Dicers are proteins of the ribonuclease III family with the ability to process dsRNA, involved in regulation of gene expression at the post-transcriptional level. Dicers are conserved from basal metazoans to higher metazoans and contain a number of functional domains that interact with dsRNA. The completed genome sequences of over 34 invertebrate species allowed us to systematically investigate Dicer genes over a diverse range of phyla. The majority of invertebrate Dicers clearly fell into the Dicer1 or Dicer2 subfamilies. Most nematodes possessed only one Dicer gene, a member of the Dicer1 subfamily, whereas two Dicer genes (Dicer1 and Dicer2) were present in all platyhelminths surveyed. Analysis of the key domains showed that a 5′ pocket was conserved across members of the Dicer1 subfamily, with the exception of the nematode Bursaphelenchus xylophilus. Interestingly, Nematostella vectensis DicerB grouped into Dicer2 subfamily harbored a 5′ pocket, which is commonly present in Dicer1. Similarly, the 3′ pocket was also found to be conserved in all Dicer proteins with the exceptions of Schmidtea mediterranea Dicer2 and Trichoplax adherens Dicer A. The loss of catalytic residues in the RNase III domain was noted in platyhelminths and cnidarians, and the ‘ball’ and ‘socket’ junction between two RNase III domains in platyhelminth Dicers was different from the canonical junction, suggesting the possibility of different conformations. The present data suggest that Dicers might have duplicated and diversified independently, and have evolved for various functions in invertebrates.
References
[1]
Lamontagne B, Larose S, Boulanger J, Elela SA (2001) The RNase III family: a conserved structure and expanding functions in eukaryotic dsRNA metabolism. Curr Issues Mol Biol 3: 71–78.
[2]
He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522–531. doi: 10.1038/nrg1379
[3]
Hammond SM, Boettcher S, Caudy AA, Kobayashi R, Hannon GJ (2001) Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293: 1146–1150. doi: 10.1126/science.1064023
[4]
Wang Y, Juranek S, Li H, Sheng G, Wardle GS, et al. (2009) Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461: 754–761. doi: 10.1038/nature08434
[5]
Cerutti H, Casas-Mollano JA (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 50: 81–99. doi: 10.1007/s00294-006-0078-x
[6]
Shabalina SA, Koonin EV (2008) Origins and evolution of eukaryotic RNA interference. Trends Ecol Evol 23: 578–587. doi: 10.1016/j.tree.2008.06.005
[7]
Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363–366. doi: 10.1038/35053110
[8]
Margis R, Fusaro AF, Smith NA, Curtin SJ, Watson JM, et al. (2006) The evolution and diversification of Dicers in plants. FEBS Lett 580: 2442–2450. doi: 10.1016/j.febslet.2006.03.072
[9]
Blaszczyk J, Tropea JE, Bubunenko M, Routzahn KM, Waugh DS, et al. (2001) Crystallographic and modeling studies of RNase III suggest a mechanism for double-stranded RNA cleavage. Structure 9: 1225–1236. doi: 10.1016/s0969-2126(01)00685-2
[10]
Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W (2004) Single processing center models for human Dicer and bacterial RNase III. Cell 118: 57–68. doi: 10.1016/j.cell.2004.06.017
[11]
MacRae IJ, Zhou K, Doudna JA (2007) Structural determinants of RNA recognition and cleavage by Dicer. Nat Struct Mol Biol 14: 934–940. doi: 10.1038/nsmb1293
[12]
Park JE, Heo I, Tian Y, Simanshu DK, Chang H, et al. (2011) Dicer recognizes the 5' end of RNA for efficient and accurate processing. Nature 475: 201–205. doi: 10.1038/nature10198
[13]
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290–301. doi: 10.1093/nar/gkr1065
[14]
Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40: D302–305. doi: 10.1093/nar/gkr931
[15]
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797. doi: 10.1093/nar/gkh340
[16]
Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189–1191. doi: 10.1093/bioinformatics/btp033
[17]
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540–552. doi: 10.1093/oxfordjournals.molbev.a026334
[18]
Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164–1165. doi: 10.1093/bioinformatics/btr088
[19]
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.
[20]
Kurimoto K, Muto Y, Obayashi N, Terada T, Shirouzu M, et al. (2005) Crystal structure of the N-terminal RecA-like domain of a DEAD-box RNA helicase, the Dugesia japonica vasa-like gene B protein. J Struct Biol 150: 58–68. doi: 10.1016/j.jsb.2005.01.006
[21]
Ji X (2006) Structural basis for non-catalytic and catalytic activities of ribonuclease III. Acta Crystallogr D Biol Crystallogr 62: 933–940. doi: 10.1107/s090744490601153x
[22]
Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, et al. (2008) Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455: 1193–1197. doi: 10.1038/nature07415
[23]
de Jong D, Eitel M, Jakob W, Osigus HJ, Hadrys H, et al. (2009) Multiple dicer genes in the early-diverging metazoa. Molecular Biology and Evolution 26: 1333–1340. doi: 10.1093/molbev/msp042
[24]
Krishna S, Nair A, Cheedipudi S, Poduval D, Dhawan J, et al. (2013) Deep sequencing reveals unique small RNA repertoire that is regulated during head regeneration in Hydra magnipapillata. Nucleic Acids Research 41: 599–616. doi: 10.1093/nar/gks1020
[25]
Moran Y, Praher D, Fredman D, Technau U (2013) The Evolution of MicroRNA Pathway Protein Components in Cnidaria. Molecular Biology and Evolution 30: 2541–2552. doi: 10.1093/molbev/mst159
[26]
Han J, Lee Y, Yeom KH, Nam JW, Heo I, et al. (2006) Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125: 887–901. doi: 10.1016/j.cell.2006.03.043
[27]
Ji XH (2008) The mechanism of RNase III action: How Dicer dices. Rna Interference 320: 99–116. doi: 10.1007/978-3-540-75157-1_5
