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MBE Advance Access published online on February 14, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn045
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Origin, Evolution and Biological Role of miRNA Cluster in DLK-DIO3 Genomic Region in Placental Mammals

Evgeny A. Glazov, Sean McWilliam, Wesley C. Barris and Brian P. Dalrymple*

CSIRO Livestock Industries, QBP, 306 Carmody Road, St Lucia, QLD 4067, Australia

* Corresponding author: Brian Dalrymple, CSIRO Livestock Industries, Brisbane QLD 4067 Australia, Phone: +61 7 3214-2503, Fax: +61 7 3214-2900, E-mail: brian.dalrymple{at}csiro.au

Received for publication October 25, 2007. Revision received January 9, 2008. Accepted for publication February 4, 2008.

microRNAs are a rapidly growing family of small regulatory RNAs modulating gene expression in plants and animals. In animals, most of the microRNAs discovered in early studies were found to be evolutionarily conserved across the whole kingdom. More recent studies, however, have identified many microRNAs that are specific to a particular group of organisms or even a single species. These present a question about evolution of the individual microRNAs and their role in establishing and maintaining lineage specific functions and characteristics.

In this study we describe a detailed analysis of the microRNA cluster (hereafter mir-379/mir-656 cluster) located within the imprinted DLK-DIO3 region on human chromosome 14. We show that orthologous microRNA clusters are present in all sequenced genomes of the placental (eutherian) mammals, but not in the marsupial (metatherian), monotreme (prototherian), or any other vertebrate genomes. We provide evidence that the locus encompassing this cluster emerged in an early eutherian ancestor prior to the radiation of modern placental mammals by tandem duplication of the ancient precursor sequence. The original amplified cluster may have contained in excess of 250 microRNA precursor sequences, most of which now appear to be inactive. Examination of the eutherian genomes showed that the cluster has been maintained in evolution for approximately 100 million years.

Analysis of genes that contain predicted evolutionarily conserved targets for microRNAs from this cluster revealed significant overrepresentation of the Gene Ontology (GO) terms associated with biological processes such as neurogenesis, embryonic development, transcriptional regulation, and RNA metabolism. Consistent with these findings a survey of the microRNA expression data within the cluster demonstrates a strong bias towards brain and placenta samples from adult organisms, and some embryonic tissues.

Our results suggest that emergence of the mir-379/mir-656 miRNA cluster was one of the factors that facilitated evolution of the placental mammals. Overrepresentation of genes involved in regulation of neurogenesis among predicted miRNAs targets indicate an important role of the mir-379/mir-656 cluster in this biological process in the placental mammals.

Key Words: microRNA • genome evolution • comparative genomics • mammalian genome • placental mammals


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