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Transcriptome analysis of adipose tissue from pigs divergent in feed efficiency reveals alteration in gene networks related to adipose growth, lipid metabolism, extracellular matrix, and immune response

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Abstract

Adipose tissue is hypothesized to play a vital role in regulation of feed efficiency (FE; efficiency in converting energy and nutrients into tissue), of which improvement will simultaneously reduce environmental impact and feed cost per pig. The objective of the present study was to sequence the subcutaneous adipose tissue transcriptome in FE-divergent pigs (n = 16) and identify relevant biological processes underpinning observed differences in FE. We previously demonstrated that high-FE pigs were associated with lower fatness when compared to their counterparts. Here, ontology analysis of a total of 209 annotated genes that were differentially expressed at a p < 0.01 revealed establishment of a dense extracellular matrix and inhibition of capillary formation as one underlying mechanism to achieve suppressed adipogenesis. Moreover, mechanisms ensuring an efficient utilization of lipids in high-FE pigs might be orchestrated by upstream regulators including CEBPA and EGF. Consequently, high-FE adipose tissue could exhibit more efficient cholesterol disposal, whilst inhibition of inflammatory and immune response in high-FE pigs may be an indicator of an optimally functioning adipose tissue. Taken together, adipose tissue growth, extracellular matrix formation, lipid metabolism and inflammatory and immune response are key biological events underpinning the differences in FE. Further investigations focusing on elucidating these processes would assist the animal production industry in optimizing strategies related to nutrient utilization and product quality.

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Abbreviations

FE:

Feed efficiency

RFI:

Residual feed intake

LRFI:

Low RFI

HRFI:

High RFI

High-FE:

LRFI

Low-FE:

HRFI

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Funding

The ECO-FCE project was funded by the European Union Seventh Framework Programme (FP7 2007/2013) under grant agreement No. 311794.

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Authors and Affiliations

  1. Teagasc, Food Research Centre, Ashtown, Dublin 15, Ireland

    Justyna Horodyska & Ruth M. Hamill

  2. Leibniz Institute for Farm Animal Biology (FBN), Institute for Genome Biology, Dummerstorf, Germany

    Justyna Horodyska, Henry Reyer, Klaus Wimmers & Nares Trakooljul

  3. Faculty of Agricultural and Environmental Sciences, University Rostock, Rostock, Germany

    Klaus Wimmers

  4. Teagasc, Pig Development Department, AGRIC, Moorepark, Fermoy, Co. Cork, Ireland

    Peadar G. Lawlor

Authors
  1. Justyna Horodyska
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  2. Henry Reyer
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  3. Klaus Wimmers
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  4. Nares Trakooljul
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  5. Peadar G. Lawlor
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  6. Ruth M. Hamill
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Contributions

JH collected samples, extracted RNA, prepared libraries, validated RNA-seq via qPCR, carried out data analysis and wrote the manuscript; HR participated in statistical analysis and edited the manuscript; KW contributed to experimental design, established lab protocols and edited the manuscript; NT assisted in library preparation, performed RNA-seq and data analysis, and edited the manuscript; PGL provided and screened the animals on RFI, participated in data collection and analysis, and edited the manuscript; RMH conceived the experiment and contributed to experimental design, collected samples and edited the manuscript.

Corresponding author

Correspondence to Ruth M. Hamill.

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Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

Animal care, slaughter and tissue collection of the animals used in this study were performed in compliance with national regulations related to animal research and commercial slaughtering and were approved by the Teagasc Animal Ethics Committee.

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Communicated by S. Hohmann.

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Horodyska, J., Reyer, H., Wimmers, K. et al. Transcriptome analysis of adipose tissue from pigs divergent in feed efficiency reveals alteration in gene networks related to adipose growth, lipid metabolism, extracellular matrix, and immune response. Mol Genet Genomics 294, 395–408 (2019). https://doi.org/10.1007/s00438-018-1515-5

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