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Open Access Highly Accessed Research article

Genetic architecture of gene expression in ovine skeletal muscle

Lisette JA Kogelman12, Keren Byrne3, Tony Vuocolo3, Nathan S Watson-Haigh17, Haja N Kadarmideen14, James W Kijas3, Hutton V Oddy5, Graham E Gardner6, Cedric Gondro5 and Ross L Tellam3*

Author Affiliations

1 CSIRO Livestock Industries, ATSIP, PMB CSIRO Aitkenvale, Townsville QLD 4814, Australia

2 Wageningen University and Research Centre (WUR), Animal Breeding and Genetics, Wageningen, The Netherlands

3 CSIRO Livestock Industries, Queensland Bioscience Precinct, St. Lucia, Brisbane, QLD 4067, Australia

4 Division of Genetics and Bioinformatics, Faculty of Life Sciences, University of Copenhagen, 1870 Frederiksberg C, Denmark

5 School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia

6 School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA 6150, Australia

7 The Australian Wine Research Institute, P.O. Box 197, Glen Osmond, SA 5064, Australia

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BMC Genomics 2011, 12:607  doi:10.1186/1471-2164-12-607

Published: 15 December 2011

Abstract

Background

In livestock populations the genetic contribution to muscling is intensively monitored in the progeny of industry sires and used as a tool in selective breeding programs. The genes and pathways conferring this genetic merit are largely undefined. Genetic variation within a population has potential, amongst other mechanisms, to alter gene expression via cis- or trans-acting mechanisms in a manner that impacts the functional activities of specific pathways that contribute to muscling traits. By integrating sire-based genetic merit information for a muscling trait with progeny-based gene expression data we directly tested the hypothesis that there is genetic structure in the gene expression program in ovine skeletal muscle.

Results

The genetic performance of six sires for a well defined muscling trait, longissimus lumborum muscle depth, was measured using extensive progeny testing and expressed as an Estimated Breeding Value by comparison with contemporary sires. Microarray gene expression data were obtained for longissimus lumborum samples taken from forty progeny of the six sires (4-8 progeny/sire). Initial unsupervised hierarchical clustering analysis revealed strong genetic architecture to the gene expression data, which also discriminated the sire-based Estimated Breeding Value for the trait. An integrated systems biology approach was then used to identify the major functional pathways contributing to the genetics of enhanced muscling by using both Estimated Breeding Value weighted gene co-expression network analysis and a differential gene co-expression network analysis. The modules of genes revealed by these analyses were enriched for a number of functional terms summarised as muscle sarcomere organisation and development, protein catabolism (proteosome), RNA processing, mitochondrial function and transcriptional regulation.

Conclusions

This study has revealed strong genetic structure in the gene expression program within ovine longissimus lumborum muscle. The balance between muscle protein synthesis, at the levels of both transcription and translation control, and protein catabolism mediated by regulated proteolysis is likely to be the primary determinant of the genetic merit for the muscling trait in this sheep population. There is also evidence that high genetic merit for muscling is associated with a fibre type shift toward fast glycolytic fibres. This study provides insight into mechanisms, presumably subject to strong artificial selection, that underpin enhanced muscling in sheep populations.