LTL of pigs differing in FE status. A total of 272 annotated genes were differentially expressed with a P < 0.01. Functional annotation revealed a number of biological events related to immune response, growth, carbohydrate & lipid metabolism and connective tissue indicating that these might be the key mechanisms governing differences in FE. Five most significant bio-functions altered in FE groups were ‘haematological system development & function’, ‘lymphoid tissue structure & development’, ‘tissue morphology’, ‘cellular movement’ and ‘immune cell trafficking’. Top significant canonical pathways represented among the differentially expressed genes included ‘IL-8 signalling’, ‘leukocyte extravasation signalling, ‘sphingosine-1-phosphate signalling’, ‘PKCθ signalling in T lymphocytes’ and ‘fMLP signalling in neutrophils’. A minor impairment in the quality of meat, in relation to texture and water-holding capacity, produced by high-FE pigs was observed. High-FE pigs also had reduced intramuscular fat content and improved nutritional profile in terms of fatty acid composition. CONCLUSIONS: Ontology analysis revealed enhanced activity of adaptive immunity and phagocytes in high-FE pigs suggesting more efficient conserving of resources, which can be utilised for other important biological processes. Shifts in carbohydrate conversion into glucose in FE-divergent muscle may underpin the divergent evolution of pH profile in meat from the FE-groups. Moreover, altered amino acid metabolism and increased mobilisation & flux of calcium may influence growth in FE-divergent muscle. Furthermore, decreased degradation of fibroblasts in FE-divergent muscle could impact on collagen turnover and alter tenderness of meat, whilst enhanced lipid degradation in high-FE pigs may potentially underlie a more efficient fat metabolism in these animals. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5175-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-62114752018-11-08 RNA-seq of muscle from pigs divergent in feed efficiency and product quality identifies differences in immune response, growth, and macronutrient and connective tissue metabolism Horodyska, Justyna Wimmers, Klaus Reyer, Henry Trakooljul, Nares Mullen, Anne Maria Lawlor, Peadar G. Hamill, Ruth M. BMC Genomics Research Article BACKGROUND: Feed efficiency (FE) is an indicator of efficiency in converting energy and nutrients from feed into a tissue that is of major environmental and economic significance. The molecular mechanisms contributing to differences in FE are not fully elucidated, therefore the objective of this study was to profile the porcine Longissimus thoracis et lumborum (LTL) muscle transcriptome, examine the product quality from pigs divergent in FE and investigate the functional networks underpinning the potential relationship between product quality and FE. RESULTS: RNA-Seq (n = 16) and product quality (n = 40) analysis were carried out in the LTL of pigs differing in FE status. A total of 272 annotated genes were differentially expressed with a P < 0.01. Functional annotation revealed a number of biological events related to immune response, growth, carbohydrate & lipid metabolism and connective tissue indicating that these might be the key mechanisms governing differences in FE. Five most significant bio-functions altered in FE groups were ‘haematological system development & function’, ‘lymphoid tissue structure & development’, ‘tissue morphology’, ‘cellular movement’ and ‘immune cell trafficking’. Top significant canonical pathways represented among the differentially expressed genes included ‘IL-8 signalling’, ‘leukocyte extravasation signalling, ‘sphingosine-1-phosphate signalling’, ‘PKCθ signalling in T lymphocytes’ and ‘fMLP signalling in neutrophils’. A minor impairment in the quality of meat, in relation to texture and water-holding capacity, produced by high-FE pigs was observed. High-FE pigs also had reduced intramuscular fat content and improved nutritional profile in terms of fatty acid composition. CONCLUSIONS: Ontology analysis revealed enhanced activity of adaptive immunity and phagocytes in high-FE pigs suggesting more efficient conserving of resources, which can be utilised for other important biological processes. Shifts in carbohydrate conversion into glucose in FE-divergent muscle may underpin the divergent evolution of pH profile in meat from the FE-groups. Moreover, altered amino acid metabolism and increased mobilisation & flux of calcium may influence growth in FE-divergent muscle. Furthermore, decreased degradation of fibroblasts in FE-divergent muscle could impact on collagen turnover and alter tenderness of meat, whilst enhanced lipid degradation in high-FE pigs may potentially underlie a more efficient fat metabolism in these animals. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5175-y) contains supplementary material, which is available to authorized users. BioMed Central 2018-11-01 /pmc/articles/PMC6211475/ /pubmed/30384851 http://dx.doi.org/10.1186/s12864-018-5175-y Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Horodyska, Justyna
Wimmers, Klaus
Reyer, Henry
Trakooljul, Nares
Mullen, Anne Maria
Lawlor, Peadar G.
Hamill, Ruth M.
RNA-seq of muscle from pigs divergent in feed efficiency and product quality identifies differences in immune response, growth, and macronutrient and connective tissue metabolism
title RNA-seq of muscle from pigs divergent in feed efficiency and product quality identifies differences in immune response, growth, and macronutrient and connective tissue metabolism
title_full RNA-seq of muscle from pigs divergent in feed efficiency and product quality identifies differences in immune response, growth, and macronutrient and connective tissue metabolism
title_fullStr RNA-seq of muscle from pigs divergent in feed efficiency and product quality identifies differences in immune response, growth, and macronutrient and connective tissue metabolism
title_full_unstemmed RNA-seq of muscle from pigs divergent in feed efficiency and product quality identifies differences in immune response, growth, and macronutrient and connective tissue metabolism
title_short RNA-seq of muscle from pigs divergent in feed efficiency and product quality identifies differences in immune response, growth, and macronutrient and connective tissue metabolism
title_sort rna-seq of muscle from pigs divergent in feed efficiency and product quality identifies differences in immune response, growth, and macronutrient and connective tissue metabolism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6211475/
https://www.ncbi.nlm.nih.gov/pubmed/30384851
http://dx.doi.org/10.1186/s12864-018-5175-y
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