Maternal undernutrition during periconceptional period affects whole-genome ovine muscle methylation in adult offspring
- PMID: 35580043
- PMCID: PMC9387600
- DOI: 10.1093/jas/skac180
Maternal undernutrition during periconceptional period affects whole-genome ovine muscle methylation in adult offspring
Abstract
Experimental and epidemiological studies suggest that maternal nutritional status during early pregnancy, including the period around the time of conception, may induce long-lasting epigenetic changes in the offspring. However, this remains largely unexplored in livestock. Therefore, the objective of this study was to evaluate if modification of the maternal diet of sheep (CTR: control; UND: 50% undernutrition) during the periconceptional period (42 d in total: -14/+28 from mating), would impact CpG methylation in muscle tissue (Longissimus dorsi) of adult offspring (11.5 mo old). Reduced representation bisulfite sequencing identified 262 (Edge-R, FDR < 0.05) and 686 (logistic regression, FDR < 0.001) differentially methylated regions (DMRs) between the UND and CTR groups. Gene ontology analysis identified genes related to development, functions of the muscular system, and steroid hormone receptor activity within the DMRs. The data reported here show that nutritional stress during early pregnancy leads to epigenetic modifications in the muscle of the resulting offspring, with possible implications for cardiac dysfunction, muscle physiology, and meat production.
Keywords: diet; epigenetics; methylation; muscle; undernutrition.
Plain language summary
The formation of the epigenetic pattern of an organism is highly sensitive to environmental factors, especially during early mammalian development, when epigenetic reprogramming of the whole genome takes place. In utero adverse conditions experienced during early pregnancy, such as maternal undernutrition, may induce long-lasting epigenetic changes in the resulting offspring. This study investigated the CpG methylation variations in muscle tissue of adult offspring induced by differences in the diet of their mothers during pregnancy. Our data show that undernutrition during pregnancy leads to epigenetic alterations in the muscle of the offspring, with a potential impact on animal health and productivity.
© The Author(s) 2022. Published by Oxford University Press on behalf of the American Society of Animal Science. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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References
-
- Bindea, G., Mlecnik B., Hackl H., Charoentong P., Tosolini M., Kirilovsky A., Fridman W. H., Pagès F., Trajanoski Z., and Galon J... 2009. ClueGO, a cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 25:1091–1093. doi:10.1093/bioinformatics/btp101 - DOI - PMC - PubMed
-
- Boyer, J. G., Prasad V., Song T., Lee D., Fu X., Grimes K. M., Sargent M. A., Sadayappan S., and Molkentin J. D... 2019. ERK1/2 signaling induces skeletal muscle slow fiber-type switching and reduces muscular dystrophy disease severity. JCI Insight. 5:e127356. doi:10.1172/jci.insight.127356 - DOI - PMC - PubMed