title: The evolution of microRNA pathway protein components in Cnidaria.
abstract: In the last decade, it became evident that posttranscriptional regulation of gene expression by microRNAs is a central biological process in both plants and animals. Yet, our knowledge about microRNA biogenesis and utilization in animals stems mostly from the study of Bilateria. In this study, we identified genes encoding the protein components of different parts of the microRNA pathway in Cnidaria, the likely sister phylum of Bilateria. These genes originated from three cnidarian lineages (sea anemones, stony corals, and hydras) that are separated by at least 500 My from one another. We studied the expression and phylogeny of the cnidarian homologs of Drosha and Pasha (DGCR8) that compose the microprocessor, the RNAse III enzyme Dicer and its partners, the HEN1 methyltransferase, the Argonaute protein effectors, as well as members of the GW182 protein family. We further reveal that whereas the bilaterian dicer partners Loquacious/TRBP and PACT are absent from Cnidaria, this phylum contains homologs of the double-stranded RNA-binding protein HYL1, the Dicer partner found in plants. We also identified HYL1 homologs in a sponge and a ctenophore. This finding raises questions regarding the independent evolution of the microRNA pathway in plants and animals, and together with the other results shed new light on the evolution of an important regulatory pathway.
authors.affiliation: Department for Molecular Evolution and Development, Center for Organismal Systems Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.
authors.forename: Yehu
authors.initials: Y
authors.lastname: Moran
authors.forename: Daniela
authors.initials: D
authors.lastname: Praher
authors.forename: David
authors.initials: D
authors.lastname: Fredman
authors.forename: Ulrich
authors.initials: U
authors.lastname: Technau
mesh_terms: D020816:Amino Acid Motifs / Q000235:genetics; D000595:Amino Acid Sequence; D000818:Animals; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D060565:Argonaute Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D003063:Cnidaria / Q000145:classification / Q000235:genetics*; D019143:Evolution, Molecular; D005786:Gene Expression Regulation; D006801:Humans; D008780:Methyltransferases / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D035683:MicroRNAs / Q000235:genetics*; D008969:Molecular Sequence Data; D010802:Phylogeny; D011506:Proteins / Q000737:chemistry* / Q000235:genetics / Q000378:metabolism*; D043244:Ribonuclease III / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D016415:Sequence Alignment; D015398:Signal Transduction
chemical_list: D060565:Argonaute Proteins; D035683:MicroRNAs; D011506:Proteins; D008780:Methyltransferases; D043244:Ribonuclease III
keywords: Cnidaria; Nematostella; microRNA; posttranscriptional regulation
references.citation: Proc Natl Acad Sci U S A. 2012 Jan 24;109(4):1104-9
references.pmid: 22232654
references.citation: Cell Mol Life Sci. 2006 Nov;63(22):2560-70
references.pmid: 16952052
references.citation: Cell. 2004 Apr 2;117(1):69-81
references.pmid: 15066283
references.citation: Nature. 2010 Mar 25;464(7288):592-6
references.pmid: 20228792
references.citation: EMBO J. 2010 Nov 3;29(21):3688-700
references.pmid: 20859253
references.citation: J Mol Biol. 2008 Jun 27;380(1):237-43
references.pmid: 18508075
references.citation: Proc Biol Sci. 2009 Dec 22;276(1677):4261-70
references.pmid: 19759036
references.citation: RNA. 2009 Aug;15(8):1433-42
references.pmid: 19535464
references.citation: Nature. 2008 Oct 30;455(7217):1193-7
references.pmid: 18830242
references.citation: Trends Cell Biol. 2000 Jun;10(6):220-4
references.pmid: 10802537
references.citation: Science. 2007 Jul 6;317(5834):86-94
references.pmid: 17615350
references.citation: BMC Genomics. 2013 Mar 25;14:204
references.pmid: 23530871
references.citation: Mol Biol Evol. 2011 Aug;28(8):2289-303
references.pmid: 21325094
references.citation: Nat Struct Mol Biol. 2012 Aug;19(8):760-6
references.pmid: 22796965
references.citation: Nucleic Acids Res. 2013 Jan 7;41(1):599-616
references.pmid: 23166307
references.citation: Nat Rev Mol Cell Biol. 2009 Feb;10(2):126-39
references.pmid: 19165215
references.citation: Cell. 2012 Nov 21;151(5):1055-67
references.pmid: 23178124
references.citation: Wiley Interdiscip Rev RNA. 2013 Jul-Aug;4(4):423-35
references.pmid: 23681777
references.citation: Cell. 2009 Feb 20;136(4):669-87
references.pmid: 19239888
references.citation: Nature. 2011 Jul 24;476(7360):320-3
references.pmid: 21785439
references.citation: Cell. 2012 Jul 6;150(1):100-10
references.pmid: 22682761
references.citation: Science. 2011 Nov 25;334(6059):1091-7
references.pmid: 22116879
references.citation: BMC Genomics. 2012 Dec 20;13:714
references.pmid: 23256903
references.citation: Bioinformatics. 2004 Dec 12;20(18):3702-4
references.pmid: 15284097
references.citation: J Exp Zool B Mol Dev Evol. 2013 Mar;320(2):84-93
references.pmid: 23349041
references.citation: Nat Rev Genet. 2008 Nov;9(11):831-42
references.pmid: 18852696
references.citation: Nature. 2010 Feb 25;463(7284):1084-8
references.pmid: 20118916
references.citation: Plant Signal Behav. 2012 Oct 1;7(10):1224-9
references.pmid: 22902697
references.citation: Nucleic Acids Res. 2011 Jan;39(Database issue):D225-9
references.pmid: 21109532
references.citation: Nature. 2011 Jul 13;475(7355):201-5
references.pmid: 21753850
references.citation: Trends Genet. 2008 Sep;24(9):431-8
references.pmid: 18676050
references.citation: Nat Struct Mol Biol. 2012 Jun 05;19(6):586-93
references.pmid: 22664986
references.citation: Trends Genet. 2011 Jan;27(1):7-13
references.pmid: 21047698
references.citation: Nucleic Acids Res. 2012 Jan;40(Database issue):D136-43
references.pmid: 22139910
references.citation: Development. 2011 Apr;138(8):1447-58
references.pmid: 21389047
references.citation: Nature. 2010 Jun 3;465(7298):584-9
references.pmid: 20424607
references.citation: Genes Dev. 2010 Sep 1;24(17):1951-60
references.pmid: 20713509
references.citation: PLoS Biol. 2011 Mar;9(3):e1000602
references.pmid: 21423652
references.citation: Mol Ecol. 2012 May;21(10):2440-54
references.pmid: 22490231
references.citation: Bioinformatics. 2005 May 1;21(9):2104-5
references.pmid: 15647292
references.citation: Nat Struct Mol Biol. 2011 Sep 18;18(10):1153-8
references.pmid: 21926993
references.citation: Science. 2010 Jun 25;328(5986):1694-8
references.pmid: 20448148
references.citation: Nature. 2009 Oct 8;461(7265):823-7
references.pmid: 19812675
references.citation: Evol Dev. 2005 May-Jun;7(3):201-15
references.pmid: 15876193
references.citation: Nature. 2012 Jun 20;486(7403):368-74
references.pmid: 22722195
references.citation: Mar Biotechnol (NY). 2013 Jun;15(3):329-39
references.pmid: 23151943
references.citation: PLoS One. 2011;6(7):e22725
references.pmid: 21829492
references.citation: Nucleic Acids Res. 2012 Jul;40(12):5651-65
references.pmid: 22402495
references.citation: Cell. 2012 Oct 26;151(3):533-46
references.pmid: 23063653
references.citation: Bioinformatics. 2006 Jan 15;22(2):195-201
references.pmid: 16301204
references.citation: Genome Biol. 2008 Jan 17;9(1):R10
references.pmid: 18201385
references.citation: Cell. 2009 Jan 23;136(2):215-33
references.pmid: 19167326
references.citation: Nat Rev Genet. 2011 Feb;12(2):99-110
references.pmid: 21245828
references.citation: Nat Struct Mol Biol. 2005 Apr;12(4):340-9
references.pmid: 15800637
references.citation: Mol Biol Evol. 2013 Mar;30(3):627-41
references.pmid: 23180579
references.citation: BMC Bioinformatics. 2004 Aug 19;5:113
references.pmid: 15318951
references.citation: Genome Biol. 2011;12(4):221
references.pmid: 21554756
references.citation: Bioinformatics. 2009 Aug 1;25(15):1972-3
references.pmid: 19505945
references.citation: Nucleic Acids Res. 2012 Jan;40(Database issue):D290-301
references.pmid: 22127870
references.citation: Cell Res. 2012 Apr;22(4):624-36
references.pmid: 22410795
references.citation: Bioessays. 2012 Oct;34(10):857-66
references.pmid: 22847169
references.citation: Mol Biol Evol. 2009 Jun;26(6):1333-40
references.pmid: 19276153
references.citation: Cell. 2009 Jul 23;138(2):340-51
references.pmid: 19632183
references.citation: J Biol Chem. 2000 Nov 24;275(47):36957-65
references.pmid: 10948199
references.citation: Nat Rev Immunol. 2010 Sep;10(9):632-44
references.pmid: 20706278
references.citation: Evol Dev. 2009 Jan-Feb;11(1):50-68
references.pmid: 19196333
references.citation: Curr Biol. 2004 Feb 17;14(4):346-51
references.pmid: 14972688
references.citation: Cold Spring Harb Protoc. 2009 Sep;2009(9):pdb.prot5282
references.pmid: 20147267
references.citation: Cell Rep. 2013 Jun 27;3(6):1901-9
references.pmid: 23746446
references.citation: Syst Biol. 2010 May;59(3):307-21
references.pmid: 20525638
references.citation: Cell. 2009 Jul 23;138(2):328-39
references.pmid: 19632182
references.citation: Proc Natl Acad Sci U S A. 2004 Jan 27;101(4):1093-8
references.pmid: 14722360
references.citation: RNA. 2009 May;15(5):781-93
references.pmid: 19304925
references.citation: Nat Rev Genet. 2011 Jan;12(1):19-31
references.pmid: 21116305