Small networks of expressed genes in the whole blood and relationships to profiles in circulating metabolites provide insights in inter-individual variability of feed efficiency in growing pigs

Abstract Background Feed efficiency is a research priority to support a sustainable meat production. It is recognized as a complex trait that integrates multiple biological pathways orchestrated in and by various tissues. This study aims to determine networks between biological entities to explain i...

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Main Authors: Camille Juigné, Emmanuelle Becker, Florence Gondret
Format: Article
Language:English
Published: BMC 2023-10-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-023-09751-1
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author Camille Juigné
Emmanuelle Becker
Florence Gondret
author_facet Camille Juigné
Emmanuelle Becker
Florence Gondret
author_sort Camille Juigné
collection DOAJ
description Abstract Background Feed efficiency is a research priority to support a sustainable meat production. It is recognized as a complex trait that integrates multiple biological pathways orchestrated in and by various tissues. This study aims to determine networks between biological entities to explain inter-individual variation of feed efficiency in growing pigs. Results The feed conversion ratio (FCR), a measure of feed efficiency, and its two component traits, average daily gain and average daily feed intake, were obtained from 47 growing pigs from a divergent selection for residual feed intake and fed high-starch or high-fat high-fiber diets during 58 days. Datasets of transcriptomics (60 k porcine microarray) in the whole blood and metabolomics (1H-NMR analysis and target gas chromatography) in plasma were available for all pigs at the end of the trial. A weighted gene co-expression network was built from the transcriptomics dataset, resulting in 33 modules of co-expressed molecular probes. The eigengenes of eight of these modules were significantly ( $$P \le 0.05$$ P ≤ 0.05 ) or tended to be ( $$0.05 < P \le 0.10$$ 0.05 < P ≤ 0.10 ) correlated to FCR. Great homogeneity in the enriched biological pathways was observed in these modules, suggesting co-expressed and co-regulated constitutive genes. They were mainly enriched in genes participating to immune and defense-related processes, and to a lesser extent, to translation, cell development or learning. They were also generally associated with growth rate and percentage of lean mass. In the whole network, only one module composed of genes participating to the response to substances, was significantly associated with daily feed intake and body adiposity. The plasma profiles in circulating metabolites and in fatty acids were summarized by weighted linear combinations using a dimensionality reduction method. Close association was thus found between a module composed of co-expressed genes participating to T cell receptor signaling and cell development process in the whole blood and related to FCR, and the circulating concentrations of polyunsaturated fatty acids in plasma. Conclusion These systemic approaches have highlighted networks of entities driving key biological processes involved in the phenotypic difference in feed efficiency between animals. Connecting transcriptomics and metabolic levels together had some additional benefits.
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spelling doaj.art-cd0ab8ed087843eb83706bbe4779c5e52023-10-29T12:15:34ZengBMCBMC Genomics1471-21642023-10-0124112010.1186/s12864-023-09751-1Small networks of expressed genes in the whole blood and relationships to profiles in circulating metabolites provide insights in inter-individual variability of feed efficiency in growing pigsCamille Juigné0Emmanuelle Becker1Florence Gondret2PEGASE, INRAE, Institut AgroUniversity Rennes, Inria, CNRS, IRISA - UMR 6074PEGASE, INRAE, Institut AgroAbstract Background Feed efficiency is a research priority to support a sustainable meat production. It is recognized as a complex trait that integrates multiple biological pathways orchestrated in and by various tissues. This study aims to determine networks between biological entities to explain inter-individual variation of feed efficiency in growing pigs. Results The feed conversion ratio (FCR), a measure of feed efficiency, and its two component traits, average daily gain and average daily feed intake, were obtained from 47 growing pigs from a divergent selection for residual feed intake and fed high-starch or high-fat high-fiber diets during 58 days. Datasets of transcriptomics (60 k porcine microarray) in the whole blood and metabolomics (1H-NMR analysis and target gas chromatography) in plasma were available for all pigs at the end of the trial. A weighted gene co-expression network was built from the transcriptomics dataset, resulting in 33 modules of co-expressed molecular probes. The eigengenes of eight of these modules were significantly ( $$P \le 0.05$$ P ≤ 0.05 ) or tended to be ( $$0.05 < P \le 0.10$$ 0.05 < P ≤ 0.10 ) correlated to FCR. Great homogeneity in the enriched biological pathways was observed in these modules, suggesting co-expressed and co-regulated constitutive genes. They were mainly enriched in genes participating to immune and defense-related processes, and to a lesser extent, to translation, cell development or learning. They were also generally associated with growth rate and percentage of lean mass. In the whole network, only one module composed of genes participating to the response to substances, was significantly associated with daily feed intake and body adiposity. The plasma profiles in circulating metabolites and in fatty acids were summarized by weighted linear combinations using a dimensionality reduction method. Close association was thus found between a module composed of co-expressed genes participating to T cell receptor signaling and cell development process in the whole blood and related to FCR, and the circulating concentrations of polyunsaturated fatty acids in plasma. Conclusion These systemic approaches have highlighted networks of entities driving key biological processes involved in the phenotypic difference in feed efficiency between animals. Connecting transcriptomics and metabolic levels together had some additional benefits.https://doi.org/10.1186/s12864-023-09751-1Feed efficiencyFatty acidsMetabolomicMolecular modules
spellingShingle Camille Juigné
Emmanuelle Becker
Florence Gondret
Small networks of expressed genes in the whole blood and relationships to profiles in circulating metabolites provide insights in inter-individual variability of feed efficiency in growing pigs
BMC Genomics
Feed efficiency
Fatty acids
Metabolomic
Molecular modules
title Small networks of expressed genes in the whole blood and relationships to profiles in circulating metabolites provide insights in inter-individual variability of feed efficiency in growing pigs
title_full Small networks of expressed genes in the whole blood and relationships to profiles in circulating metabolites provide insights in inter-individual variability of feed efficiency in growing pigs
title_fullStr Small networks of expressed genes in the whole blood and relationships to profiles in circulating metabolites provide insights in inter-individual variability of feed efficiency in growing pigs
title_full_unstemmed Small networks of expressed genes in the whole blood and relationships to profiles in circulating metabolites provide insights in inter-individual variability of feed efficiency in growing pigs
title_short Small networks of expressed genes in the whole blood and relationships to profiles in circulating metabolites provide insights in inter-individual variability of feed efficiency in growing pigs
title_sort small networks of expressed genes in the whole blood and relationships to profiles in circulating metabolites provide insights in inter individual variability of feed efficiency in growing pigs
topic Feed efficiency
Fatty acids
Metabolomic
Molecular modules
url https://doi.org/10.1186/s12864-023-09751-1
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