RNA Editing in Mitochondrial Trans-Introns Is Required for Splicing

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Farré, Jean Claude ^a,d   Aknin, Cindy ^a   Araya, Alejandro ^a,b   Castandet, Benoît ^a,c  

^a University Victor Segalen   (France)

^b Univ Bordeaux   (France)

^c United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; CYTOSINE; MESSENGER RNA; MITOCHONDRIAL RNA; URIDINE;

ARTICLE; GENE MUTATION; IN VIVO STUDY; INTRON; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; RNA ANALYSIS; RNA EDITING; RNA SPLICING; RNA STRUCTURE; SEQUENCE HOMOLOGY; TRANS SPLICING; TRANSGENE; WHEAT;

BASE SEQUENCE; EXONS; GENE ORDER; GENES, PLANT; INTRONS; MITOCHONDRIA; MUTATION; NUCLEIC ACID CONFORMATION; RNA EDITING; RNA, PLANT; TRANS-SPLICING; TRANSGENES; TRITICUM;

TRITICUM AESTIVUM;

EID: 84871445428     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052644     Document Type: Article

References (53)

1. Liere K, Weihe A, Borner T, (2011) The transcription machineries of plant mitochondria and chloroplasts: Composition, function, and regulation. J Plant Physiol 168: 1345-1360.
2. Kuhn K, Weihe A, Borner T, (2005) Multiple promoters are a common feature of mitochondrial genes in Arabidopsis. Nucleic Acids Res 33: 337-346.
3. Bonen L, (2008) Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion 8: 26-34.
4. Castandet B, Araya A, (2011) RNA editing in plant organelles. Why make it easy? Biochemistry (Moscow) 76: 924-931.
5. Blanc V, Litvak S, Araya A, (1995) RNA editing in wheat mitochondria proceeds by a deamination mechanism. FEBS Lett 373: 56-60.
6. Bégu D, Graves PV, Domec C, Arselin G, Litvak S, et al. (1990) RNA editing of wheat mitochondrial ATP synthase subunit 9: direct protein and cDNA sequencing. Plant Cell 2: 1283-1290.
7. Covello PS, Gray MW, (1990) RNA sequence and the nature of the CuA-binding site in cytochrome c oxidase. FEBS Lett 268: 5-7.
8. Hernould M, Suharsono S, Litvak S, Araya A, Mouras A, (1993) Male-sterility induction in transgenic tobacco plants with an unedited atp9 mitochondrial gene from wheat. Proc Natl Acad Sci U S A 90: 2370-2374.
9. Zabaleta E, Mouras A, Hernould M, Suharsono, Araya A, (1996) Transgenic male-sterile plant induced by an unedited atp9 gene is restored to fertility by inhibiting its expression with antisense RNA. Proc Natl Acad Sci U S A 93: 11259-11263.
10. Sharp PA, (1991) "Five easy pieces". Science 254: 663.
11. Martin W, Koonin EV, (2006) Introns and the origin of nucleus-cytosol compartmentalization. Nature 440: 41-45.
12. Michel F, Ferat JL, (1995) Structure and activities of group II introns. Annu Rev Biochem 64: 435-461.
13. Waldsich C, Pyle AM, (2007) A folding control element for tertiary collapse of a group II intron ribozyme. Nat Struct Mol Biol 14: 37-44.
14. Zanlungo S, Quinones V, Moenne A, Holuigue L, Jordana X, (1995) Splicing and editing of rps10 transcripts in potato mitochondria. Curr Genet 27: 565-571.
15. Wissinger B, Schuster W, Brennicke A, (1991) Trans splicing in Oenothera mitochondria: nad1 mRNAs are edited in exon and trans-splicing group II intron sequences. Cell 65: 473-482.
16. Binder S, Marchfelder A, Brennicke A, Wissinger B, (1992) RNA editing in trans-splicing intron sequences of nad2 mRNAs in Oenothera mitochondria. J Biol Chem 267: 7615-7623.
17. Bégu D, Castandet B, Araya A, (2011) RNA editing restores critical domains of a group I intron in fern mitochondria. Curr Genet 57: 317-325.
18. Börner GV, Morl M, Wissinger B, Brennicke A, Schmelzer C, (1995) RNA editing of a group II intron in Oenothera as a prerequisite for splicing. Mol Gen Genet 246: 739-744.
19. Carrillo C, Bonen L, (1997) RNA editing status of nad7 intron domains in wheat mitochondria. Nucleic Acids Res 25: 403-409.
20. Castandet B, Choury D, Bégu D, Jordana X, Araya A, (2010) Intron RNA editing is essential for splicing in plant mitochondria. Nucleic Acids Res 38: 7112-7121.
21. Chapdelaine Y, Bonen L, (1991) The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: a trans-splicing model for this gene-in-pieces. Cell 65: 465-472.
22. Pereira de Souza A, Jubier MF, Delcher E, Lancelin D, Lejeune B, (1991) A trans-splicing model for the expression of the tripartite nad5 gene in wheat and maize mitochondria. Plant Cell 3: 1363-1378.
23. Bégu D, Mercado A, Farré JC, Moenne A, Holuigue L, et al. (1998) Editing status of mat-r transcripts in mitochondria from two plant species: C-to-U changes occur in putative functional RT and maturase domains. Curr Genet 33: 420-428.
24. Farré JC, Araya A, (1999) The mat-r open reading frame is transcribed from a non-canonical promoter and contains an internal promoter to co-transcribe exons nad1e and nad5III in wheat mitochondria. Plant Mol Biol 40: 959-967.
25. Li CF, Costa M, Michel F, (2011) Linking the branchpoint helix to a newly found receptor allows lariat formation by a group II intron. EMBO J 30: 3040-3051.
26. Schmelzer C, Schweyen RJ, (1986) Self-splicing of group II introns in vitro: mapping of the branch point and mutational inhibition of lariat formation. Cell 46: 557-565.
27. Schlatterer JC, Crayton SH, Greenbaum NL, (2006) Conformation of the Group II intron branch site in solution. J Am Chem Soc 128: 3866-3867.
28. de Longevialle AF, Meyer EH, Andrés C, Taylor NL, Lurin C, et al. (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 Intron 1 in Arabidopsis thaliana. Plant Cell 19: 3256-3265.
29. Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, et al. (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18: 2650-2663.
30. de Longevialle AF, Small ID, Lurin C, (2010) Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol Plant 3: 691-705.
31. Farré JC, Choury D, Araya A, (2007) In organello gene expression and RNA editing studies by electroporation-mediated transformation of isolated plant mitochondria. Methods Enzymol 424: 483-500.
32. Carrillo C, Chapdelaine Y, Bonen L, (2001) Variation in sequence and RNA editing within core domains of mitochondrial group II introns among plants. Mol Gen Genet 264: 595-603.
33. Li-Pook-Than J, Bonen L, (2006) Multiple physical forms of excised group II intron RNAs in wheat mitochondria. Nucleic Acids Res 34: 2782-2790.
34. Vogel J, Borner T, (2002) Lariat formation and a hydrolytic pathway in plant chloroplast group II intron splicing. EMBO J 21: 3794-3803.
35. Pyle AM, (2010) The tertiary structure of group II introns: implications for biological function and evolution. Crit Rev Biochem Mol Biol 45: 215-232.
36. Choury D, Farre JC, Jordana X, Araya A, (2005) Gene expression studies in isolated mitochondria: Solanum tuberosum rps10 is recognized by cognate potato but not by the transcription, splicing and editing machinery of wheat mitochondria. Nucleic Acids Res 33: 7058-7065.
37. Farré JC, Araya A, (2001) Gene expression in isolated plant mitochondria: high fidelity of transcription, splicing and editing of a transgene product in electroporated organelles. Nucleic Acids Res 29: 2484-2491.
38. Elina H, Brown GG, (2010) Extensive mis-splicing of a bi-partite plant mitochondrial group II intron. Nucleic Acids Res 38: 996-1008.
39. Farré JC, Araya A, (2002) RNA splicing in higher plant mitochondria: determination of functional elements in group II intron from a chimeric cox II gene in electroporated wheat mitochondria. Plant J 29: 203-213.
40. van der Veen R, Kwakman JH, Grivell LA, (1987) Mutations at the lariat acceptor site allow self-splicing of a group II intron without lariat formation. EMBO J 6: 3827-3831.
41. Daniels DL, Michels WJ Jr, Pyle AM, (1996) Two competing pathways for self-splicing by group II introns: a quantitative analysis of in vitro reaction rates and products. J Mol Biol 256: 31-49.
42. Chu VT, Liu Q, Podar M, Perlman PS, Pyle AM, (1998) More than one way to splice an RNA: branching without a bulge and splicing without branching in group II introns. RNA 4: 1186-1202.
43. Jarrell KA, Dietrich RC, Perlman PS, (1988) Group II intron domain 5 facilitates a trans-splicing reaction. Mol Cell Biol 8: 2361-2366.
44. Chanfreau G, Jacquier A, (1996) An RNA conformational change between the two chemical steps of group II self-splicing. EMBO J 15: 3466-3476.
45. Costa M, Deme E, Jacquier A, Michel F, (1997) Multiple tertiary interactions involving domain II of group II self-splicing introns. J Mol Biol 267: 520-536.
46. Hamill S, Pyle AM, (2006) The receptor for branch-site docking within a group II intron active site. Mol Cell 23: 831-840.
47. Li CF, Costa M, Bassi G, Lai YK, Michel F, (2011) Recurrent insertion of 5′-terminal nucleotides and loss of the branchpoint motif in lineages of group II introns inserted in mitochondrial preribosomal RNAs. RNA 17: 1321-1335.
48. Granlund M, Michel F, Norgren M, (2001) Mutually exclusive distribution of IS1548 and GBSi1, an active group II intron identified in human isolates of group B streptococci. J Bacteriol 183: 2560-2569.
49. Toor N, Robart AR, Christianson J, Zimmerly S, (2006) Self-splicing of a group IIC intron: 5′ exon recognition and alternative 5′ splicing events implicate the stem-loop motif of a transcriptional terminator. Nucleic Acids Res 34: 6461-6471.
50. Osenberg S, Paz Yaacov N, Safran M, Moshkovitz S, Shtrichman R, et al. (2010) Alu sequences in undifferentiated human embryonic stem cells display high levels of A-to-I RNA editing. PLoS One 5: e11173.
51. Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M, et al. (2004) Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat Biotechnol 22: 1001-1005.
52. Laurencikiene J, Kallman AM, Fong N, Bentley DL, Ohman M, (2006) RNA editing and alternative splicing: the importance of co-transcriptional coordination. EMBO Rep 7: 303-307.
53. Finta C, Zaphiropoulos PG, (2002) Intergenic mRNA molecules resulting from trans-splicing. J Biol Chem 277: 5882-5890.