The Landscape of A-to-I RNA Editome Is Shaped by Both Positive and Purifying Selection

PLoS Genetics

Volumn 12, Issue 7, 2016, Pages

  Yu, Yao ^a   Zhou, Hongxia ^a   Kong, Yimeng ^a   Pan, Bohu ^a   Chen, Longxian ^a   Wang, Hongbing ^b   Hao, Pei ^c,d   Li, Xuan ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c INSTITUTE PASTEUR OF SHANGHAI   (China)

^d SHANGHAI CENTER FOR BIOINFORMATION TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DIPLOIDY; DROSOPHILA; HETEROZYGOSITY; HUMAN; LANDSCAPE; MATING SYSTEM; MULTIGENE FAMILY; NERVOUS SYSTEM FUNCTION; PHYLOGENY; PLASTICITY; PURIFYING SELECTION; RNA EDITING; SPECIES; ANIMAL; CONSERVED SEQUENCE; EXON; GENETIC SELECTION; GENETICS; MOLECULAR EVOLUTION;

ADENOSINE; INOSINE; TRANSCRIPTOME;

ADENOSINE; ANIMALS; CONSERVED SEQUENCE; DROSOPHILA; EVOLUTION, MOLECULAR; EXONS; INOSINE; PHYLOGENY; RNA EDITING; SELECTION, GENETIC; TRANSCRIPTOME;

EID: 84982816198     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006191     Document Type: Article

References (83)

1. Benne R, Van Den Burg J, Brakenhoff JPJ, Sloof P, Van Boom JH, Tromp MC, Major transcript of the frameshifted coxll gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell. 1986;46(6): 819–26. 3019552
2. Seeburg PH, Higuchi M, Sprengel R, RNA editing of brain glutamate receptor channels: mechanism and physiology. Brain Res Brain Res Rev. 1998;26(2–3): 217–29. 9651532
3. Palladino MJ, Keegan LP, O'Connell MA, Reenan RA, dADAR, a Drosophila double-stranded RNA-specific adenosine deaminase is highly developmentally regulated and is itself a target for RNA editing. RNA. 2000;6(7): 1004–18. 10917596
4. Bass BL, RNA Editing by Adenosine Deaminases That Act on RNA. Annu Rev Biochem. 2002;71:817–46. 12045112
5. Rueter SM, Dawson TR, Emeson RB, Regulation of alternative splicing by RNA editing. Nature. 1999;399(6731):75–80. 10331393
6. Lev-Maor G, Sorek R, Levanon EY, Paz N, Eisenberg E, Ast G, RNA-editing-mediated exon evolution. Genome Biol. 2007;8(2): R29–R. 17326827
7. Kawahara Y, Zinshteyn B, Sethupathy P, Iizasa H, Hatzigeorgiou AG, Nishikura K, Redirection of Silencing Targets by Adenosine-to-Inosine Editing of miRNAs. Science (New York, NY). 2007;315(5815): 1137–40.
8. Kawahara Y, Megraw M, Kreider E, Iizasa H, Valente L, Hatzigeorgiou AG, et al. Frequency and fate of microRNA editing in human brain. Nucleic Acids Res. 2008;36(16): 5270–80. doi: 10.1093/nar/gkn47918684997
9. Barraud P, Allain FHT, ADAR Proteins: Double-stranded RNA and Z-DNA Binding Domains. Curr Top Microbiol Immunol. 2012;353: 35–60. doi: 10.1007/82_2011_14521728134
10. Rodriguez J, Menet JS, Rosbash M, Nasent-seq indicates widespread cotranscriptional RNA editing in Drosophila. Mol Cell. 2012;47(1): 27–37. doi: 10.1016/j.molcel.2012.05.00222658416
11. Polson AG, Bass BL, Preferential selection of adenosines for modification by double-stranded RNA adenosine deaminase. The EMBO Journal. 1994;13(23): 5701–11. 7527340
12. Lehmann KA, Bass BL, Double-Stranded RNA Adenosine Deaminases ADAR1 and ADAR2 Have Overlapping Specificities. Biochemistry. 2000; 39(42): 12875–84. 11041852
13. Bass BL, RNA editing and hypermutation by adenosine deamination. Trends Biochem Sci. 1997;22(5): 157–62. 9175473
14. Ensterö M, Daniel C, Wahlstedt H, Major F, Öhman M, Recognition and coupling of A-to-I edited sites are determined by the tertiary structure of the RNA. Nucleic Acids Res. 2009;37(20): 6916–26. doi: 10.1093/nar/gkp73119740768
15. Higuchi M, Maas S, Single FN, Hartner J, Rozov A, Burnashev N, et al. Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature. 2000;406(6791): 78–81. 10894545
16. Hartner JC, Schmittwolf C, Kispert A, Muller AM, Higuchi M, Seeburg PH, Liver Disintegration in the Mouse Embryo Caused by Deficiency in the RNA-editing Enzyme ADAR1. J Biol Chem. 2003;279(6): 4894–902. 14615479
17. Palladino MJ, Keegan LP, O'Connell MA, Reenan RA, A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell. 2000Aug18;102(4): 437–49. 10966106
18. Wang Q, Khillan J, Gadue P, Nishikura K, Requirement of the RNA Editing Deaminase ADAR1 Gene for Embryonic Erythropoiesis. Science. 2000;290(5497): 1765–8. 11099415
19. Bahn JH, Lee JH, Li G, Greer C, Peng G, Xiao X, Accurate identification of A-to-I RNA editing in human by transcriptome sequencing. Genome Res. 2011;22(1): 142–50. doi: 10.1101/gr.124107.11121960545
20. Danecek P, Nellåker C, McIntyre RE, Buendia-Buendia JE, Bumpstead S, Ponting CP, et al. High levels of RNA-editing site conservation amongst 15 laboratory mouse strains. Genome Biol. 2012;13(4): r26–r26.
21. St Laurent G, Tackett MR, Nechkin S, Shtokalo D, Antonets D, Savva YA, et al. Genome-wide analysis of A-to-I RNA editing by single-molecule sequencing in Drosophila. Nat Struct Mol Biol. 2013;20(11): 1333–9. doi: 10.1038/nsmb.267524077224
22. Chen J-Y, Peng Z, Zhang R, Yang X-Z, Tan BC-M, Fang H, et al. RNA Editome in Rhesus Macaque Shaped by Purifying Selection. PLoS Genet. 2014;10(4): e1004274. doi: 10.1371/journal.pgen.100427424722121
23. Higuchi M, Single FN, Köhler M, Sommer B, Sprengel R, Seeburg PH, RNA editing of AMPA receptor subunit GluR-B: A base-paired intron-exon structure determines position and efficiency. Cell. 1993;75(7): 1361–70. 8269514
24. Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H, Sanders-Bush E, et al. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature. 1997;387(6630): 303–8. 9153397
25. Garrett S, Rosenthal JJC, RNA Editing Underlies Temperature Adaptation in K(+) Channels from Polar Octopuses. Science (New York, NY). 2012;335(6070): 848–51.
26. Mannion Niamh M, Greenwood SM, Young R, Cox S, Brindle J, Read D, et al. The RNA-Editing Enzyme ADAR1 Controls Innate Immune Responses to RNA. Cell reports. 2014;9(4): 1482–94. doi: 10.1016/j.celrep.2014.10.04125456137
27. Xu G, Zhang J, Human coding RNA editing is generally nonadaptive. Proc Natl Acad Sci U S A. 2014;111(10): 3769–74. doi: 10.1073/pnas.132174511124567376
28. Gommans WM, Mullen SP, Maas S, RNA editing: a driving force for adaptive evolution?BioEssays: news and reviews in molecular, cellular and developmental biology. 2009;31(10): 1137–45.
29. Xu G, Zhang J, In Search of Beneficial Coding RNA Editing. Mol Biol Evol. 2015;32(2): 536–41. doi: 10.1093/molbev/msu31425392343
30. Celniker SE, Dillon LAL, Gerstein MB, Gunsalus KC, Henikoff S, Karpen GH, et al. Unlocking the secrets of the genome. Nature. 2009;459(7249): 927–30. doi: 10.1038/459927a19536255
31. Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, Canese K, et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2011;39(Database issue): D38–D51. doi: 10.1093/nar/gkq117221097890
32. Edgar R, Domrachev M, Lash AE, Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30(1): 207–10. 11752295
33. McQuilton P, St. Pierre SE, Thurmond J, FlyBase CFlyBase 101 –the basics of navigating FlyBase. Nucleic Acids Res. 2012;40: D706–D14. doi: 10.1093/nar/gkr103022127867
34. Chen D, Berger J, Fellner M, Suzuki T, FLYSNPdb: a high-density SNP database of Drosophila melanogaster. Nucleic Acids Res. 2009;37: D567–D70. doi: 10.1093/nar/gkn58318784187
35. Hedges SB, Dudley J, Kumar S, TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics. 2006;22(23): 2971–2. 17021158
36. Ramaswami G, Zhang R, Piskol R, Keegan LP, Deng P, O'Connell MA, et al. Identifying RNA editing sites using RNA sequencing data alone. Nat Meth. 2013;10(2): 128–32.
37. Hoopengardner B, Bhalla T, Staber C, Reenan R, Nervous System Targets of RNA Editing Identified by Comparative Genomics. Science. 2003;301(5634): 832–6. 12907802
38. Stapleton M, Carlson JW, Celniker SE, RNA editing in Drosophila melanogaster: New targets and functional consequences. RNA. 2006;12(11): 1922–32. 17018572
39. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, et al. The developmental transcriptome of Drosophila melanogaster. Nature. 2011;471(7339): 473–9. doi: 10.1038/nature0971521179090
40. Lu Z, Matera AG, Vicinal: a method for the determination of ncRNA ends using chimeric reads from RNA-seq experiments. Nucleic Acids Res. 2014;42(9): e79–e. doi: 10.1093/nar/gku20724623808
41. Smibert P, Miura P, Westholm JO, Shenker S, May G, Duff MO, et al. Global Patterns of Tissue-Specific Alternative Polyadenylation in Drosophila. Cell reports. 2012;1(3): 277–89. 22685694
42. Keegan LP, Brindle J, Gallo A, Leroy A, Reenan RA, O'Connell MA, Tuning of RNA editing by ADAR is required in Drosophila. The EMBO Journal. 2005;24(12): 2183–93. 15920480
43. Li JB, Levanon EY, Yoon J-K, Aach J, Xie B, LeProust E, et al. Genome-Wide Identification of Human RNA Editing Sites by Parallel DNA Capturing and Sequencing. Science. 2009;324(5931): 1210–3. doi: 10.1126/science.117099519478186
44. Bazak L, Haviv A, Barak M, Jacob-Hirsch J, Deng P, Zhang R, et al. A-to-I RNA editing occurs at over a hundred million genomic sites, located in a majority of human genes. Genome Res. 2013;24(3): 365–76. doi: 10.1101/gr.164749.11324347612
45. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotech. 2010;28(5): 511–5.
46. Bonnet E, Wuyts J, Rouzé P, Van de Peer Y, Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences. Bioinformatics. 2004;20(17): 2911–7. 15217813
47. Clote P, FerrÉ F, Kranakis E, Krizanc D, Structural RNA has lower folding energy than random RNA of the same dinucleotide frequency. RNA. 2005;11(5): 578–91. 15840812
48. Lu ZJ, Yip KY, Wang G, Shou C, Hillier LW, Khurana E, et al. Prediction and characterization of noncoding RNAs in C. elegans by integrating conservation, secondary structure, and high-throughput sequencing and array data. Genome Res. 2011;21(2): 276–85. doi: 10.1101/gr.110189.11021177971
49. Juravleva EV, Mironov AA, Evolution of non-Coding RNAs in Drosophila melanogaster Genome. Biofizika. 2015;60(5): 906–13. 26591601
50. Lorenz R, Bernhart SH, Höner zu Siederdissen C, Tafer H, Flamm C, Stadler PF, et al. ViennaRNA Package 2.0. Algorithms for Molecular Biology: AMB. 2011;6: 26. doi: 10.1186/1748-7188-6-2622115189
51. Sakurai M, Ueda H, Yano T, Okada S, Terajima H, Mitsuyama T, et al. A biochemical landscape of A-to-I RNA editing in the human brain transcriptome. Genome Res. 2014;24(3): 522–34. doi: 10.1101/gr.162537.11324407955
52. Cohen O, Ashkenazy H, Belinky F, Huchon D, Pupko T, GLOOME: gain loss mapping engine. Bioinformatics. 2010;26(22): 2914–5. doi: 10.1093/bioinformatics/btq54920876605
53. Cohen O, Pupko T, Inference and Characterization of Horizontally Transferred Gene Families Using Stochastic Mapping. Mol Biol Evol. 2010;27(3): 703–13. doi: 10.1093/molbev/msp24019808865
54. Chen L, Characterization and comparison of human nuclear and cytosolic editomes. Proc Natl Acad Sci U S A. 2013;110(29): E2741–E7. doi: 10.1073/pnas.121888411023818636
55. Nei M, Kumar S, Molecular Evolution and Phylogenetics: Oxford University Press; 2000.
56. Young MD, Wakefield MJ, Smyth GK, Oshlack A, Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010;11(2): R14–R14. doi: 10.1186/gb-2010-11-2-r1420132535
57. Benjamini Y, Hochberg Y, Controlling the false discovery rate: a pratical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological). 1995;57: 12.
58. Ryan MY, Maloney R, Fineberg JD, Reenan RA, Horn R, RNA editing in eag potassium channels: Biophysical consequences of editing a conserved S6 residue. Channels. 2012;6(6): 443–52. doi: 10.4161/chan.2231423064203
59. Dickman DK, Kurshan PT, Schwarz TL, Mutations in a Drosophila α2δ Voltage-Gated Calcium Channel Subunit Reveal a Crucial Synaptic Function. The Journal of Neuroscience. 2008;28(1): 31–8. doi: 10.1523/JNEUROSCI.4498-07.200818171920
60. Ly CV, Yao C-K, Verstreken P, Ohyama T, Bellen HJ, straightjacket is required for the synaptic stabilization of cacophony, a voltage-gated calcium channel α(1) subunit. The Journal of Cell Biology. 2008;181(1): 157–70. doi: 10.1083/jcb.20071215218391075
61. Kurshan PT, Oztan A, Schwarz TL, Presynaptic [alpha]2[delta]-3 is required for synaptic morphogenesis independent of its Ca2+-channel functions. Nat Neurosci. 2009;12(11): 1415–23. doi: 10.1038/nn.241719820706
62. McGraw LA, Gibson G, Clark AG, Wolfner MF, Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster. Curr Biol. 2004Aug24;14(16): 1509–14. 15324670
63. Goldman TD, Arbeitman MN, Genomic and functional studies of Drosophila sex hierarchy regulated gene expression in adult head and nervous system tissues. PLoS Genet. 2007Nov;3(11): e216. 18039034
64. Alon S, Garrett SC, Levanon EY, Olson S, Graveley BR, Rosenthal JJC, et al. The majority of transcripts in the squid nervous system are extensively recoded by A-to-I RNA editing. eLife. 2015;4: e05198.
65. Sommer B, Kohler M, Sprengel R, Seeburg PH, RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell. 1991Oct4;67(1): 11–9. 1717158
66. Greger IH, Akamine P, Khatri L, Ziff EB, Developmentally regulated, combinatorial RNA processing modulates AMPA receptor biogenesis. Neuron. 2006Jul6;51(1): 85–97. 16815334
67. Jepson JEC, Reenan RA, RNA editing in regulating gene expression in the brain. Biochim Biophys Acta. 2008;1779(8): 459–70. 18086576
68. Jin Y, Zhang W, Li Q, Origins and evolution of ADAR-mediated RNA editing. IUBMB Life. 2009Jun;61(6): 572–8. doi: 10.1002/iub.20719472181
69. Maldonado C, Alicea D, Gonzalez M, Bykhovskaia M, Marie B, Adar is essential for optimal presynaptic function. Mol Cell Neurosci. 2013;52: 173–80. doi: 10.1016/j.mcn.2012.10.00923127996
70. Hanrahan CJ, Palladino MJ, Ganetzky B, Reenan RA, RNA Editing of the Drosophila para Na+ Channel Transcript: Evolutionary Conservation and Developmental Regulation. Genetics. 2000July1, 2000;155(3): 1149–60. 10880477
71. Wahlstedt H, Daniel C, Ensterö M, Öhman M, Large-scale mRNA sequencing determines global regulation of RNA editing during brain development. Genome Res. 2009;19(6): 978–86. doi: 10.1101/gr.089409.10819420382
72. Ohlson J, Pedersen JS, Haussler D, Öhman M, Editing modifies the GABA(A) receptor subunit α3. RNA. 2007;13(5): 698–703. 17369310
73. Joshi NA JN. F. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files. Available online. 2011.
74. Langmead B, Salzberg SL, Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4): 357–9. doi: 10.1038/nmeth.192322388286
75. Trapnell C, Pachter L, Salzberg SL, TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9): 1105–11. doi: 10.1093/bioinformatics/btp12019289445
76. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16): 2078–9. doi: 10.1093/bioinformatics/btp35219505943
77. Wang K, Li M, Hakonarson H, ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38(16): e164–e. doi: 10.1093/nar/gkq60320601685
78. Li L, Stoeckert CJ, Roos DS, OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes. Genome Res. 2003;13(9): 2178–89. 12952885
79. Cao Z, Yu Y, Wu Y, Hao P, Di Z, He Y, et al. The genome of Mesobuthus martensii reveals a unique adaptation model of arthropods. Nat Commun. [Article]. 2013;4.
80. Overbeek R, Fonstein M, D’Souza M, Pusch GD, Maltsev N, The use of gene clusters to infer functional coupling. Proc Natl Acad Sci U S A. 1999;96(6): 2896–901. 10077608
81. Yang Z, PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol. 2007;24(8): 1586–91. 17483113
82. Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, et al. The Ecoresponsive Genome of Daphnia pulex. Science. 2011;331(6017): 555–61. doi: 10.1126/science.119776121292972
83. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;44(D1): D279–D85. doi: 10.1093/nar/gkv134426673716