Novel modes of RNA editing in mitochondria

Nucleic Acids Research

Volumn 44, Issue 10, 2016, Pages 4907-4919

  Moreira, Sandrine ^a   Valach, Matus ^a   Aoulad Aissa, Mohamed ^a   Otto, Christian ^b   Burger, Gertraud ^a  

^a Universite de Montreal   (Canada)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; CYTOSINE; INOSINE; MESSENGER RNA; RIBOSOME RNA; TRANSCRIPTOME; URIDINE; RNA; RNA, MITOCHONDRIAL;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DIPLONEMA PAPILLATUM; DIPLONEMID; EUGLENOZOA; EUKARYOTE; GENE DELETION; GENE INSERTION; GENE SEQUENCE; GENE STRUCTURE; GENETIC TRANSCRIPTION; GENOME; MITOCHONDRION; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA EDITING; RNA STRUCTURE; SEQUENCE HOMOLOGY; CHEMISTRY; DEAMINATION; GENETICS; METABOLISM; MITOCHONDRIAL GENE; RNA GENE; TRANS SPLICING;

ADENOSINE; DEAMINATION; EUGLENOZOA; GENES, MITOCHONDRIAL; GENES, RRNA; INOSINE; MITOCHONDRIA; RNA; RNA EDITING; TRANS-SPLICING; TRANSCRIPTOME;

EID: 84973518527     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw188     Document Type: Article

References (81)

1. Maas, S., Kawahara, Y., Tamburro, K.M., and Nishikura, K. (2006). A-to-I RNA editing, and human disease. RNA Biol., 3, 1-9
2. Dunin-Horkawicz, S., Czerwoniec, A., Gajda, M.J., Feder, M., Grosjean, H., and Bujnicki, J.M. (2006). MODOMICS: a database of RNA modification pathways. Nucleic Acids Res., 34, D145-D149
3. Rodriguez, J., Menet, J.S., and Rosbash, M. (2012). Nascent-seq indicates widespread cotranscriptional RNA editing in Drosophila. Mol. Cell, 47, 27-37
4. Gott, J.M. (2003). Expanding genome capacity via RNA editing. C R Biol., 326, 901-908
5. Cheng, Y.W., Visomirski-Robic, L.M., and Gott, J.M. (2001). Non-templated addition of nucleotides to the 3? end of nascent RNA during RNA editing in Physarum. EMBO J., 20, 1405-1414
6. Jackson, C.J., Norman, J.E., Schnare, M.N., Gray, M.W., Keeling, P.J., and Waller, R.F. (2007). Broad genomic, and transcriptional analysis reveals a highly derived genome in dinoflagellate mitochondria. BMC Biol., 5, 41
7. Knoop, V. (2011). When you can?t trust the DNA: RNA editing changes transcript sequences. Cell Mol. Life Sci., 68, 567-586
8. Basilio, C., Wahba, A.J., Lengyel, P., Speyer, J.F., and Ochoa, S. (1962). Synthetic polynucleotides, and the amino acid code. V. Proc. Natl. Acad. Sci. U.S.A., 48, 613-616
9. Jackman, J.E., and Alfonzo, J.D. (2013). Transfer RNA modifications: nature?s combinatorial chemistry playground. Wiley Interdiscip. Rev. RNA, 4, 35-48
10. Betat, H., Long, Y., Jackman, J.E., and Morl, M. (2014). From end to end: tRNA editing at 5?-and 3?-terminal positions. Int. J. Mol. Sci., 15, 23975-23998
11. Benne, R., Van den Burg, J., Brakenhoff, J.P., Sloof, P., Van Boom, J.H., and Tromp, M.C. (1986). Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell, 46, 819-826
12. Grewe, F., Herres, S., Viehover, P., Polsakiewicz, M., Weisshaar, B., and Knoop, V. (2011). A unique transcriptome: 1782 positions of RNA editing alter 1406 codon identities in mitochondrial mRNAs of the lycophyte Isoetes engelmannii. Nucleic Acids Res., 39, 2890-2902
13. Hecht, J., Grewe, F., and Knoop, V. (2011). Extreme RNA editing in coding islands, and abundant microsatellites in repeat sequences of Selaginella moellendorffii mitochondria: the root of frequent plant mtDNA recombination in early tracheophytes. Genome Biol. Evol., 3, 344-358
14. Rüdinger, M., Fritz-Laylin, L., Polsakiewicz, M., and Knoop, V. (2011). Plant-type mitochondrial RNA editing in the protist Naegleria gruberi. RNA, 17, 2058-2062
15. Fu, C.J., Sheikh, S., Miao, W., Andersson, S.G., and Baldauf, S.L. (2014). Missing genes, multiple ORFs, and C-to-U type RNA editing in Acrasis kona (Heterolobosea, Excavata) mitochondrial DNA. Genome Biol. Evol., 6, 2240-2257
16. Burger, G., Yan, Y., Javadi, P., and Lang, B.F. (2009). Group I-intron trans-splicing, and mRNA editing in the mitochondria of placozoan animals. Trends Genet., 25, 381-386
17. Janke, A., and Paabo, S. (1993). Editing of a tRNA anticodon in marsupial mitochondria changes its codon recognition. Nucleic Acids Res., 21, 1523-1525
18. Randau, L., Stanley, B.J., Kohlway, A., Mechta, S., Xiong, Y., and Soll, D. (2009). A cytidine deaminase edits C to U in transfer RNAs in Archaea. Science, 324, 657-659
19. Rosenberg, B.R., Hamilton, C.E., Mwangi, M.M., Dewell, S., and Papavasiliou, F.N. (2011). Transcriptome-wide sequencing reveals numerous APOBEC1 mRNA-editing targets in transcript 3? UTRs. Nat. Struct. Mol. Biol., 18, 230-236
20. Powell, L.M., Wallis, S.C., Pease, R.J., Edwards, Y.H., Knott, T.J., and Scott, J. (1987). A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell, 50, 831-840
21. Takenaka, M., Zehrmann, A., Verbitskiy, D., Hartel, B., and Brennicke, A. (2013). RNA editing in plants, and its evolution. Annu. Rev. Genet., 47, 335-352
22. Wulff, B.E., and Nishikura, K. (2010). Substitutional A-to-I RNA editing. Wiley Interdiscip. Rev. RNA, 1, 90-101
23. Kleinman, C.L., and Majewski, J. (2012). Comment on ?Widespread RNA, and DNA sequence differences in the human transcriptome?. Science, 335, 1302
24. Simpson, L., Thiemann, O.H., Savill, N.J., Alfonzo, J.D., and Maslov, D.A. (2000). Evolution of RNA editing in trypanosome mitochondria. Proc. Natl. Acad. Sci. U.S.A., 97, 6986-6993
25. Lukes, J., Flegontova, O., and Horak, A. (2015). Diplonemids. Curr. Biol., 25, R702-R704
26. De Vargas, C., Audic, S., Henry, N., Decelle, J., Mahe, F., Logares, R., Lara, E., Berney, C., Le Bescot, N., Probert, I., et al. (2015). Ocean plankton. Eukaryotic plankton diversity in the sunlit ocean. Science, 348, 1261605
27. Lara, E., Moreira, D., Vereshchaka, A., and Lopez-Garcia, P. (2009). Pan-oceanic distribution of new highly diverse clades of deep-sea diplonemids. Environ. Microbiol., 11, 47-55
28. Marande, W., and Burger, G. (2007). Mitochondrial DNA as a genomic jigsaw puzzle. Science, 318, 415
29. Vlcek, C., Marande, W., Teijeiro, S., Lukeš, J., and Burger, G. (2011). Systematically fragmented genes in a multipartite mitochondrial genome. Nucleic Acids Res., 39, 979-988
30. Kiethega, G.N., Yan, Y., Turcotte, M., and Burger, G. (2013). RNA-level unscrambling of fragmented genes in Diplonema mitochondria. RNA Biol., 10, 301-313
31. Kiethega, G.N., Turcotte, M., and Burger, G. (2011). Evolutionary conserved cox1 trans-splicing without cis-motifs. Mol. Biol. Evol., 28, 2425-2458
32. Valach, M., Moreira, S., Kiethega, G.N., and Burger, G. (2014). Trans-splicing, and RNA editing of LSU rRNA in Diplonema mitochondria. Nucleic Acids Res., 42, 2660-2672
33. Rodriguez-Ezpeleta, N., Teijeiro, S., Forget, L., Burger, G., and Lang, B.F. (2009). Construction of cDNA libraries: focus on protists, and fungi. In: Parkinson, J (ed). Methods in Molecular Biology: Expressed Sequence Tags (ESTs). Humana Press, Totowa, NJ, Vol. 533, 33-47
34. Cattenoz, P.B., Taft, R.J., Westhof, E., and Mattick, J.S. (2013). Transcriptome-wide identification of A >I RNA editing sites by inosine specific cleavage. RNA, 19, 257-270
35. Morse, D.P., and Bass, B.L. (1997). Detection of inosine in messenger RNA by inosine-specific cleavage. Biochemistry, 36, 8429-8434
36. Myers, E.W., Sutton, G.G., Delcher, A.L., Dew, I.M., Fasulo, D.P., Flanigan, M.J., Kravitz, S.A., Mobarry, C.M., Reinert, K.H., Remington, K.A., et al. (2000). A whole-genome assembly of Drosophila. Science, 287, 2196-2204
37. Li, W., Jaroszewski, L., and Godzik, A. (2002). Tolerating some redundancy significantly speeds up clustering of large protein databases. Bioinformatics, 18, 77-82
38. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast, and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25
39. Thorvaldsdottir, H., Robinson, J.T., and Mesirov, J.P. (2013). Integrative Genomics Viewer (IGV): high-performance genomics data visualization, and exploration. Brief. Bioinform., 14, 178-192
40. Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy, and high throughput. Nucleic Acids Res., 32, 1792-1797
41. Valdar, W.S. (2002). Scoring residue conservation. Proteins, 48, 227-241
42. Xie, Y., Wu, G., Tang, J., Luo, R., Patterson, J., Liu, S., Huang, W., He, G., Gu, S., Li, S., et al. (2014). SOAPdenovo-Trans: De novo transcriptome assembly with short RNA-Seq reads. Bioinformatics, 30, 1660-1666
43. Luo, R., Liu, B., Xie, Y., Li, Z., Huang, W., Yuan, J., He, G., Chen, Y., Pan, Q., Liu, Y., et al. (2012). SOAPdenovo2: an empirically improved memory-efficient short-read De novo assembler. Gigascience, 1, 18
44. Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol., 29, 644-652
45. DePristo, M.A., Banks, E., Poplin, R., Garimella, K.V., Maguire, J.R., Hartl, C., Philippakis, A.A., del Angel, G., Rivas, M.A., Hanna, M., et al. (2011). A framework for variation discovery, and genotyping using next-generation DNA sequencing data. Nat. Genet., 43, 491-498
46. Van der Auwera, G.A., Carneiro, M.O., Hartl, C., Poplin, R., Del Angel, G., Levy-Moonshine, A., Jordan, T., Shakir, K., Roazen, D., Thibault, J., et al. (2013). From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinformatics, 11, 11-33
47. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W., and Noble, W.S. (2009). MEME SUITE: tools for motif discovery, and searching. Nucleic Acids Res., 37, W202-W208
48. Mathews, D.H. (2014). Using the RNAstructure Software Package to predict conserved RNA structures. Curr. Protoc. Bioinformatics, 46, 11-22
49. Bellaousov, S., Reuter, J.S., Seetin, M.G., and Mathews, D.H. (2013). RNAstructure: web servers for RNA secondary structure prediction, and analysis. Nucleic Acids Res., 41, W471-W474
50. Lorenz, R., Bernhart, S.H., Honer Zu Siederdissen, C., Tafer, H., Flamm, C., Stadler, P.F., and Hofacker, I.L. (2011). ViennaRNA Package 2.0. Algorithms Mol. Biol., 6, 26
51. Will, S., Joshi, T., Hofacker, I.L., Stadler, P.F., and Backofen, R. (2012). LocARNA-P: accurate boundary prediction, and improved detection of structural RNAs. RNA, 18, 900-914
52. Smith, C., Heyne, S., Richter, A.S., Will, S., and Backofen, R. (2010). Freiburg RNA Tools: a web server integrating INTARNA, EXPARNA, and LOCARNA. Nucleic Acids Res., 38, W373-W377
53. Sonnhammer, E.L., and Durbin, R. (1995). A dot-matrix program with dynamic threshold control suited for genomic DNA, and protein sequence analysis. Gene, 167, GC1-GC10
54. Kall, L., Krogh, A., and Sonnhammer, E.L. (2004). A combined transmembrane topology, and signal peptide prediction method. J. Mol. Biol., 338, 1027-1036
55. Artimo, P., Jonnalagedda, M., Arnold, K., Baratin, D., Csardi, G., De Castro, E., Duvaud, S., Flegel, V., Fortier, A., Gasteiger, E., et al. (2012). ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res., 40, W597-W603
56. Pett, W., Ryan, J.F., Pang, K., Mullikin, J.C., Martindale, M.Q., Baxevanis, A.D., and Lavrov, D.V. (2011). Extreme mitochondrial evolution in the ctenophore Mnemiopsis leidyi: Insight from mtDNA, and the nuclear genome. Mitochondrial DNA, 22, 130-142
57. Spencer, D.F., and Gray, M.W. (2011). Ribosomal RNA genes in Euglena gracilis mitochondrial DNA: fragmented genes in a seemingly fragmented genome. Mol. Genet. Genomics, 285, 19-31
58. Feagin, J.E., Mericle, B.L., Werner, E., and Morris, M. (1997). Identification of additional rRNA fragments encoded by the Plasmodium falciparum 6 kb element. Nucleic Acids Res., 25, 438-446
59. Driscoll, D.M., and Innerarity, T.L. (2001). RNA editing by cytidine deamination in mammals. In: Bass, BL (ed). RNA Editing. Oxford University Press, Oxford, Vol. 34, pp. 61-76
60. Mower, J.P., and Palmer, J.D. (2006). Patterns of partial RNA editing in mitochondrial genes of Beta vulgaris. Mol. Genet. Genomics, 276, 285-293
61. Picardi, E., Horner, D.S., Chiara, M., Schiavon, R., Valle, G., and Pesole, G. (2010). Large-scale detection, and analysis of RNA editing in grape mtDNA by RNA deep-sequencing. Nucleic Acids Res., 38, 4755-4767
62. Inada, M., Sasaki, T., Yukawa, M., Tsudzuki, T., and Sugiura, M. (2004). A systematic search for RNA editing sites in pea chloroplasts: an editing event causes diversification from the evolutionarily conserved amino acid sequence. Plant Cell Physiol., 45, 1615-1622
63. Verbitskiy, D., Takenaka, M., Neuwirt, J., van der Merwe, J.A., and Brennicke, A. (2006). Partially edited RNAs are intermediates of RNA editing in plant mitochondria. Plant J., 47, 408-416
64. Cardi, T., Giegé, P., Kahlau, S., and Scotti, N. (2012). Expression profiling of organellar genes. In: Bock, R, and Knoop, V (eds). Genomics of Chloroplasts, and Mitochondria. Springer, Heidelberg, Vol. 35, pp. 323-355
65. Yusupov, M.M., Yusupova, G.Z., Baucom, A., Lieberman, K., Earnest, T.N., Cate, J.H., and Noller, H.F. (2001). Crystal structure of the ribosome at 5.5 A resolution. Science, 292, 883-896
66. Cannone, J.J., Subramanian, S., Schnare, M.N., Collett, J.R., D?Souza, L.M., Du, Y., Feng, B., Lin, N., Madabusi, L.V., Muller, K.M., et al. (2002). The comparative RNA web (CRW) site: an online database of comparative sequence, and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics, 3, 2
67. Aphasizheva, I., and Aphasizhev, R. (2010). RET1-catalyzed uridylylation shapes the mitochondrial transcriptome in Trypanosoma brucei. Mol. Cell. Biol., 30, 1555-1567
68. Mungpakdee, S., Shinzato, C., Takeuchi, T., Kawashima, T., Koyanagi, R., Hisata, K., Tanaka, M., Goto, H., Fujie, M., Lin, S., et al. (2014). Massive gene transfer, and extensive RNA editing of a symbiotic dinoflagellate plastid genome. Genome Biol. Evol., 6, 1408-1422
69. Roy, J., Faktorova, D., Benada, O., Lukes, J., and Burger, G. (2007). Description of Rhynchopus euleeides n. sp. (Diplonemea), a free-living marine euglenozoan. J. Eukaryot. Microbiol., 54, 137-145
70. Simpson, L. (1987). The mitochondrial genome of kinetoplastid protozoa: genomic organization, transcription, replication, and evolution. Annu. Rev. Microbiol., 41, 363-382
71. Lavrov, D.V., Adamski, M., Chevaldonné, P., and Adamska, M. (2016). Extensive mitochondrial mRNA editing, and unusual mitochondrial genome organization in calcaronean sponges. Curr. Biol., 26, 86-92
72. Alseth, I., Dalhus, B., and Bjoras, M. (2014). Inosine in DNA, and RNA. Curr. Opin. Genet. Dev., 26, 116-123
73. Gray, M.W. (1976). O2?-Methylinosine, a constituent of the ribosomal RNA of Crithidia fasciculata. Nucleic Acids Res., 3, 977-988
74. Murphy, F.V.t., and Ramakrishnan, V. (2004). Structure of a purine-purine wobble base pair in the decoding center of the ribosome. Nat. Struct. Mol. Biol., 11, 1251-1252
75. Blanc, V., Park, E., Schaefer, S., Miller, M., Lin, Y., Kennedy, S., Billing, A.M., Ben Hamidane, H., Graumann, J., Mortazavi, A., et al. (2014). Genome-wide identification, and functional analysis of Apobec-1-mediated C-to-U RNA editing in mouse small intestine, and liver. Genome Biol., 15, R79
76. Hough, R.F., and Bass, B.L. (2001). Adenosine deaminases that act on RNA. In: Bass, BL (ed). RNA Editing. Oxford University Press, Oxford, pp. 77-108
77. Aphasizhev, R., and Aphasizheva, I. (2011). Uridine insertion/deletion editing in trypanosomes: a playground for RNA-guided information transfer. Wiley Interdiscip. Rev. RNA, 2, 669-685
78. Nishikura, K. (2010). Functions, and regulation of RNA editing by ADAR deaminases. Annu. Rev. Biochem., 79, 321-349
79. Stoltzfus, A. (1999). On the possibility of constructive neutral evolution. J. Mol. Evol., 49, 169-181
80. Jacob, F. (1977). Evolution, and tinkering. Science, 196, 1161-1166
81. Göringer, H.U. (2012). ?Gestalt, composition, and function of the Trypanosoma brucei editosome. Annu. Rev. Microbiol., 66, 65-82