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Ancient animal microRNAs and the evolution of tissue identity

Nature volume 463, pages 1084–1088 (2010)Cite this article

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Abstract

The spectacular escalation in complexity in early bilaterian evolution correlates with a strong increase in the number of microRNAs1,2. To explore the link between the birth of ancient microRNAs and body plan evolution, we set out to determine the ancient sites of activity of conserved bilaterian microRNA families in a comparative approach. We reason that any specific localization shared between protostomes and deuterostomes (the two major superphyla of bilaterian animals) should probably reflect an ancient specificity of that microRNA in their last common ancestor. Here, we investigate the expression of conserved bilaterian microRNAs in Platynereis dumerilii, a protostome retaining ancestral bilaterian features3,4, in Capitella, another marine annelid, in the sea urchin Strongylocentrotus, a deuterostome, and in sea anemone Nematostella, representing an outgroup to the bilaterians. Our comparative data indicate that the oldest known animal microRNA, miR-100, and the related miR-125 and let-7 were initially active in neurosecretory cells located around the mouth. Other sets of ancient microRNAs were first present in locomotor ciliated cells, specific brain centres, or, more broadly, one of four major organ systems: central nervous system, sensory tissue, musculature and gut. These findings reveal that microRNA evolution and the establishment of tissue identities were closely coupled in bilaterian evolution. Also, they outline a minimum set of cell types and tissues that existed in the protostome–deuterostome ancestor.

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Figure 1: Foregut-related expression of conserved microRNAs.
Figure 2: MicroRNAs expressed in locomotor ciliated cells.
Figure 3: Expression of brain-specific microRNAs.
Figure 4: MicroRNAs demarcating organ systems.

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Data deposits

Sequences for Platynereis miRNA primary transcripts pri-miR-100/let-7, pri-miR-12/216 and pri-miR-183/263 were deposited in the GenBank database with accession numbers FJ838789.1, FJ838790.1 and GU224283, respectively.

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Acknowledgements

We thank A. Fischer for drawing schematic illustrations and providing probes for tropomyosin 1, A. Boutla for advice when initiating the project, J. Brennecke for help with small RNA cloning and discussions, M. Hentze for critical reading of the manuscript, P. Steinmetz and U. Technau for Nematostella embryos and discussions, E. Arboleda and I. Arnone for sea urchin plutei and discussions. V. Benes and the EMBL-Genecore facility for expert technical advice, W. R. McCombie, M. Rooks and E. Hodges for help with sequencing and M. Arumugam, V. Van Noort, J. Muller and C. Creevey for advice in target analysis.

Author Contributions F.C. initiated the project, cloned Platynereis small RNAs, characterized the temporal and spatial expression of ancient miRNAs and their targets, coordinated the collaborations and wrote the paper. F.R. analysed and evaluated the Solexa sequencing data. R.T. assembled the 3′UTRs of targets from Platynereis ESTs and provided riboprobes. O.S. did the SNP and miRNA::target co-expression analysis. K.T. performed target predictions under the supervision of P.B., and S.K characterized foxa2 expression. H.S. generated probes for targets in situ screen. G.J.H. hosted the small RNA cloning and sequencing. D.A. analysed comparative miRNA expression, provided ideas and strategies and wrote the paper. All authors discussed the results and commented on the manuscript.

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Author notes

  1. Florian Raible & Sebastian Klaus

    Present address: Present addresses: Max F. Perutz Laboratories, Campus Vienna Biocenter, Dr. Bohr-Gasse 9/4, A-1030 Vienna, Austria (F.R.); J. W. Goethe - Universität Frankfurt Biologie-Campus, Siesmayerstrasse 70-72, D-60323 Frankfurt, Germany (S.K.).,

Authors and Affiliations

  1. Developmental Biology Unit,,

    Foteini Christodoulou, Florian Raible, Raju Tomer, Oleg Simakov, Sebastian Klaus, Heidi Snyman & Detlev Arendt

  2. Computational Biology Unit, European Molecular Biology Laboratory, D-69117 Heidelberg, Germany ,

    Florian Raible, Kalliopi Trachana & Peer Bork

  3. Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA ,

    Gregory J. Hannon

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  1. Foteini Christodoulou
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Correspondence to Detlev Arendt.

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Christodoulou, F., Raible, F., Tomer, R. et al. Ancient animal microRNAs and the evolution of tissue identity. Nature 463, 1084–1088 (2010). https://doi.org/10.1038/nature08744

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