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Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals
Andrew Grimson1,2, Mansi Srivastava4, Bryony Fahey3, Ben J. Woodcroft3, H. Rosaria Chiang1,2, Nicole King4, Bernard M. Degnan3, Daniel S. Rokhsar4,5 & David P. Bartel1,2
1 Whitehead Institute for Biomedical Research, 9 Cambridge Center, Cambridge, Massachusetts 02142, USA
2 Howard Hughes Medical Institute, Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA
3 School of Integrative Biology, University of Queensland, Brisbane 4072, Australia
4 Department of Molecular and Cell Biology and Center for Integrative Genomics, University of California at Berkeley, Berkeley, California 94720, USA
5 Department of Energy, Joint Genome Institute, Walnut Creek, California 94598, USA
In bilaterian animals, such as humans, flies and worms, hundreds of microRNAs (s), 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.