Dataset Information

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

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.

SUBMITTER: Seiliez I

PROVIDER: S-EPMC4344431 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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

Seiliez Iban I Froehlich Jacob Michael JM Marandel Lucie L Gabillard Jean-Charles JC Biga Peggy R PR

Cell and tissue research 20141210 3

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, ...[more]

PMID: 25487404

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Project description:BACKGROUND: Spermatogenesis is a late developmental process that involves a coordinated expression program in germ cells and a permanent communication between the testicular somatic cells and the germ-line. Current knowledge regarding molecular factors driving male germ cell proliferation and differentiation in vertebrates is still limited and mainly based on existing data from rodents and human. Fish with a marked reproductive cycle and a germ cell development in synchronous cysts have proven to be choice models to study precise stages of the spermatogenetic development and the germ cell-somatic cell communication network. In this study we used 9K cDNA microarrays to investigate the expression profiles underlying testis maturation during the male reproductive cycle of the trout, Oncorhynchus mykiss. RESULTS: Using total testis samples at various developmental stages and isolated spermatogonia, spermatocytes and spermatids, 3379 differentially expressed trout cDNAs were identified and their gene activation or repression patterns throughout the reproductive cycle were reported. We also performed a tissue-profiling analysis and highlighted many genes for which expression signals were restricted to the testes or gonads from both sexes. The search for orthologous genes in genome-sequenced fish species and the use of their mammalian orthologs allowed us to provide accurate annotations for trout cDNAs. The analysis of the GeneOntology terms therefore validated and broadened our interpretation of expression clusters by highlighting enriched functions that are consistent with known sequential events during male gametogenesis. Furthermore, we compared expression profiles of trout and mouse orthologs and identified a complement of genes for which expression during spermatogenesis was maintained throughout evolution. CONCLUSION: A comprehensive study of gene expression and associated functions during testis maturation and germ cell differentiation in the rainbow trout is presented. The study identifies new pathways involved during spermatogonia self-renewal or rapid proliferation, meiosis and gamete differentiation, in fish and potentially in all vertebrates. It also provides the necessary basis to further investigate the hormonal and molecular networks that trigger puberty and annual testicular recrudescence in seasonally breeding species.

Project description:BackgroundIdentifying ecologically significant phenotypic traits and the genomic mechanisms that underly them are crucial steps in understanding traits associated with population divergence. We used genome-wide data to identify genomic regions associated with key traits that distinguish two ecomorphs of rainbow trout (Oncorhynchus mykiss)-insectivores and piscivores-that coexist for the non-breeding portion of the year in Kootenay Lake, southeastern British Columbia. "Gerrards" are large-bodied, rapidly growing piscivores with high metabolic rates that spawn north of Kootenay Lake in the Lardeau River, in contrast to the insectivorous populations that are on average smaller in body size, with lower growth and metabolic rates, mainly forage on aquatic insects, and spawn in tributaries immediately surrounding Kootenay Lake. We used pool-seq data representing ~ 60% of the genome and 80 fish per population to assess the level of genomic divergence between ecomorphs and to identify and interrogate loci that may play functional or selective roles in their divergence.ResultsGenomic divergence was high between sympatric insectivores and piscivores ([Formula: see text] = 0.188), and in fact higher than between insectivorous populations from Kootenay Lake and the Blackwater River ([Formula: see text] = 0.159) that are > 500 km apart. A window-based [Formula: see text] analysis did not reveal "islands" of genomic differentiation; however, the window with highest [Formula: see text] estimate did include a gene associated with insulin secretion. Although we explored the use of the "Local score" approach to identify genomic outlier regions, this method was ultimately not used because simulations revealed a high false discovery rate (~ 20%). Gene ontology (GO) analysis identified several growth processes as enriched in genes occurring in the ~ 200 most divergent genomic windows, indicating many loci of small effect involved in growth and growth-related metabolic processes are associated with the divergence of these ecomorphs.ConclusionOur results reveal a high degree of genomic differentiation between piscivorous and insectivorous populations and indicate that the large body piscivorous phenotype is likely not due to one or a few loci of large effect. Rather, the piscivore phenotype may be controlled by several loci of small effect, thus highlighting the power of whole-genome resequencing in identifying genomic regions underlying population-level phenotypic divergences.

Dataset Information

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

Publications

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

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