MicroRNAs and essential components of the microRNA processing machinery are not encoded in the genome of the ctenophore Mnemiopsis leidyi

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Maxwell, Evan K ^a,b   Ryan, Joseph F ^a,c   Schnitzler, Christine E ^a   Browne, William E ^d   Baxevanis, Andreas D ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b BOSTON UNIVERSITY   (United States)

^c UNIVERSITY OF BERGEN   (Norway)

^d Department of Biology   (United States)

Author keywords

Ctenophore; Drosha; Metazoa; Microprocessor complex; MicroRNA; MiRNA; Mnemiopsis leidyi; Pasha; Ribonuclease III; RNase III

Indexed keywords

DROSHA PROTEIN; MICRORNA; NUCLEAR PROTEIN; PASHA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; CTENOPHORA; EMBRYO; GENE CONTROL; GENE MAPPING; GENOME; MNEMIOPSIS LEIDYI; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; RNA PROCESSING; RNA SEQUENCE;

ANIMALS; BASE SEQUENCE; CTENOPHORA; EVOLUTION, MOLECULAR; GENETIC LOCI; GENOMICS; MICRORNAS; RNA PROCESSING, POST-TRANSCRIPTIONAL;

ANIMALIA; CTENOPHORA (COELENTERATES); METAZOA; MNEMIOPSIS; MNEMIOPSIS LEIDYI; PLACOZOA; TRICHOPLAX;

EID: 84871202631     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-714     Document Type: Article

References (54)

1. Ruby JG, Jan CH, Bartel DP. Intronic microRNA precursors that bypass Drosha processing. Nature 2007, 448:83-86. 10.1038/nature05983, 2475599, 17589500.
2. Berezikov E, Chung W-J, Willis J, Cuppen E, Lai EC. Mammalian mirtron genes. Mol Cell 2007, 28:328-336. 10.1016/j.molcel.2007.09.028, 2763384, 17964270.
3. Axtell MJ, Westholm JO, Lai EC. Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 2011, 12:221. 10.1186/gb-2011-12-4-221, 3218855, 21554756.
4. Schickel R, Boyerinas B, Park S-M, Peter ME. MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 2008, 27:5959-5974. 10.1038/onc.2008.274, 18836476.
5. Liu N, Okamura K, Tyler DM, Phillips MD, Chung W-J, Lai EC. The evolution and functional diversification of animal microRNA genes. Cell Res 2008, 18:985-996. 10.1038/cr.2008.278, 2712117, 18711447.
6. Berezikov E. Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 2011, 12:846-860. 10.1038/nrg3079, 22094948.
7. Shabalina SA, Koonin EV. Origins and evolution of eukaryotic RNA interference. Trends Ecol Evol 2008, 23:578-587. 10.1016/j.tree.2008.06.005, 2695246, 18715673.
8. Kosik KS. MicroRNAs tell an evo-devo story. Nat Rev Neurosci 2009, 10:754-759. 10.1038/nrn2713, 19738624.
9. Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP. Early origins and evolution of microRNAs and piwi-interacting RNAs in animals. Nature 2008, 455:1193-1197. 10.1038/nature07415, 18830242.
10. Cerutti H, Casas-Mollano JA. On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 2006, 50:81-99. 10.1007/s00294-006-0078-x, 2583075, 16691418.
11. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Bio 2009, 10:126-139.
12. Peterson KJ, Dietrich MR, McPeek MA. MicroRNAs and metazoan macroevolution: insights into canalization, complexity, and the Cambrian explosion. BioEssays 2009, 31:736-747. 10.1002/bies.200900033, 19472371.
13. Wheeler BM, Heimberg AM, Moy VN, Sperling EA, Holstein TW, Heber S, Peterson KJ. The deep evolution of metazoan microRNAs. EvoDevo 2009, 11:50-68.
14. Niwa R, Slack FJ. The evolution of animal microRNA function. Curr Opin Genet Dev 2007, 17:145-150. 10.1016/j.gde.2007.02.004, 17317150.
15. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297. 10.1016/S0092-8674(04)00045-5, 14744438.
16. Jones-Rhoades MW, Bartel DP, Bartel B. MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 2006, 57:19-53. 10.1146/annurev.arplant.57.032905.105218, 16669754.
17. Hinas A, Reimegard J, Wagner EGH, Nellen W, Ambros VR, Soderbom F. The small RNA repertoire of Dictyostelium discoideum and its regulation by components of the RNAi pathway. Nucleic Acids Res 2007, 35:6714-6726. 10.1093/nar/gkm707, 2175303, 17916577.
18. Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury J-M, Badger JH, et al. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 2010, 465:617-621. 10.1038/nature09016, 20520714.
19. Huang A, He L, Wang G. Identification and characterization of microRNAs from Phaeodactylum tricornutum by high-throughput sequencing and bioinformatics analysis. BMC Genomics 2011, 12:337. 10.1186/1471-2164-12-337, 3141676, 21718527.
20. Lin W-C, Li S-C, Lin W-C, Shin J-W, Hu S-N, Yu X-M, Huang T-Y, Chen S-C, Chen H-C, Chen S-J, et al. Identification of microRNA in the protist Trichomonas vaginalis. Genomics 2009, 93:487-493. 10.1016/j.ygeno.2009.01.004, 19442639.
21. Chen XS, Collins LJ, Biggs PJ, Penny D. High throughput genome-wide survey of small RNAs from the parasitic protists Giardia intestinalis and Trichomonas vaginalis. Genome Biol Evol 2009, 1:165-175. 2817412, 20333187.
22. Huang P-J, Lin W-C, Chen S-C, Lin Y-H, Sun C-H, Lyu P-C, Tang P. Identification of putative miRNAs from the deep-branching unicellular flagellates. Genomics 2012, 99:101-107. 10.1016/j.ygeno.2011.11.002, 22120185.
23. Lin W-C, Huang K-Y, Chen S-C, Huang T-Y, Chen S-J, Huang P-J, Tang P. Malate dehydrogenase is negatively regulated by miR-1 in Trichomonas vaginalis. Parasitol Res 2009, 105:1683-1689. 10.1007/s00436-009-1616-5, 19777264.
24. Li W, Saraiya AA, Wang CC. Gene regulation in Giardia lamblia involves a putative microRNA derived from a small nucleolar RNA. PLoS Negl Trop Dis 2011, 5:e1338. 10.1371/journal.pntd.0001338, 3196473, 22028939.
25. Saraiya AA, Li W, Wang CC. A microRNA derived from an apparent canonical biogenesis pathway regulates variant surface protein gene expression in Giardia lamblia. RNA 2011, 17:2152-2164. 10.1261/rna.028118.111, 3222128, 22033329.
26. Saraiya AA, Wang CC. SnoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 2008, 4:e1000224. 10.1371/journal.ppat.1000224, 2583053, 19043559.
27. Braun L, Cannella D, Ortet P, Barakat M, Sautel CF, Kieffer S, Garin J, Bastien O, Voinnet O, Hakimi MA. A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii. PLoS Pathog 2010, 6:e1000920. 10.1371/journal.ppat.1000920, 2877743, 20523899.
28. Molnár A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC. MiRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 2007, 447:1126-1129. 10.1038/nature05903, 17538623.
29. Zhao T, Li G, Mi S, Li S, Hannon GJ, Wang XJ, Qi Y. A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 2007, 21:1190-1203. 10.1101/gad.1543507, 1865491, 17470535.
30. Tarver JE, Donoghue PCJ, Peterson KJ. Do miRNAs have a deep evolutionary history?. BioEssays 2012, 34:857-866. 10.1002/bies.201200055, 22847169.
31. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, et al. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749. 10.1038/nature06614, 18322464.
32. Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, et al. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Biol Sci 2009, 276:4261-4270. 10.1098/rspb.2009.0896, 2817096, 19759036.
33. Ryan JF, Pang K, Comparative Sequencing Program N, Mullikin JC, Martindale MQ, Baxevanis AD. The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. EvoDevo 2010, 1:9. 10.1186/2041-9139-1-9, 2959044, 20920347.
34. Reitzel AM, Pang K, Ryan JF, Mullikin JC, Martindale MQ, Baxevanis AD, Tarrant AM. Nuclear receptors from the ctenophore Mnemiopsis leidyi lack a zinc-finger DNA-binding domain: lineage-specific loss or ancestral condition in the emergence of the nuclear receptor superfamily?. EvoDevo 2011, 2:3. 10.1186/2041-9139-2-3, 3038971, 21291545.
35. Pang K, Ryan JF, Baxevanis AD, Martindale MQ. Evolution of the TGF-β signaling pathway and its potential role in the ctenophore, Mnemiopsis leidyi. PLoS ONE 2011, 6:e24152. 10.1371/journal.pone.0024152, 3169577, 21931657.
36. Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alie A, Morgenstern B, Manuel M, et al. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 2010, 27:1983-1987. 10.1093/molbev/msq089, 2922619, 20378579.
37. Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, et al. The dynamic genome of Hydra. Nature 2010, 464:592-596. 10.1038/nature08830, 20228792.
38. Hertel J, de Jong D, Marz M, Rose D, Tafer H, Tanzer A, Schierwater B, Stadler PF. Non-coding RNA annotation of the genome of Trichoplax adhaerens. Nucleic Acids Res 2009, 37:1602-1615. 10.1093/nar/gkn1084, 2655684, 19151082.
39. MacRae IJ, Doudna JA. Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Cur Opin Struct Biol 2007, 17:138-145.
40. Mochizuki K. A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev 2005, 19:77-89. 10.1101/gad.1265105, 540227, 15598983.
41. MacRae IJ, Zhou K, Doudna JA. Structural determinants of RNA recognition and cleavage by Dicer. Nat Struct Mol Biol 2007, 14:934-940. 10.1038/nsmb1293, 17873886.
42. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011, 39:W29-W37. 10.1093/nar/gkr367, 3125773, 21593126.
43. de Jong D, Eitel M, Jakob W, Osigus H-J, Hadrys H, Desalle R, Schierwater B. Multiple Dicer genes in the early-diverging metazoa. Mol Biol Evol 2009, 26:1333-1340. 10.1093/molbev/msp042, 19276153.
44. Zhang L, Hou D, Chen X, Li D, Zhu L, Zhang Y, Li J, Bian Z, Liang X, Cai X, et al. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res 2011, 1-20.
45. Flynt AS, Greimann JC, Chung W-J, Lima CD, Lai EC. MicroRNA biogenesis via splicing and exosome-mediated trimming in Drosophila. Molecular Cell 2010, 38:900-907. 10.1016/j.molcel.2010.06.014, 2904328, 20620959.
46. Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, Poustka AJ, Wallberg A, Peterson KJ, Telford MJ. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 2011, 470:255-258. 10.1038/nature09676, 21307940.
47. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
48. Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 2012, 40:37-52. 10.1093/nar/gkr688, 3245920, 21911355.
49. Hackenberg M, Sturm M, Langenberger D, Falcon-Perez JM, Aransay AM. miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments. Nucleic Acids Res 2009, 37:W68-W76. 10.1093/nar/gkp347, 2703919, 19433510.
50. Markham NR, Zuker M. UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 2008, 453:3-31. 10.1007/978-1-60327-429-6_1, 18712296.
51. Chung WJ, Agius P, Westholm JO, Chen M, Okamura K, Robine N, Leslie CS, Lai EC. Computational and experimental identification of mirtrons in Drosophila melanogaster and Caenorhabditis elegans. Genome Res 2011, 21:286-300. 10.1101/gr.113050.110, 3032932, 21177960.
52. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105. 10.1093/bioinformatics/bti263, 15647292.
53. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 2008, 57:758-771. 10.1080/10635150802429642, 18853362.
54. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574. 10.1093/bioinformatics/btg180, 12912839.