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The Deep Evolution of Metazoan Micrornas

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The Deep Evolution of Metazoan Micrornas EVOLUTION & DEVELOPMENT 11:1, 50–68 (2009) DOI: 10.1111/j.1525-142X.2008.00302.x The deep evolution of metazoan microRNAs Benjamin M. Wheeler,a Alysha M. Heimberg,b Vanessa N. Moy,b Erik A. Sperling,c Thomas W. Holstein,d Steffen Heber,e and Kevin J. Petersonb,Ã aDepartment of Computer Science, North Carolina State University, Raleigh, NC 27695, USA bDepartment of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA cDepartment of Geology and Geophysics, Yale University, P.O. Box 208109, New Haven, CT 06520, USA dMolekulare Evolution und Genomik, Heidelberger Institut fu¨r Zoologie, Neuenheimer Feld 230, 69120 Heidelberg, Germany eBioinformatics Research Center, North Carolina State University, Raleigh, NC 27695, USA Ã Author for correspondence (email: [email protected]) SUMMARY microRNAs (miRNAs) are approximately evolutionary trends elucidated from the model systems are 22-nucleotide noncoding RNA regulatory genes that are key generally true for all miRNA families and metazoan taxa explored: players in cellular differentiation and homeostasis. They might the continuous addition of miRNA families with only rare also play important roles in shaping metazoan macro- substitutions to the mature sequence, and only rare instances evolution. Previous studies have shown that miRNAs are of secondary loss. Despite this conservation, we document continuously being added to metazoan genomes through time, evolutionary stable shifts to the determination of position 1 of the and, once integrated into gene regulatory networks, show only mature sequence, a phenomenon we call seed shifting, as well rare mutations within the primary sequence of the mature gene as the ability to post-transcriptionally edit the 50 end of the mature product and are only rarely secondarily lost. However, because read, changing the identity of the seed sequence and possibly the the conclusions from these studies were largely based on repertoire of downstream targets. Finally, we describe a novel phylogenetic conservation of miRNAs between model systems type of miRNA in demosponges that, although shows a different like Drosophila and the taxon of interest, it was unclear if these pre-miRNA structure, still shows remarkable conservation of the trends would describe most miRNAs in most metazoan taxa. mature sequence in the two sponge species analyzed. We Here, we describe the shared complement of miRNAs among 18 propose that miRNAs might be excellent phylogenetic markers, animal species using a combination of 454 sequencing of small and suggest that the advent of morphological complexity might RNA libraries with genomic searches. We show that the have its roots in miRNA innovation. INTRODUCTION different evolutionary pattern. Initial surveys of miRNAs across the animal kingdom demonstrated a very compelling microRNAs (miRNAs) are a recently discovered group of feature of miRNA evolution when compared with the small RNA regulatory genes that have captured the attention evolution of the protein-coding repertoire: miRNA families of investigators interested in the control of cellular differen- are continuously being added to bilaterian lineages through tiation (Ambros 2004; Zhao and Srivastava 2007; Hobert evolutionary time such that vertebrates, for example, were 2008; Makeyev and Maniatis 2008; van Rooij et al. 2008; Yi characterized by the possession of miRNA families not found et al. 2008), its misregulation (Lu et al. 2005; Meltzer 2005; in arthropods, and vice versa (Hertel et al. 2006; Sempere Calin and Croce 2006; Esquela-Kerscher and Slack 2006; et al. 2006; Prochnik et al. 2007; Heimberg et al. 2008). Fur- He et al. 2007; Sevignani et al. 2007; Barbarotto et al. 2008; ther, these authors showed that miRNAs, once integrated Medina and Slack 2008; Yang et al. 2008), and its evolution into the genomic regulatory circuitry, are only rarely (Sempere et al. 2006; Heimberg et al. 2008; Pierce et al. 2008). secondarily lost, and the mature miRNA sequences are With the demonstration that morphologically complex ani- under intense negative selection. mals like vertebrates and fruit flies possess a protein-coding Because of these features, evolutionary biologists have genetic tool kit that is largely conserved across Metazoa attempted to reconstruct the phylogenetic history of the (Peterson and Sperling 2007; Putnam et al. 2007; Ryan et al. miRNAs found in vertebrates, insects, and nematodes, and 2007; Simionato et al. 2007; Yamada et al. 2007; Larroux noted the following. First, known miRNAs neither could be et al. 2008), investigators began to look at other components found nor could be detected in sponges (Sempere et al. 2006; of gene regulatory networks for molecules that might show a Prochnik et al. 2007). Second, bilaterians had a greatly 50 & 2009 The Author(s) Journal compilation & 2009 Wiley Periodicals, Inc. Wheeler et al. Deep evolution of metazoan microRNAs 51 expanded repertoire of miRNAs as compared with cnidarians Table 1. Taxonomic nomenclature (Sempere et al. 2006; Prochnik et al. 2007), and vertebrates had a greatly expanded set of miRNAs as compared with MetazoaFDemospongia1Eumetazoa F 1 bilaterian invertebrates (Hertel et al. 2006; Heimberg et al. Demospongia (Haplosclerida) Haliclona Amphimedon EumetazoaFCnidaria1Triploblastica 2008), and both of these advents correlated with increases to CnidariaFNematostella (Anthozoa)1Hydra (Hydrozoa) morphological complexity (Sempere et al. 2006; Lee et al. TriploblasticaFSymsagittifera (Acoela)1Nephrozoa 2007; Niwa and Slack 2007; Heimberg et al. 2008). Third, NephrozoaFProtostomia1Deuterostomia only a small subset of the bilaterian miRNAs were detected in ProtostomiaFEcdysozoa1Eutrochozoa acoel flatworms, consistent with both their relatively simple EcdysozoaFPriapulus (Priapulida)1Arthropoda morphology and their inferred phylogenetic position ArthropodaFIxodes (Chelicerata)1Pancrustacea F 1 (Sempere et al. 2006, 2007; Bagun˜ a` et al. 2008). Hence, Pancrustacea Daphnia (Crustacea) Drosophila (Insecta) EutrochozoaFCerebratulus (Nemertea)1Neotrochozoa miRNAs could be very useful tools to explore hypotheses NeotrochozoaFAnnelida1Mollusca centered around the molecular basis of morphological com- AnnelidaFNereis1Capitella plexity (Sempere et al. 2006; Lee et al. 2007; Niwa and Slack Mollusca (Gastropoda)FHaliotis1Lottia 2007; Heimberg et al. 2008), the phenomenon of develop- DeuterostomiaFAmbulacraria1Chordata mental canalization (Hornstein and Shomron 2006; Cui et al. AmbulacrariaFEchinodermata1Saccoglossus (Hemichordata) 2007; Peterson 2008), the control of the tempo of morpho- Echinodermata (Eleutherozoa)FStrongylocentrotus (Echino- 1 logical evolution (Peterson et al. 2007), and the interrelation- idea) Henricia (Asteroidea) ChordataFBranchiostoma (Cephalochordata)1Homo (Vertebrata) ships among metazoan taxa (Sempere et al. 2007; Sperling and Peterson in press). However, all of these evolutionary surveys necessarily relied on comparing the conserved miRNAs between the tax- unsampled for their miRNA complements, including demo- on of interest, whether annelid, agnathan, or acoel flatworm, sponges, cnidarians, annelids, gastropod molluscs, hemichor- with the known miRNA complement of mammals, arthro- dates, and echinoderms (see Table 1 for all taxonomic pods, and/or nematodes because the complements of only nomenclature used throughout this article). All of these clades these three model taxa had been explored independently of have unique miRNA families not found anywhere else in the phylogenetic conservation (Lagos-Quintana et al. 2001; Lau animal kingdom, including demosponges, which appear to et al. 2001; Lee and Ambros 2001). Thus, if a taxon increased possess a novel type of miRNA, a type that more closely its rate of mutation or secondarily lost many miRNAs, then resembles plant miRNAs than known animal miRNAs. We the phylogenetic history of that particular miRNA would be show that protostomes and deuterostomes have a greatly inaccurately reconstructed, leading to potentially spurious expanded number of miRNAs as compared with either acoel claims about the import of miRNAs with respect to metazoan flatworms or to cnidarians, and that the rate of acquisition of macroevolution. Although a few more recent studies have these novel miRNAs is not seen anywhere else in the animal explored the miRNA repertoire of additional taxa indepen- tree except at the base of the vertebrates (Heimberg et al. dent of phylogenetic conservation (Palakodeti et al. 2006; 2008). Importantly, all of the miRNAs, including the sponge Fu et al. 2008), an independent test of these claims through an miRNAs, show remarkable conservation of the mature gene examination of the evolutionary dynamics of miRNAs has yet sequence. When substitutions do occur, they occur at pre- to be explored in a taxon where both phylogenetic position dictable positions along the mature sequence, with the highest and time of origin were carefully controlled. frequency of changes localized to the 30 end of the mature Here, we explore the evolutionary dynamics of miRNAs gene product. In a few cases, the identification of nucleotide 1 across metazoan phylogeny and through deep evolutionary of the mature sequence of a specific miRNA in two or more time by combining 454 sequencing of miRNA libraries with taxa has been moved toward either 50 or 30, a phenomenon we genomic searches. By sequencing a library from a taxon that call ‘‘seed shifting’’ because the identity of positions 2–8, and is a sister lineage to a second taxon with a sequenced genome,
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