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Maternal and paternal genomes differentially affect myofibre characteristics and muscle weights of bovine fetuses at midgestation

By R. Xiang, M. Ghani Poor Samami, W. Johns, T. Eindorf, D. Rutley, Z. Kruk, C. Fitzsimmons, D. Thomsen, C. Roberts, B. Burns, G. Anderson, P. Greenwood and S. Hiendleder

Abstract

Postnatal myofibre characteristics and muscle mass are largely determined during fetal development and may be significantly affected by epigenetic parent-of-origin effects. However, data on such effects in prenatal muscle development that could help understand unexplained variation in postnatal muscle traits are lacking. In a bovine model we studied effects of distinct maternal and paternal genomes, fetal sex, and non-genetic maternal effects on fetal myofibre characteristics and muscle mass. Data from 73 fetuses (Day153, 54% term) of four genetic groups with purebred and reciprocal cross Angus and Brahman genetics were analyzed using general linear models. Parental genomes explained the greatest proportion of variation in myofibre size of Musculus semitendinosus (80–96%) and in absolute and relative weights of M. supraspinatus, M. longissimus dorsi, M. quadriceps femoris and M. semimembranosus (82–89% and 56–93%, respectively). Paternal genome in interaction with maternal genome (P<0.05) explained most genetic variation in cross sectional area (CSA) of fast myotubes (68%), while maternal genome alone explained most genetic variation in CSA of fast myofibres (93%, P<0.01). Furthermore, maternal genome independently (M. semimembranosus, 88%, P<0.0001) or in combination (M. supraspinatus, 82%; M. longissimus dorsi, 93%; M. quadriceps femoris, 86%) with nested maternal weight effect (5–6%, P<0.05), was the predominant source of variation for absolute muscle weights. Effects of paternal genome on muscle mass decreased from thoracic to pelvic limb and accounted for all (M. supraspinatus, 97%, P<0.0001) or most (M. longissimus dorsi, 69%, P<0.0001; M. quadriceps femoris, 54%, P<0.001) genetic variation in relative weights. An interaction between maternal and paternal genomes (P<0.01) and effects of maternal weight (P<0.05) on expression of H19, a master regulator of an imprinted gene network, and negative correlations between H19 expression and fetal muscle mass (P<0.001), suggested imprinted genes and miRNA interference as mechanisms for differential effects of maternal and paternal genomes on fetal muscle.Ruidong Xiang, Mani Ghanipoor-Samami, William H. Johns, Tanja Eindorf, David L. Rutley, Zbigniew A. Kruk, Carolyn J. Fitzsimmons, Dana A. Thomsen, Claire T. Roberts, Brian M. Burns, Gail I. Anderson, Paul L. Greenwood, Stefan Hiendlede

Topics: Muscle, Skeletal; Fetus; Animals; Cattle; Body Weight; Organ Size; Gene Expression Regulation, Developmental; Genome; Models, Genetic; Female; Male; Genetic Variation; Muscle Fibers, Skeletal; RNA, Long Untranslated
Publisher: Public Library of Science
Year: 2013
DOI identifier: 10.1371/journal.pone.0053402
OAI identifier: oai:digital.library.adelaide.edu.au:2440/78967
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