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Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals

Abstract

In bilaterian animals, such as humans, flies and worms, hundreds of microRNAs (miRNAs), some conserved throughout bilaterian evolution, collectively regulate a substantial fraction of the transcriptome. In addition to miRNAs, other bilaterian small RNAs, known as Piwi-interacting RNAs (piRNAs), protect the genome from transposons. Here we identify small RNAs from animal phyla that diverged before the emergence of the Bilateria. The cnidarian Nematostella vectensis (starlet sea anemone), a close relative to the Bilateria, possesses an extensive repertoire of miRNA genes, two classes of piRNAs and a complement of proteins specific to small-RNA biology comparable to that of humans. The poriferan Amphimedon queenslandica (sponge), one of the simplest animals and a distant relative of the Bilateria, also possesses miRNAs, both classes of piRNAs and a full complement of the small-RNA machinery. Animal miRNA evolution seems to have been relatively dynamic, with precursor sizes and mature miRNA sequences differing greatly between poriferans, cnidarians and bilaterians. Nonetheless, miRNAs and piRNAs have been available as classes of riboregulators to shape gene expression throughout the evolution and radiation of animal phyla.

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Figure 1: Phylogenetic distribution of annotated miRNAs.
Figure 2: The miRNAs of N. vectensis.
Figure 3: The miRNAs of Amphimedon queenslandica.
Figure 4: The piRNAs of basal metazoans.

Accession codes

Primary accessions

Gene Expression Omnibus

Data deposits

RNA sequencing data were deposited in the Gene Expression Omnibus (http://www.ncbi.nlm.nih.gov/geo/) under accession number GSE12578.

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Acknowledgements

We thank M. Abedin and E. Begovic for preparing the Monosiga and Trichoplax samples, respectively, W. Johnston for technical assistance, and J. Grenier, C. Mayr, C. Jan and N. Lau for discussions. This work was supported by an NIH postdoctoral fellowship (A.G.), and by grants from the NIH (D.P.B.), Richard Melmon (M.S., N.K. and D.S.R.), the Center for Integrative Genomics (M.S. and D.S.R.), the Gordon and Betty Moore Foundation (N.K.) and the Australian Research Council (B.F., B.J.W. and B.M.D.). D.P.B. is an investigator of the Howard Hughes Medical Institute.

Author Contributions A.G. constructed the libraries using procedures developed by H.R.C., and analysed the sequencing reads and protein homology. M.S., B.F., B.J.W., N.K., B.M.D. and D.S.R. provided samples for RNA extraction. A.G. and D.P.B. designed the study and prepared the manuscript, with input from other authors.

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Correspondence to David P. Bartel.

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Grimson, A., Srivastava, M., Fahey, B. et al. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455, 1193–1197 (2008). https://doi.org/10.1038/nature07415

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