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Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria

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Abstract

During evolution, most of the bacterial genes from the ancestral endosymbiotic α-proteobacteria at the origin of mitochondria have been either lost or transferred to the nuclear genome. A crucial evolutionary step was the establishment of macromolecule import systems to allow the come back of proteins and RNAs into the organelle. Paradoxically, the few mitochondria-encoded protein genes remain essential and must be translated by a mitochondrial translation machinery mainly constituted by nucleus-encoded components. Two crucial partners of the mitochondrial translation machinery are the aminoacyl-tRNA synthetases and the tRNAs. All mitochondrial aminoacyl-tRNA synthetases and many tRNAs are imported from the cytosol into the mitochondria in eukaryotic cells. During the last few years, their origin and their import into the organelle have been studied in evolutionary distinct organisms and we review here what is known in this field.

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References

  • Akashi K, Grandjean O, Small I (1998a) Potential dual targeting of an Arabidopsis archaebacterial-like histidyl-tRNA synthetase to mitochondria and chloroplasts. FEBS Lett 431:39–44

    PubMed  CAS  Google Scholar 

  • Akashi K, Takenaka M, Yamaoka S, Suyama Y, Fukuzawa H, Ohyama K (1998b) Coexistence of nuclear DNA-encoded tRNAVal(AAC) and mitochondrial DNA-encoded tRNAVal(UAC) in mitochondria of a liverwort Marchantia polymorpha. Nucleic Acids Res 26:2168–2172

    PubMed  CAS  Google Scholar 

  • Baker MJ, Frazier AE, Gulbis JM, Ryan MT (2007) Mitochondrial protein-import machinery: correlating structure with function. Trends Cell Biol 17:456–464

    PubMed  CAS  Google Scholar 

  • Berg M, Rogers R, Muralla R, Meinke D (2005) Requirement of aminoacyl-tRNA synthetases for gametogenesis and embryo development in Arabidopsis. Plant J 44:866–878

    PubMed  CAS  Google Scholar 

  • Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, Bohme U, Hannick L, Aslett MA, Shallom J, Marcello L, Hou L, Wickstead B, Alsmark UC, Arrowsmith C, Atkin RJ, Barron AJ, Bringaud F, Brooks K, Carrington M, Cherevach I, Chillingworth TJ, Churcher C, Clark LN, Corton CH, Cronin A, Davies RM, Doggett J, Djikeng A, Feldblyum T, Field MC, Fraser A, Goodhead I, Hance Z, Harper D, Harris BR, Hauser H, Hostetler J, Ivens A, Jagels K, Johnson D, Johnson J, Jones K, Kerhornou AX, Koo H, Larke N, Landfear S, Larkin C, Leech V, Line A, Lord A, Macleod A, Mooney PJ, Moule S, Martin DM, Morgan GW, Mungall K, Norbertczak H, Ormond D, Pai G, Peacock CS, Peterson J, Quail MA, Rabbinowitsch E, Rajandream MA, Reitter C, Salzberg SL, Sanders M, Schobel S, Sharp S, Simmonds M, Simpson AJ, Tallon L, Turner CM, Tait A, Tivey AR, Van Aken S, Walker D, Wanless D, Wang S, White B, White O, Whitehead S, Woodward J, Wortman J, Adams MD, Embley TM, Gull K, Ullu E, Barry JD, Fairlamb AH, Opperdoes F, Barrell BG, Donelson JE, Hall N, Fraser CM, Melville SE, El-Sayed NM (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309:416–422

    PubMed  CAS  Google Scholar 

  • Bhattacharyya SN, Adhya S (2004) The complexity of mitochondrial tRNA import. RNA Biol 1:84–88

    PubMed  CAS  Google Scholar 

  • Bhattacharyya SN, Chatterjee S, Adhya S (2002) Mitochondrial RNA import in Leishmania tropica: aptamers homologous to multiple tRNA domains that interact cooperatively or antagonistically at the inner membrane. Mol Cell Biol 22:4372–4382

    PubMed  CAS  Google Scholar 

  • Bhattacharyya SN, Chatterjee S, Goswami S, Tripathi G, Dey SN, Adhya S (2003) “Ping-pong” interactions between mitochondrial tRNA import receptors within a multiprotein complex. Mol Cell Biol 23:5217–5224

    PubMed  CAS  Google Scholar 

  • Bonnefond L, Fender A, Rudinger-Thirion J, Giege R, Florentz C, Sissler M (2005) Toward the full set of human mitochondrial aminoacyl-tRNA synthetases: characterization of AspRS and TyrRS. Biochemistry 44:4805–4816

    PubMed  CAS  Google Scholar 

  • Bouzaidi-Tiali N, Aeby E, Charriere F, Pusnik M, Schneider A (2007) Elongation factor 1a mediates the specificity of mitochondrial tRNA import in T. brucei. EMBO J 26:4302–4312

    PubMed  CAS  Google Scholar 

  • Brindefalk B, Viklund J, Larsson D, Thollesson M, Andersson SG (2007) Origin and evolution of the mitochondrial aminoacyl-tRNA synthetases. Mol Biol Evol 24:743–756

    PubMed  CAS  Google Scholar 

  • Burger G, Gray M, Lang B (2003) Mitochondrial genomes: anything goes. Trends Genet 19:709–716

    PubMed  CAS  Google Scholar 

  • Charriere F, Helgadottir S, Horn EK, Soll D, Schneider A (2006) Dual targeting of a single tRNA(Trp) requires two different tryptophanyl-tRNA synthetases in Trypanosoma brucei. Proc Natl Acad Sci USA 103:6847–6852

    PubMed  CAS  Google Scholar 

  • Chatton B, Walter P, Ebel JP, Lacroute F, Fasiolo F (1988) The yeast VAS1 gene both mitochondrial and cytoplasmic Valyl-tRNA synthetases. J Biol Chem 263:52–57

    PubMed  CAS  Google Scholar 

  • Chen DT, Shi X, Suyama Y (1994) In vivo expression and mitochondrial import of normal and mutated tRNAthr in Leishmania. Mol Biochem Parasitol 64:121–133

    PubMed  CAS  Google Scholar 

  • Chen H-C, Viry-Moussaïd M, Dietrich A, Wintz H (1997) Evolution of a mitochondrial tRNAPhe gene in A. thaliana: import of cytosolic tRNAPhe into mitochondria. Biochem Biophys Res Commun 237:432–437

    PubMed  CAS  Google Scholar 

  • Chihara T, Luginbuhl D, Luo L (2007) Cytoplasmic and mitochondrial protein translation in axonal and dendritic terminal arborization. Nat Neurosci 10:828–837

    PubMed  CAS  Google Scholar 

  • Delage L, Dietrich A, Cosset A, Maréchal-Drouard L (2003a) In vitro import of a nuclearly encoded tRNA into mitochondria of Solanum tuberosum. Mol Cell Biol 23:4000–4012

    PubMed  CAS  Google Scholar 

  • Delage L, Duchêne AM, Zaepfel M, Maréchal-Drouard L (2003b) The anticodon and the D-domain sequences are essential determinants for plant cytosolic tRNA(Val) import into mitochondria. Plant J 34:623–633

    PubMed  CAS  Google Scholar 

  • Dietrich A, Maréchal-Drouard L, Carneiro V, Cosset A, Small I (1996) A single base change prevents import of cytosolic tRNA(Ala) into mitochondria in transgenic plants. Plant J 10:913–918

    PubMed  CAS  Google Scholar 

  • Dietrich A, Souciet G, Colas B, Weil JH (1983) Phaseolus vulgaris cytoplasmic leucyl-tRNA synthetase. Purification and comparison of its catalytic, structural, and immunological properties with those of the chloroplastic enzyme. J Biol Chem 258:12386–12393

    PubMed  CAS  Google Scholar 

  • Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14:307–311

    PubMed  CAS  Google Scholar 

  • Dorner M, Altmann M, Paabo S, Morl M (2001) Evidence for import of a lysyl-tRNA into marsupial mitochondria. Mol Biol Cell 12:2688–2698

    PubMed  CAS  Google Scholar 

  • Duchêne A-M, Maréchal-Drouard L (2001) The chloroplast derived trnW and trnM-e genes are not expressed in Arabidopsis mitochondria. Biochem Biophys Res Commun 285:1213–1216

    PubMed  Google Scholar 

  • Duchêne AM, Peeters N, Dietrich A, Cosset A, Small ID, Wintz H (2001) Overlapping destinations for two dual targeted glycyl-tRNA synthetases in Arabidopsis thaliana and Phaseolus vulgaris. J Biol Chem 276:15275–15283

    PubMed  Google Scholar 

  • Duchêne AM, Giritch A, Hoffmann B, Cognat V, Lancelin D, Peeters NM, Zaepfel M, Maréchal-Drouard L, Small ID (2005) Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:16484–16489

    PubMed  Google Scholar 

  • Edvardson S, Shaag A, Kolesnikova O, Gomori JM, Tarassov I, Einbinder T, Saada A, Elpeleg O (2007) Deleterious mutation in the mitochondrial arginyl-transfer RNA synthetase gene is associated with pontocerebellar hypoplasia. Am J Hum Genet 81:857–862

    PubMed  CAS  Google Scholar 

  • Entelis NS, Kieffer S, Kolesnikova OA, Martin RP, Tarassov IA (1998) Structural requirements of tRNALys for its import into yeast mitochondria. Proc Natl Acad Sci USA 95:2838–2843

    PubMed  CAS  Google Scholar 

  • Entelis NS, Kolesnikova OA, Dogan S, Martin RP, Tarassov IA (2001a) 5 S rRNA and tRNA import into human mitochondria. Comparison of in vitro requirements. J Biol Chem 276:45642–45653

    PubMed  CAS  Google Scholar 

  • Entelis NS, Kolesnikova OA, Martin RP, Tarassov IA (2001b) RNA delivery into mitochondria. Adv Drug Deliv Rev 49:199–215

    PubMed  CAS  Google Scholar 

  • Entelis N, Brandina I, Kamenski P, Krasheninnikov IA, Martin RP, Tarassov I (2006) A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae. Genes Dev 20:1609–1620

    PubMed  CAS  Google Scholar 

  • Florentz C, Sohm B, Tryoen-Toth P, Putz J, Sissler M (2003) Human mitochondrial tRNAs in health and disease. Cell Mol Life Sci 60:1356–1375

    PubMed  CAS  Google Scholar 

  • Garcia LT, Leite NR, Alfonzo JD, Thiemann OH (2007) Effects of Trypanosoma brucei tryptophanyl-tRNA synthetases silencing by RNA interference. Mem Inst Oswaldo Cruz 102:757–762

    PubMed  CAS  Google Scholar 

  • Glover KE, Spencer DF, Gray MW (2001) Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria. J Biol Chem 276:639–648

    PubMed  CAS  Google Scholar 

  • Helm M, Brule H, Friede D, Giege R, Putz D, Florentz C (2000) Search for characteristic structural features of mammalian mitochondrial tRNAs. RNA 6:1356–1379

    PubMed  CAS  Google Scholar 

  • Henkin TM, Glass BL, Grundy FJ (1992) Analysis of the Bacillus subtilis tyrS gene: conservation of a regulatory sequence in multiple tRNA synthetase genes. J Bacteriol 174:1299–1306

    PubMed  CAS  Google Scholar 

  • Huang HY, Tang HL, Chao HY, Yeh LS, Wang CC (2006) An unusual pattern of protein expression and localization of yeast alanyl-tRNA synthetase isoforms. Mol Microbiol 60:189–198

    PubMed  CAS  Google Scholar 

  • Hughes TR, Marton MJ, Jones AR, Roberts CJ, Stoughton R, Armour CD, Bennett HA, Coffey E, Dai H, He YD, Kidd MJ, King AM, Meyer MR, Slade D, Lum PY, Stepaniants SB, Shoemaker DD, Gachotte D, Chakraburtty K, Simon J, Bard M, Friend SH (2000) Functional discovery via a compendium of expression profiles. Cell 102:109–126

    PubMed  CAS  Google Scholar 

  • Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, Anupama A, Apostolou Z, Attipoe P, Bason N, Bauser C, Beck A, Beverley SM, Bianchettin G, Borzym K, Bothe G, Bruschi CV, Collins M, Cadag E, Ciarloni L, Clayton C, Coulson RM, Cronin A, Cruz AK, Davies RM, De Gaudenzi J, Dobson DE, Duesterhoeft A, Fazelina G, Fosker N, Frasch AC, Fraser A, Fuchs M, Gabel C, Goble A, Goffeau A, Harris D, Hertz-Fowler C, Hilbert H, Horn D, Huang Y, Klages S, Knights A, Kube M, Larke N, Litvin L, Lord A, Louie T, Marra M, Masuy D, Matthews K, Michaeli S, Mottram JC, Muller-Auer S, Munden H, Nelson S, Norbertczak H, Oliver K, O’Neil S, Pentony M, Pohl TM, Price C, Purnelle B, Quail MA, Rabbinowitsch E, Reinhardt R, Rieger M, Rinta J, Robben J, Robertson L, Ruiz JC, Rutter S, Saunders D, Schafer M, Schein J, Schwartz DC, Seeger K, Seyler A, Sharp S, Shin H, Sivam D, Squares R, Squares S, Tosato V, Vogt C, Volckaert G, Wambutt R, Warren T, Wedler H, Woodward J, Zhou S, Zimmermann W, Smith DF, Blackwell JM, Stuart KD, Barrell B, Myler PJ (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309:436–442

    PubMed  Google Scholar 

  • Jarvis P, Robinson C (2004) Mechanisms of protein import and routing in chloroplasts. Curr Biol 14:R1064–1077

    PubMed  CAS  Google Scholar 

  • Kamenski P, Kolesnikova O, Jubenot V, Entelis N, Krasheninnikov IA, Martin RP, Tarassov I (2007) Evidence for an adaptation mechanism of mitochondrial translation via tRNA import from the cytosol. Mol Cell 26:625–637

    PubMed  CAS  Google Scholar 

  • Kaneko T, Suzuki T, Kapushoc ST, Rubio MA, Ghazvini J, Watanabe K, Simpson L (2003) Wobble modification differences and subcellular localization of tRNAs in Leishmania tarentolae: implication for tRNA sorting mechanism. EMBO J 22:657–667

    PubMed  CAS  Google Scholar 

  • Kapushoc ST, Alfonzo JD, Simpson L (2002) Differential localization of nuclear-encoded tRNAs between the cytosol and mitochondrion in Leishmania tarentolae. RNA 8:57–68

    PubMed  CAS  Google Scholar 

  • Kapushoc ST, Alfonzo JD, Rubio MA, Simpson L (2000) End processing precedes mitochondrial importation and editing of tRNAs in Leishmania tarentolae. J Biol Chem 275:37907–37914

    PubMed  CAS  Google Scholar 

  • Kolesnikova OA, Entelis NS, Jacquin-Becker C, Goltzene F, Chrzanowska-Lightowlers ZM, Lightowlers RN, Martin RP, Tarassov I (2004) Nuclear DNA-encoded tRNAs targeted into mitochondria can rescue a mitochondrial DNA mutation associated with the MERRF syndrome in cultured human cells. Hum Mol Genet 13:2519–2534

    PubMed  CAS  Google Scholar 

  • Kumar R, Maréchal-Drouard L, Akama K, Small I (1996) Striking differences in mitochondrial tRNA import between different plant species. Mol Gen Genet 252:404–411

    Article  PubMed  CAS  Google Scholar 

  • Kumazawa Y, Himeno H, K–I M, Watanae K (1991) Unilateral aminoacylation specificity beteen bovine mitochondria and eubacteria. J Biochem 109:421–427

    PubMed  CAS  Google Scholar 

  • Laforest MJ, Delage L, Maréchal-Drouard L (2005) The T-domain of cytosolic tRNAVal, an essential determinant for mitochondrial import. FEBS Lett 579:1072–1078

    PubMed  CAS  Google Scholar 

  • Leveque F, Gazeau M, Fromant M, Blanquet S, Plateau P (1991) Control of Escherichia coli lysyl-tRNA synthetase expression by anaerobiosis. J Bacteriol 173:7903–7910

    PubMed  CAS  Google Scholar 

  • Lohse M, Drechsel O, Bock R (2007) OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 52:267–274

    PubMed  CAS  Google Scholar 

  • Macasev D, Newbigin E, Whelan J, Lithgow T (2000) How do plant mitochondria avoid importing chloroplast proteins? Components of the import apparatus Tom20 and Tom22 from Arabidopsis differ from their fungal counterparts. Plant Physiol 123:811–816

    PubMed  CAS  Google Scholar 

  • Mahapatra S, Adhya S (1996) Import of RNA into Leishmania mitochondria occurs through direct interaction with membrane-bound receptors. J Biol Chem 271:20432–20437

    PubMed  CAS  Google Scholar 

  • Mahapatra S, Ghosh S, Bera SK, Ghosh T, Das A, Adhya S (1998) The D arm of tRNATyr is necessary and sufficient for import into Leishmania mitochondria in vitro. Nucleic Acids Res 26:2037–2041

    PubMed  CAS  Google Scholar 

  • Mahata B, Mukherjee S, Mishra S, Bandyopadhyay A, Adhya S (2006) Functional delivery of a cytosolic tRNA into mutant mitochondria of human cells. Science 314:471–474

    PubMed  CAS  Google Scholar 

  • Maréchal-Drouard L, Guillemaut P, Cosset A, Arbogast M, Weber F, Weil JH, Dietrich A (1990) Transfer RNAs of potato (Solanum tuberosum) mitochondria have different genetic origins. Nucleic Acids Res 18:3689–3696

    PubMed  Google Scholar 

  • Maréchal-Drouard L, Weil JH, Dietrich A (1993) Transfer RNAs and transfer RNA genes in plants. Annu Rev Plant Physiol 44:13–32

    Google Scholar 

  • Margeot A, Garcia M, Wang W, Tetaud E, di Rago JP, Jacq C (2005) Why are many mRNAs translated to the vicinity of mitochondria: a role in protein complex assembly? Gene 354:64–71

    PubMed  CAS  Google Scholar 

  • Menand B, Maréchal-Drouard L, Sakamoto W, Dietrich A, Wintz H (1998) A single gene of chloroplast origin codes for mitochondrial and chloroplastic methionyl-tRNA synthetase in Arabidopsis thaliana. Proc Natl Acad Sci USA 95:11014–11019

    PubMed  CAS  Google Scholar 

  • Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250

    PubMed  CAS  Google Scholar 

  • Mirande M (2007) The ins and outs of tRNA transport. EMBO Rep 8:547–549

    PubMed  CAS  Google Scholar 

  • Mireau H, Lancelin D, Small I (1996) The same Arabidopsis gene encodes both cytosolic and mitochondrial Alanyl-tRNA synthetases. Plant Cell 8:1027–1039

    PubMed  CAS  Google Scholar 

  • Mudge S, Williams J, Sutherland G, Cowan P, Power D (1998) Complex organisation of the 5′-end of the human glycine tRNA synthetase gene. Gene 209:45–50

    PubMed  CAS  Google Scholar 

  • Mukherjee S, Bhattacharyya SN, Adhya S (1999) Stepwise transfer of tRNA through the double membrane of Leishmania mitochondria. J Biol Chem 274:31249–31255

    PubMed  CAS  Google Scholar 

  • Mukherjee S, Basu S, Home P, Dhar G, Adhya S (2007) Necessary and sufficient factors for the import of transfer RNA into the kinetoplast mitochondrion. EMBO Rep 8:589–595

    PubMed  CAS  Google Scholar 

  • Mulero JJ, Rosenthal JK, Fox TD (1994) PET112, a Saccharomyces cerevisiae nuclear gene required to maintain rho+mitochondrial DNA. Curr Genet 25:299–304

    PubMed  CAS  Google Scholar 

  • Nabholz C, Hauser R, Schneider A (1997) Leishmania tarentolae contains distinct cytosolic and mitochondrial glutaminyl-tRNA synthetase activities. Proc Natl Acad Sci USA 94:7903–7908

    PubMed  CAS  Google Scholar 

  • Nabholz CE, Horn EK, Schneider A (1999) tRNAs and proteins are imported into mitochondria of Trypanosoma brucei by two distinct mechanisms. Mol Biol Cell 10:2547–2557

    PubMed  CAS  Google Scholar 

  • Natsoulis G, Hilger F, Fink G (1986) The HTS1 gene encodes both the cytoplasmic and mitochondrial histidine-tRNA synthetases of S. cerevisae. Cell 46:235–243

    Google Scholar 

  • Neupert W, Herrmann JM (2007) Translocation of proteins into mitochondria. Annu Rev Biochem 76:723–749

    PubMed  CAS  Google Scholar 

  • Peeters NM, Chapron A, Giritch A, Grandjean O, Lancelin D, Lhomme T, Vivrel A, Small I (2000) Duplication and quadruplication of Arabidopsis thaliana cysteinyl- and asparaginyl-tRNA synthetase genes of organellar origin. J Mol Evol 50:413–423

    PubMed  CAS  Google Scholar 

  • Perry AJ, Hulett JM, Likic VA, Lithgow T, Gooley PR (2006) Convergent evolution of receptors for protein import into mitochondria. Curr Biol 16:221–229

    PubMed  CAS  Google Scholar 

  • Pujol C, Maréchal-Drouard L, Duchêne AM (2007) How can organellar protein N-terminal sequences be dual targeting signals? In silico analysis and mutagenesis approach. J Mol Biol 369:356–367

    PubMed  CAS  Google Scholar 

  • Pujol C, Bailly M, Kern D, Maréchal-Drouard L, Becker H, Duchêne AM (2008) Dual-targeted tRNA-dependent amidotransferase ensures both mitochondrial and chloroplastic Gln-tRNAGln synthesis in plants. Proc Natl Acad Sci USA 105:6481–6485

    PubMed  CAS  Google Scholar 

  • Putz J, Dupuis B, Sissler M, Florentz C (2007) Mamit-tRNA, a database of mammalian mitochondrial tRNA primary and secondary structures. RNA 13:1184–1190

    PubMed  CAS  Google Scholar 

  • Randau L, Soll D (2008) Transfer RNA genes in pieces. EMBO Rep 9:623–628

    PubMed  CAS  Google Scholar 

  • Rinehart J, Horn EK, Wei D, Soll D, Schneider A (2004) Non-canonical eukaryotic glutaminyl- and glutamyl-tRNA synthetases form mitochondrial aminoacyl-tRNA in Trypanosoma brucei. J Biol Chem 279:1161–1166

    PubMed  CAS  Google Scholar 

  • Rinehart J, Krett B, Rubio MA, Alfonzo JD, Soll D (2005) Saccharomyces cerevisiae imports the cytosolic pathway for Gln-tRNA synthesis into the mitochondrion. Genes Dev 19:583–592

    PubMed  CAS  Google Scholar 

  • Rokov-Plavec J, Dulic M, Duchêne AM, Weygand-Durasevic I (2008) Dual targeting of organellar seryl-tRNA synthetase to maize mitochondria and chloroplasts. Plant Cell Rep 27:1157–1168

    PubMed  CAS  Google Scholar 

  • Rubio MA, Liu X, Yuzawa H, Alfonzo JD, Simpson L (2000) Selective importation of RNA into isolated mitochondria from Leishmania tarentolae. RNA 6:988–1003

    PubMed  CAS  Google Scholar 

  • Rubio MA, Rinehart JJ, Krett B, Duvezin-Caubet S, Reichert AS, Soll D, Alfonzo JD (2008) Mammalian mitochondria have the innate ability to import tRNAs by a mechanism distinct from protein import. Proc Natl Acad Sci USA 105:9186–9191

    PubMed  CAS  Google Scholar 

  • Rusconi CP, Cech TR (1996) The anticodon is the signal sequence for mitochondrial import of glutamine tRNA in Tetrahymena. Genes Dev 10:2870–2880

    PubMed  CAS  Google Scholar 

  • Salinas T, Schaeffer C, Maréchal-Drouard L, Duchêne AM (2005) Sequence dependence of tRNA(Gly) import into tobacco mitochondria. Biochimie 87:863–872

    PubMed  CAS  Google Scholar 

  • Salinas T, Duchêne AM, Delage L, Nilsson S, Glaser E, Zaepfel M, Maréchal-Drouard L (2006) The voltage-dependent anion channel, a major component of the tRNA import machinery in plant mitochondria. Proc Natl Acad Sci USA 103:18362–18367

    PubMed  CAS  Google Scholar 

  • Salinas T, Duchêne AM, Maréchal-Drouard L (2008) Recent advances in tRNA mitochondrial import. Trends Biochem Sci 33:320–329

    PubMed  CAS  Google Scholar 

  • Scheper GC, van der Klok T, van Andel RJ, van Berkel CG, Sissler M, Smet J, Muravina TI, Serkov SV, Uziel G, Bugiani M, Schiffmann R, Krageloh-Mann I, Smeitink JA, Florentz C, Van Coster R, Pronk JC, van der Knaap MS (2007) Mitochondrial aspartyl-tRNA synthetase deficiency causes leukoencephalopathy with brain stem and spinal cord involvement and lactate elevation. Nat Genet 39:534–539

    PubMed  CAS  Google Scholar 

  • Schneider A (2001) Does the evolutionary history of aminoacyl-tRNA synthetases explain the loss of mitochondrial tRNA genes? Trends Genet 17:557–559

    PubMed  CAS  Google Scholar 

  • Schneider A, Maréchal-Drouard L (2000) Mitochondrial tRNA import: are there distinct mechanisms? Trends Cell Biol 10:509–513

    PubMed  CAS  Google Scholar 

  • Schneider A, Bursac D, Lithgow T (2007) The direct route: a simplified pathway for protein import into the mitochondrion of trypanosomes. Trends Cell Biol 18:12–18

    Google Scholar 

  • Sherrer RL, Yermovsky-Kammerer AE, Hajduk SL (2003) A sequence motif within trypanosome precursor tRNAs influences abundance and mitochondrial localization. Mol Cell Biol 23:9061–9072

    PubMed  CAS  Google Scholar 

  • Sjoling S, Glaser E (1998) Mitochondrial targeting peptides in plants. Trends Plant Sci 3:136–140

    Google Scholar 

  • Smirnov A, Tarassov I, Mager-Heckel AM, Letzelter M, Martin RP, Krasheninnikov IA, Entelis N (2008) Two distinct structural elements of 5S rRNA are needed for its import into human mitochondria. RNA 14:749–759

    PubMed  CAS  Google Scholar 

  • Souciet G, Menand B, Ovesna L, Cosset A, Dietrich A, Wintz H (1999) Characterization of two bifunctional Arabdopsis thaliana genes coding for mitochondrial and cytosolic forms of valyl-tRNA synthetase and threonyl-tRNA synthetase by alternative use of two in-frame AUGs. Eur J Biochem 266:848–854

    PubMed  CAS  Google Scholar 

  • Steinberg S, Cedergren R (1994) Structural compensation in atypical mitochondrial tRNAs. Nat Struct Biol 1:507–510

    PubMed  CAS  Google Scholar 

  • Suyama Y (1967) The origins of mitochondrial ribonucleic acids in Tetrahymena pyriformis. Biochemistry 6:2829–2839

    PubMed  CAS  Google Scholar 

  • Suyama Y (1986) Two dimensional polyacrylamide gel electrophoresis analysis of Tetrahymena mitochondrial tRNA. Curr Genet 10:411–420

    PubMed  CAS  Google Scholar 

  • Suyama Y, Wong S, Campbell DA (1998) Regulated tRNA import in Leishmania mitochondria. Biochim Biophys Acta 1396:138–142

    PubMed  CAS  Google Scholar 

  • Tan TH, Pach R, Crausaz A, Ivens A, Schneider A (2002a) tRNAs in Trypanosoma brucei: genomic organization, expression, and mitochondrial import. Mol Cell Biol 22:3707–3717

    PubMed  CAS  Google Scholar 

  • Tan THP, Bochud-Allemann N, Schneider A (2002b) Eukaryotic-type elongator tRNAMet of Trypanosoma brucei becomes formylated after import into mitochondria. Proc Natl Acad Sci USA 99:1152–1157

    PubMed  CAS  Google Scholar 

  • Tarassov I, Entelis N, Martin RP (1995a) An intact protein translocating machinery is required for mitochondrial import of a yeast cytoplasmic tRNA. J Mol Biol 245:315–323

    PubMed  CAS  Google Scholar 

  • Tarassov I, Entelis N, Martin RP (1995b) Mitochondrial import of a cytoplasmic lysine-tRNA in yeast is mediated by cooperation of cytoplasmic and mitochondrial lysyl-tRNA synthetases. EMBO J 14:3461–3471

    PubMed  CAS  Google Scholar 

  • Tarassov I, Kamenski P, Kolesnikova O, Karicheva O, Martin RP, Krasheninnikov IA, Entelis N (2007) Import of nuclear DNA-encoded RNAs into mitochondria and mitochondrial translation. Cell Cycle 6:2473–2477

    PubMed  CAS  Google Scholar 

  • Taylor RW, Turnbull DM (2005) Mitochondrial DNA mutations in human disease. Nat Rev Genet 6:389–402

    PubMed  CAS  Google Scholar 

  • Tolkunova E, Park H, Xia J, King MP, Davidson E (2000) The human lysyl-tRNA synthetase gene encodes both the cytoplasmic and mitochondrial enzymes by means of an unusual alternative splicing of the primary transcript. J Biol Chem 275:35063–35069

    PubMed  CAS  Google Scholar 

  • Turner RJ, Lovato M, Schimmel P (2000) One of two genes encoding glycyl-tRNA synthetase in Saccharomyces cerevisiae provides mitochondrial and cytoplasmic functions. J Biol Chem 275:27681–27688

    PubMed  CAS  Google Scholar 

  • Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366, 924 nucleotides. Nat Genet 15:57–61

    PubMed  CAS  Google Scholar 

  • Uwer U, Willmitzer L, Altmann T (1998) Inactivation of a glycyl-tRNA synthetase leads to an arrest in plant embryo development. Plant Cell 10:1277–1294

    PubMed  CAS  Google Scholar 

  • Woese CR, Olsen GJ, Ibba M, Soll D (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol Mol Biol Rev 64:202–236

    PubMed  CAS  Google Scholar 

  • Wolfe KH, Morden CW, Palmer JD (1992) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89:10648–10652

    PubMed  CAS  Google Scholar 

  • Yermovsky-Kammerer AE, Hajduk SL (1999) In vitro import of a nuclearly encoded tRNA into the mitochondrion of Trypanosoma brucei. Mol Cell Biol 19:6253–6259

    PubMed  CAS  Google Scholar 

  • Zhang XP, Glaser E (2002) Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci 7:14–21

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institut de Biologie Moléculaire des Plantes, Unité Propre de Recherche du CNRS, Associated with Louis Pasteur University, 12 rue du Général Zimmer, 67084, Strasbourg Cedex, France

    Anne-Marie Duchêne, Claire Pujol & Laurence Maréchal-Drouard

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  1. Anne-Marie Duchêne
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  2. Claire Pujol
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  3. Laurence Maréchal-Drouard
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Correspondence to Anne-Marie Duchêne or Laurence Maréchal-Drouard.

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Communicated by R. Bock.

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Duchêne, AM., Pujol, C. & Maréchal-Drouard, L. Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet 55, 1–18 (2009). https://doi.org/10.1007/s00294-008-0223-9

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  • DOI: https://doi.org/10.1007/s00294-008-0223-9

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