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Evolutionary history and epigenetic regulation of the three paralogous pax7 genes in rainbow trout

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Abstract

The extraordinary muscle growth potential of teleost fish, particular those of the Salmoninae clade, elicits questions about the regulation of the relatively highly conserved transcription factors of the myogenic program. The pseudotetraploid nature of the salmonid genome adds another layer of regulatory complexity that must be reconciled with epigenetic data to improve our understanding of the achievement of lifelong muscle growth in these fish. We identify three paralogous pax7 genes (pax7a1, pax7a2 and pax7b) in the rainbow trout genome. During in vitro myogenesis, pax7a1 transcripts remain stable, whereas pax7a2 and pax7b mRNAs increase in abundance, similarly to myogenin mRNAs but in contrast to the expression pattern of the mammalian ortholog. We also profile the distribution of repressive H3K27me3 and H3K9me3 and permissive H3K4me3 marks during in vitro myogenesis across these loci and find that pax7a2 expression is associated with decreased H3K27 trimethylation, whereas pax7b expression is correlated with decreased H3K9me3 and H3K27me3. These data link the unique differential expression of pax7 paralogs with epigenetic histone modifications in a vertebrate species displaying growth divergent from that of mammals and highlight an important divergence in the regulatory mechanisms of pax7 expression among vertebrates. The system described here provides a more comprehensive picture of the combinatorial control mechanisms orchestrating skeletal muscle growth in a salmonid, leading to a better understanding of myogenesis in this species and across Vertebrata more generally.

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Acknowledgments

The authors thank Ikram Belghit, Imad Aharchaou and Alexandre Herman for their assistance in the setting up of the initial rainbow trout primary myoblast cultures.

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Authors and Affiliations

  1. INRA, UR1067 Nutrition Métabolisme Aquaculture, F-64310, St-Pée-sur-Nivelle, France

    Iban Seiliez & Lucie Marandel

  2. Department of Biology, University of Alabama at Birmingham, Birmingham, Ala., USA

    Jacob Michael Froehlich & Peggy R. Biga

  3. INRA, UR1037 Laboratoire de Physiologie et Génomique des Poissons, 35000, Rennes, France

    Jean-Charles Gabillard

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  1. Iban Seiliez
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  2. Jacob Michael Froehlich
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  3. Lucie Marandel
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  4. Jean-Charles Gabillard
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  5. Peggy R. Biga
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Correspondence to Peggy R. Biga.

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Iban Seiliez and Jacob Michael Froehlich contributed equally to the preparation of the manuscript.

This work was funded by the University of Alabama at Birmingham Nutrition and Obesity Research Center award #P30DK056336 and a University of Alabama at Birmingham Office of the Provost Faculty Development Grant to P.R.B.

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Seiliez, I., Froehlich, J.M., Marandel, L. et al. Evolutionary history and epigenetic regulation of the three paralogous pax7 genes in rainbow trout. Cell Tissue Res 359, 715–727 (2015). https://doi.org/10.1007/s00441-014-2060-0

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