Abstract
BackgroundMicroRNAs (miRNAs) are small non-coding RNA molecules with an important role upon post-transcriptional regulation. These molecules have been shown essential for several cellular processes in vertebrates, including muscle biology. Many miRNAs were described as exclusively or highly expressed in skeletal and/or cardiac muscle. However, knowledge on the genomic organization and evolution of muscle miRNAs has been unveiled in a reduced number of vertebrates and mostly only reflects their organization in mammals, whereas fish genomes remain largely uncharted. The main goal of this study was to elucidate particular features in the genomic organization and the putative evolutionary history of muscle miRNAs through a genome-wide comparative analysis of cartilaginous and bony fish genomes.ResultsAs major outcomes we show that (1) miR-208 was unexpectedly absent in cartilaginous and ray-finned fish genomes whereas it still exist in other vertebrate groups; (2) miR-499 was intergenic in medaka and stickleback conversely to other vertebrates where this miRNA is intronic; (3) the zebrafish genome is the unique harboring two extra paralogous copies of miR-499 and their host gene (Myh7b); (4) a rare deletion event of the intergenic and bicistronic cluster miR-1-1/133a-2 took place only into Tetraodontiformes genomes (pufferfish and spotted green puffer); (5) the zebrafish genome experienced a duplication event of miR-206/-133b; and (6) miR-214 was specifically duplicated in species belonging to superorder Acanthopterygii.ConclusionsDespite of the aforementioned singularities in fish genomes, large syntenic blocks containing muscle-enriched miRNAs were found to persist, denoting colligated functionality between miRNAs and neighboring genes. Based on the genomic data here obtained, we envisioned a feasible scenario for explaining muscle miRNAs evolution in vertebrates.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-014-0196-x) contains supplementary material, which is available to authorized users.
Highlights
MicroRNAs are small non-coding RNA molecules with an important role upon post-transcriptional regulation
77.8 mature sequences, the degree of similarity among orthologous was even higher, ranging from ~95% to perfectly matched sequences (Table 2). Such findings suggest that muscle miRNAs examined have been under strong selective constraint throughout the evolution of vertebrates, thereby reflecting an acquirement of primordial functions on muscle biology
The high dynamism inherent to fish genomes helps to explain the variable pattern in the distribution of miRNA genes but fails to explain the high synteny observed so far
Summary
MicroRNAs (miRNAs) are small non-coding RNA molecules with an important role upon post-transcriptional regulation. The occurrence of deeply conserved and species-specific miRNAs in metazoan, argues in favor of a permanent, rapid and uneven evolutionary process of miRNA genes In this sense, a suite of miRNAs, including miR1, −133a, −133b, −206, −208a, −208b, −214 and −499, were identified as highly enriched or expressed in cardiac and/or skeletal muscle cells of animals (reviewed in [9]). MiRNA expression profiles and functions in muscle and other tissues depend on the miRNA genomic context, which correspond to miRNA location, conservation and organization in the genome [13,14] Peculiarities such as the physical distance between miRNA genes in chromosomes [15] or miRNA location in comparison to protein coding genes (i.e., intergenic, intronic, exonic, or mirtron) may provide important clues regarding coordinated regulation and function of miRNAs. current knowledge on the genomic context of muscle miRNAs has been unveiled in a reduced number of vertebrates, preventing more informative large scale comparisons. Available data mostly reflects features from mammal miRNAs, whereas fish, the largest class of living vertebrates, remain largely uncharted
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