Abstract
Understanding how animal complexity has arisen and identifying the key genetic components of this process is a central goal of evolutionary developmental biology. The discovery of microRNAs (miRNAs) as key regulators of development has identified a new set of candidates for this role. microRNAs are small noncoding RNAs that regulate tissue-specific or temporal gene expression through base pairing with target mRNAs. The full extent of the evolutionary distribution of miRNAs is being revealed as more genomes are scrutinized. To explore the evolutionary origins of metazoan miRNAs, we searched the genomes of diverse animals occupying key phylogenetic positions for homologs of experimentally verified human, fly, and worm miRNAs. We identify 30 miRNAs conserved across bilaterians, almost double the previous estimate. We hypothesize that this larger than previously realized core set of miRNAs was already present in the ancestor of all Bilateria and likely had key roles in allowing the evolution of diverse specialist cell types, tissues, and complex morphology. In agreement with this hypothesis, we found only three, conserved miRNA families in the genome of the sea anemone Nematostella vectensis and no convincing family members in the genome of the demosponge Reniera sp. The dramatic expansion of the miRNA repertoire in bilaterians relative to sponges and cnidarians suggests that increased miRNA-mediated gene regulation accompanied the emergence of triploblastic organ-containing body plans.
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References
Aboobaker AA, Blaxter ML (2003) Hox gene loss during dynamic evolution of the nematode cluster. Curr Biol 13:37–40
Aboobaker AA, Tomancak P, Patel NH, Rubin GM, Lai E (2005) Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc Natl Acad Sci USA 102:18017–18022
Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T (2003) A uniform system for microRNA annotation. RNA (3):277–279
Bartel D, Chen C (2004) Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 5:396–400
Brennecke J, Stark A, Russell R, Cohen S (2005) Principles of microRNA-target recognition. PLoS Biol 3:e85
Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2003) MicroRNA targets in Drosophila. Genome Biol 5(1):R1
Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34:D140–D144
Hertel J, Lindemeyer M, Missal K, Fried C, Tanzer A, Flamm C, Hofacker IL, Stadler PF (2006) Students of bioinformatics computer labs 2004 and 2005. The expansion of the metazoan microRNA repertoire. BMC Genomics 7:25
Kortschak RD, Samuel G, Saint R, Miller DJ (2003) EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr Biol 13:2190–2195
Lai EC, Tomancak P, Williams RW, Rubin GM (2003) Computational identification of Drosophila microRNA genes. Genome Biol 4:R42
Pasquinelli AE, McCoy A, Jimenez E, Salo E, Ruvkun G, Martindale MQ, Baguna J (2003) Expression of the 22 nucleotide let-7 heterochronic RNA throughout the Metazoa: a role in life history evolution? Evol Dev 5:372–378
Sempere LF, Cole CN, McPeek MA, Peterson KJ (2006) The phylogenetic distribution of metazoan microRNAs: insights into evolutionary complexity and constraint. J Exp Zoolog B Mol Dev Evol. DOI 10.1002/jez.b
Technau U, Rudd S, Maxwell P, Gordon PM, Saina M, Grasso LC, Hayward DC, Sensen CW, Saint R, Holstein TW, Ball EE, Miller DJ (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21:633–639
Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM (2006) Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev 20:2202–2207
Wienholds E, Plasterk RH (2005) MicroRNA function in animal development. FEBS Lett 579 (26):5911–5922
Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, de Bruijn E, Horvitz HR, Kauppinen S, Plasterk RH (2005) MicroRNA expression in zebrafish embryonic development. Science 309:310–311
Woltering JM, Durston AJ (2006) The zebrafish hoxDb has been reduced to a single miRNA. Nat Genet 38:601–602
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
Acknowledgements
SEP is funded by the US DOE Joint Genome Institute; DSR by the Center for Integrative Genomics; and AAA by a Wellcome Trust International Research Fellowship. We are grateful to the Baylor College of Medicine Genome Sequencing Center for the prepublication use of the Tribolium castaneum and Strongylocentrotus purpuratus genome data, and the DoE Joint Genome Institute for the prepublication use of the Nematostella vectensis and Reniera sp. genome data. We are grateful to Scott Nichols for comments on the manuscript. Simon E. Prochnik and A. Aziz Aboobaker contributed equally to this work.
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Communicated by N. Satoh
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Table S1
Predicted miRNAs and clusters in metazoans. Predicted miRNAs are grouped in families that contain the same seed site (bases 1–7 or 2–8). miRNAs that lie <8 kb from each other on a genomic scaffold are boxed in the same color with the cluster number shown. Possible, but more distant clusters have a “?” in the cluster column and a note. Explanation of notes column: extend length of additional genomic sequence added to 5′ and 3′ ends of predicted miRNA hairpin before refolding and new ΔG folding energy (kcal/mol); ext predicted mature miRNA sequences were extended at the 5′ and 3′ ends to the same length as the query; poor terminal struct indicates the presence of an internal loop or bulge and a 1- to 2-bp stem before the main terminal loop; nonparsimonious miRNAs that have been predicted but appear to be nonparsimonious as they only have restricted homology to otherwise vertebrate specific miRNAs and are thus likely false positives and are not shown in Fig. 1 (XLS 72 kb).
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Prochnik, S.E., Rokhsar, D.S. & Aboobaker, A.A. Evidence for a microRNA expansion in the bilaterian ancestor. Dev Genes Evol 217, 73–77 (2007). https://doi.org/10.1007/s00427-006-0116-1
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DOI: https://doi.org/10.1007/s00427-006-0116-1