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Modifications and Innovations in the Evolution of Mitochondrial Protein Import Pathways

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Endosymbiosis

Abstract

Eukaryotic cells are defined by their mitochondria, organelles that were derived through endosymbiosis. The development of this organelle from a bacterial endosymbiont required establishment of effective protein import pathways so that much of the genetic capacity of the bacterium could be relocated to the host cell. Two realms of study have delivered insight into the early evolution of these mitochondrial pathways: (1) considering the “starting material” based on what can be observed of protein trafficking pathways in extant species of bacteria and (2) analysing the protein import pathways of parasites whose mitochondria have undergone secondary reduction and now offer insight into minimal functional pathways. These approaches have illuminated what components of bacterial trafficking pathways were co-opted in the developing mitochondrion and what further innovations occurred within the eukaryote host. Now comparative analysis of model mitochondrial systems, with organelles found in a broad diversity of eukaryotes (namely protists), shows when in eukaryotic radiation these major innovations took place and what lineage-specific changes have since occurred to mitochondrial import systems in eukaryotes.

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Notes

  1. 1.

    Note added in proof: The assembly of Rip1 was recently investigated and found to depend on the AAA-ATPase Bcs1 (Wagener et al. 2011). This raises the intriguing possibility that the Tat pathway has been replaced by a functionally homologous system that translocates the folded Fe–S containing domain, but uses an entirely different protein3 machinery to do so.

References

  • Alcock FH, Grossmann JG, Gentle IE, Likic VA, Lithgow T, Tokatlidis K (2008) Conserved substrate binding by chaperones in the bacterial periplasm and the mitochondrial intermembrane space. Biochem J 409:377–387

    Article  PubMed  CAS  Google Scholar 

  • Alcock F, Clements A, Webb C, Lithgow T (2010) Tinkering inside the organelle. Science 327:649–650

    Article  PubMed  CAS  Google Scholar 

  • Alcock F, Webb CT, Dolezal P, Hewitt V, Shingu-Vasquez M, Likic VA, Traven A, Lithgow T (2012) A small Tim homohexamer in the relict mitochondrion of Cryptosporidium. Mol Biol Evol 29:113–122

    Article  PubMed  CAS  Google Scholar 

  • Alder NN, Jensen RE, Johnson AE (2008) Fluorescence mapping of mitochondrial TIM23 complex reveals a water-facing, substrate-interacting helix surface. Cell 134:439–450

    Article  PubMed  CAS  Google Scholar 

  • Andersson SG, Kurland CG (1999) Origins of mitochondria and hydrogenosomes. Curr Opin Microbiol 2:535–541

    Article  PubMed  CAS  Google Scholar 

  • Bains G, Lithgow T (1999) The Tom channel in the mitochondrial outer membrane: alive and kicking. Bioessays 21:1–4

    Article  PubMed  CAS  Google Scholar 

  • Becker T, Pfannschmidt S, Guiard B, Stojanovski D, Milenkovic D, Kutik S, Pfanner N, Meisinger C, Wiedemann N (2008) Biogenesis of the mitochondrial TOM complex: Mim1 promotes insertion and assembly of signal-anchored receptors. J Biol Chem 283:120–127

    Article  PubMed  CAS  Google Scholar 

  • Becker T, Wenz L-S, Krüger V, Lehmann W, Müller JM, Goroncy L, Zufall N, Lithgow T, Guiard B, Chacinska A, Wagner R, Meisinger C, Pfanner N (2011) The mitochondrial import protein Mim1 promotes biogenesis of multispanning outer membrane proteins. J Cell Biol 194:387–395

    Article  PubMed  CAS  Google Scholar 

  • Berks BC, Palmer T, Sargent F (2005) Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol 8:174–181

    Article  PubMed  CAS  Google Scholar 

  • Bogsch EG, Sargent F, Stanley NR, Berks BC, Robinson C, Palmer T (1998) An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J Biol Chem 273:18003–18006

    Article  PubMed  CAS  Google Scholar 

  • Boorstein WR, Ziegelhoffer T, Craig EA (1994) Molecular evolution of the HSP70 multigene family. J Mol Evol 38:1–17

    Article  PubMed  CAS  Google Scholar 

  • Burger G, Forget L, Zhu Y, Gray MW, Lang BF (2003) Unique mitochondrial genome architecture in unicellular relatives of animals. Proc Natl Acad Sci USA 100:892–897

    Article  PubMed  CAS  Google Scholar 

  • Burri L, Williams BA, Bursac D, Lithgow T, Keeling PJ (2006) Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc Natl Acad Sci USA 103:15916–15920

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354

    PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2006) Rooting the tree of life by transition analyses. Biol Direct 1:19

    Article  PubMed  Google Scholar 

  • Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138:628–644

    Article  PubMed  CAS  Google Scholar 

  • Chan NC, Likic VA, Waller RF, Mulhern TD, Lithgow T (2006) The C-terminal TPR domain of Tom70 defines a family of mitochondrial protein import receptors found only in animals and fungi. J Mol Biol 358:1010–1022

    Article  PubMed  CAS  Google Scholar 

  • Chew O, Lister R, Qbadou S, Heazlewood JL, Soll J, Schleiff E, Millar AH, Whelan J (2004) A plant outer mitochondrial membrane protein with high amino acid sequence identity to a chloroplast protein import receptor. FEBS Lett 557:109–114

    Article  PubMed  CAS  Google Scholar 

  • Clements A, Bursac D, Gatsos X, Perry AJ, Civciristov S, Celik N, Likic VA, Poggio S, Jacobs-Wagner C, Strugnell RA, Lithgow T (2009) The reducible complexity of a mitochondrial molecular machine. Proc Natl Acad Sci USA 106:15791–15795

    Article  PubMed  CAS  Google Scholar 

  • Conte L, Zara V (2011) The rieske iron-sulfur protein: import and assembly into the cytochrome bc(1) complex of yeast mitochondria. Bioinorg Chem Appl 2011:363941

    Article  PubMed  Google Scholar 

  • D’Silva PD, Schilke B, Walter W, Andrew A, Craig EA (2003) J protein cochaperone of the mitochondrial inner membrane required for protein import into the mitochondrial matrix. Proc Natl Acad Sci USA 100:13839–13844

    Article  PubMed  Google Scholar 

  • Dagley MJ, Dolezal P, Likic VA, Smid O, Purcell AW, Buchanan SK, Tachezy J, Lithgow T (2009) The protein import channel in the outer mitosomal membrane of Giardia intestinalis. Mol Biol Evol 26:1941–1947

    Article  PubMed  CAS  Google Scholar 

  • Danne JC, Waller RF (2011) Analysis of dinoflagellate mitochondrial protein sorting signals indicates a highly stable protein targeting system across eukaryotic diversity. J Mol Biol 408:643–653

    Article  PubMed  CAS  Google Scholar 

  • de Duve C (2007) The origin of eukaryotes: a reappraisal. Nat Rev Genet 8:395–403

    Article  PubMed  Google Scholar 

  • Dolezal P, Likic V, Tachezy J, Lithgow T (2006) Evolution of the molecular machines for protein import into mitochondria. Science 313:314–318

    Article  PubMed  CAS  Google Scholar 

  • Driessen AJ, Manting EH, van der Does C (2001) The structural basis of protein targeting and translocation in bacteria. Nat Struct Biol 8:492–498

    Article  PubMed  CAS  Google Scholar 

  • Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630

    Article  PubMed  CAS  Google Scholar 

  • Funes S, Hasona A, Bauerschmitt H, Grubbauer C, Kauff F, Collins R, Crowley PJ, Palmer SR, Brady LJ, Herrmann JM (2009) Independent gene duplications of the YidC/Oxa/Alb3 family enabled a specialized cotranslational function. Proc Natl Acad Sci USA 106:6656–6661

    Article  PubMed  CAS  Google Scholar 

  • Gabaldon T, Huynen MA (2007) From endosymbiont to host-controlled organelle: the hijacking of mitochondrial protein synthesis and metabolism. PLoS Comput Biol 3:e219

    Article  PubMed  Google Scholar 

  • Gabriel K, Buchanan SK, Lithgow T (2001) The alpha and the beta: protein translocation across mitochondrial and plastid outer membranes. Trends Biochem Sci 26:36–40

    Article  PubMed  CAS  Google Scholar 

  • Gatsos X, Perry AJ, Anwari K, Dolezal P, Wolynec PP, Likic VA, Purcell AW, Buchanan SK, Lithgow T (2008) Protein secretion and outer membrane assembly in Alphaproteobacteria. FEMS Microbiol Rev 32:995–1009

    Article  PubMed  CAS  Google Scholar 

  • Gentle I, Gabriel K, Beech P, Waller R, Lithgow T (2004) The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164:19–24

    Article  PubMed  CAS  Google Scholar 

  • Gentle IE, Burri L, Lithgow T (2005) Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58:1216–1225

    Article  PubMed  CAS  Google Scholar 

  • Gentle IE, Perry AJ, Alcock FH, Likic VA, Dolezal P, Ng ET, Purcell AW, McConnville M, Naderer T, Chanez AL, Charriere F, Aschinger C, Schneider A, Tokatlidis K, Lithgow T (2007) Conserved motifs reveal details of ancestry and structure in the small TIM chaperones of the mitochondrial intermembrane space. Mol Biol Evol 24:1149–1160

    Article  PubMed  CAS  Google Scholar 

  • Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481

    Article  PubMed  CAS  Google Scholar 

  • Gray MW, Burger G, Lang BF (2001) The origin and early evolution of mitochondria. Genome Biol 2:Reviews1018

    Google Scholar 

  • Gray MW, Lang BF, Burger G (2004) Mitochondria of protists. Annu Rev Genet 38:477–524

    Article  PubMed  CAS  Google Scholar 

  • Gross J, Bhattacharya D (2009) Mitochondrial and plastid evolution in eukaryotes: an outsiders’ perspective. Nat Rev Genet 10:495–505

    Article  PubMed  CAS  Google Scholar 

  • Herrmann JM (2003) Converting bacteria to organelles: evolution of mitochondrial protein sorting. Trends Microbiol 11:74–79

    Article  PubMed  CAS  Google Scholar 

  • Hewitt V, Alcock F, Lithgow T (2011) Minor modifications and major adaptations: the evolution of molecular machines driving mitochondrial protein import. Biochim Biophys Acta 1808:947–954

    Article  PubMed  CAS  Google Scholar 

  • Hoppins SC, Nargang FE (2004) The Tim8-Tim13 complex of Neurospora crassa functions in the assembly of proteins into both mitochondrial membranes. J Biol Chem 279:12396–12405

    Article  PubMed  CAS  Google Scholar 

  • Hulett JM, Walsh P, Lithgow T (2007) Domain stealing by receptors in a protein transport complex. Mol Biol Evol 24:1909–1911

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa D, Yamamoto H, Tamura Y, Moritoh K, Endo T (2004) Two novel proteins in the mitochondrial outer membrane mediate beta-barrel protein assembly. J Cell Biol 166:621–627

    Article  PubMed  CAS  Google Scholar 

  • Jarosch E, Tuller G, Daum G, Waldherr M, Voskova A, Schweyen RJ (1996) Mrs5p, an essential protein of the mitochondrial intermembrane space, affects protein import into yeast mitochondria. J Biol Chem 271:17219–17225

    Article  PubMed  CAS  Google Scholar 

  • Jensen RE, Dunn CD (2002) Protein import into and across the mitochondrial inner membrane: role of the TIM23 and TIM22 translocons. Biochim Biophys Acta 1592:25–34

    Article  PubMed  CAS  Google Scholar 

  • Kiefer D, Kuhn A (2007) YidC as an essential and multifunctional component in membrane protein assembly. Int Rev Cytol 259:113–138

    Article  PubMed  CAS  Google Scholar 

  • Knowles TJ, Scott-Tucker A, Overduin M, Henderson IR (2009) Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat Rev Microbiol 7:206–214

    Article  PubMed  CAS  Google Scholar 

  • Koehler CM, Jarosch E, Tokatlidis K, Schmid K, Schweyen RJ, Schatz G (1998a) Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science 279:369–373

    Article  PubMed  CAS  Google Scholar 

  • Koehler CM, Merchant S, Oppliger W, Schmid K, Jarosch E, Dolfini L, Junne T, Schatz G, Tokatlidis K (1998b) Tim9p, an essential partner subunit of Tim10p for the import of mitochondrial carrier proteins. EMBO J 17:6477–6486

    Article  PubMed  CAS  Google Scholar 

  • Kutik S, Stroud DA, Wiedemann N, Pfanner N (2009) Evolution of mitochondrial protein biogenesis. Biochim Biophys Acta 1790:409–415

    Article  PubMed  CAS  Google Scholar 

  • Lang BF, Burger G, O'Kelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW (1997) An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387:493–497

    Article  PubMed  CAS  Google Scholar 

  • Lang BF, Gray MW, Burger G (1999) Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet 33:351–397

    Article  PubMed  CAS  Google Scholar 

  • Likic VA, Dolezal P, Celik N, Dagley M, Lithgow T (2010) Using hidden Markov models to discover new protein transport machines. Methods Mol Biol 619:271–284

    Article  PubMed  CAS  Google Scholar 

  • Lister R, Murcha MW, Whelan J (2003) The mitochondrial protein import machinery of plants (MPIMP) database. Nucleic Acids Res 31:325–327

    Article  PubMed  CAS  Google Scholar 

  • Lithgow T, Schneider A (2010) Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos Trans R Soc Lond B Biol Sci 365:799–817

    Article  PubMed  CAS  Google Scholar 

  • Lucattini R, Likic VA, Lithgow T (2004) Bacterial proteins predisposed for targeting to mitochondria. Mol Biol Evol 21:652–658

    Article  PubMed  CAS  Google Scholar 

  • Lueder F, Lithgow T (2009) The three domains of the mitochondrial outer membrane protein Mim1 have discrete functions in assembly of the TOM complex. FEBS Lett 583:1475–1480

    Article  PubMed  CAS  Google Scholar 

  • Macasev D, Whelan J, Newbigin E, Silva-Filho MC, Mulhern TD, Lithgow T (2004) Tom22', an 8-kDa trans-site receptor in plants and protozoans, is a conserved feature of the TOM complex that appeared early in the evolution of eukaryotes. Mol Biol Evol 21:1557–1564

    Article  PubMed  CAS  Google Scholar 

  • Mannella CA, Neuwald AF, Lawrence CE (1996) Detection of likely transmembrane beta strand regions in sequences of mitochondrial pore proteins using the Gibbs sampler. J Bioenerg Biomembr 28:163–169

    Article  PubMed  CAS  Google Scholar 

  • Mayer A, Neupert W, Lill R (1995) Mitochondrial protein import: reversible binding of the presequence at the trans side of the outer membrane drives partial translocation and unfolding. Cell 80:127–137

    Article  PubMed  CAS  Google Scholar 

  • Meisinger C, Rissler M, Chacinska A, Szklarz LK, Milenkovic D, Kozjak V, Schonfisch B, Lohaus C, Meyer HE, Yaffe MP, Guiard B, Wiedemann N, Pfanner N (2004) The mitochondrial morphology protein Mdm10 functions in assembly of the preprotein translocase of the outer membrane. Dev Cell 7:61–71

    Article  PubMed  CAS  Google Scholar 

  • Mokranjac D, Sichting M, Neupert W, Hell K (2003) Tim14, a novel key component of the import motor of the TIM23 protein translocase of mitochondria. EMBO J 22:4945–4956

    Article  PubMed  CAS  Google Scholar 

  • Molik S, Karnauchov I, Weidlich C, Herrmann RG, Klosgen RB (2001) The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J Biol Chem 276:42761–42766

    Article  PubMed  CAS  Google Scholar 

  • Müller M, Klösgen RB (2005) The Tat pathway in bacteria and chloroplasts (review). Mol Membr Biol 22:113–121

    Article  PubMed  Google Scholar 

  • Murcha MW, Elhafez D, Lister R, Tonti-Filippini J, Baumgartner M, Philippar K, Carrie C, Mokranjac D, Soll J, Whelan J (2007) Characterization of the preprotein and amino acid transporter gene family in Arabidopsis. Plant Physiol 143:199–212

    Article  PubMed  CAS  Google Scholar 

  • Natale P, Bruser T, Driessen AJ (2008) Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane – distinct translocases and mechanisms. Biochim Biophys Acta 1778:1735–1756

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ott M, Herrmann JM (2010) Co-translational membrane insertion of mitochondrially encoded proteins. Biochim Biophys Acta 1803:767–775

    Article  PubMed  CAS  Google Scholar 

  • Perry AJ, Rimmer KA, Mertens HD, Waller RF, Mulhern TD, Lithgow T, Gooley PR (2008) Structure, topology and function of the translocase of the outer membrane of mitochondria. Plant Physiol Biochem 46:265–274

    Article  PubMed  CAS  Google Scholar 

  • Pohlschroder M, Gimenez MI, Jarrell KF (2005) Protein transport in Archaea: Sec and twin arginine translocation pathways. Curr Opin Microbiol 8:713–719

    Article  PubMed  Google Scholar 

  • Pusnik M, Charriere F, Maser P, Waller RF, Dagley MJ, Lithgow T, Schneider A (2009) The single mitochondrial porin of Trypanosoma brucei is the main metabolite transporter in the outer mitochondrial membrane. Mol Biol Evol 26:671–680

    Article  PubMed  CAS  Google Scholar 

  • Rassow J, Maarse AC, Krainer E, Kubrich M, Muller H, Meijer M, Craig EA, Pfanner N (1994) Mitochondrial protein import: biochemical and genetic evidence for interaction of matrix hsp70 and the inner membrane protein MIM44. J Cell Biol 127:1547–1556

    Article  PubMed  CAS  Google Scholar 

  • Rassow J, Dekker PJ, van Wilpe S, Meijer M, Soll J (1999) The preprotein translocase of the mitochondrial inner membrane: function and evolution. J Mol Biol 286:105–120

    Article  PubMed  CAS  Google Scholar 

  • Ruiz N, Kahne D, Silhavy TJ (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4:57–66

    Article  PubMed  Google Scholar 

  • Samuelson JC, Chen M, Jiang F, Moller I, Wiedmann M, Kuhn A, Phillips GJ, Dalbey RE (2000) YidC mediates membrane protein insertion in bacteria. Nature 406:637–641

    Article  PubMed  CAS  Google Scholar 

  • Schneider HC, Berthold J, Bauer MF, Dietmeier K, Guiard B, Brunner M, Neupert W (1994) Mitochondrial Hsp70/MIM44 complex facilitates protein import. Nature 371:768–774

    Article  PubMed  CAS  Google Scholar 

  • Schneider A, Bursac D, Lithgow T (2008) The direct route: a simplified pathway for protein import into the mitochondrion of trypanosomes. Trends Cell Biol 18:12–18

    Article  PubMed  CAS  Google Scholar 

  • Smith DG, Gawryluk RM, Spencer DF, Pearlman RE, Siu KW, Gray MW (2007) Exploring the mitochondrial proteome of the ciliate protozoon Tetrahymena thermophila: direct analysis by tandem mass spectrometry. J Mol Biol 374:837–863

    Article  PubMed  CAS  Google Scholar 

  • Stuart R (2002) Insertion of proteins into the inner membrane of mitochondria: the role of the Oxa1 complex. Biochim Biophys Acta 1592:79–87

    Article  PubMed  CAS  Google Scholar 

  • Thornton N, Stroud DA, Milenkovic D, Guiard B, Pfanner N, Becker T (2010) Two modular forms of the mitochondrial sorting and assembly machinery are involved in biogenesis of alpha-helical outer membrane proteins. J Mol Biol 396:540–549

    Article  PubMed  CAS  Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    Article  PubMed  CAS  Google Scholar 

  • Tong J, Dolezal P, Selkrig J, Crawford S, Simpson AG, Noinaj N, Buchanan SK, Gabriel K, Lithgow T (2011) Ancestral and derived protein import pathways in the mitochondrion of Reclinomonas americana. Mol Biol Evol 28:1581–1591

    Article  PubMed  CAS  Google Scholar 

  • Truscott KN, Kovermann P, Geissler A, Merlin A, Meijer M, Driessen AJ, Rassow J, Pfanner N, Wagner R (2001) A presequence- and voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23. Nat Struct Biol 8:1074–1082

    Article  PubMed  CAS  Google Scholar 

  • Truscott KN, Voos W, Frazier AE, Lind M, Li Y, Geissler A, Dudek J, Muller H, Sickmann A, Meyer HE, Meisinger C, Guiard B, Rehling P, Pfanner N (2003) A J-protein is an essential subunit of the presequence translocase-associated protein import motor of mitochondria. J Cell Biol 163:707–713

    Article  PubMed  CAS  Google Scholar 

  • Tsaousis AD, Gaston D, Stechmann A, Walker PB, Lithgow T, Roger AJ (2011) A functional Tom70 in the human parasite Blastocystis sp.: implications for the evolution of the mitochondrial import apparatus. Mol Biol Evol 28:781–791

    Article  PubMed  CAS  Google Scholar 

  • van der Laan M, Nouwen NP, Driessen AJ (2005) YidC – an evolutionary conserved device for the assembly of energy-transducing membrane protein complexes. Curr Opin Microbiol 8:182–187

    Article  PubMed  Google Scholar 

  • van Dooren GG, Stimmler LM, McFadden GI (2006) Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol Rev 30:596–630

    Article  PubMed  Google Scholar 

  • Wagener N, Ackermann M, Funes S, Neupert W (2011) A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol Cell 44:191–202

    Article  PubMed  CAS  Google Scholar 

  • Waller RF, Jabbour C, Chan NC, Celik N, Likic VA, Mulhern TD, Lithgow T (2009) Evidence of a reduced and modified mitochondrial protein import apparatus in microsporidian mitosomes. Eukaryot Cell 8:19–26

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Lavrov DV (2007) Mitochondrial genome of the homoscleromorph Oscarella carmela (Porifera, Demospongiae) reveals unexpected complexity in the common ancestor of sponges and other animals. Mol Biol Evol 24:363–373

    Article  PubMed  Google Scholar 

  • Wang X, Lavrov DV (2008) Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS One 3:e2723

    Article  PubMed  Google Scholar 

  • Webb CT, Lithgow T (2010) Mitochondrial biogenesis: sorting mechanisms cooperate in ABC transporter assembly. Curr Biol 20:R564–R567

    Article  PubMed  CAS  Google Scholar 

  • Wiedemann N, Truscott KN, Pfannschmidt S, Guiard B, Meisinger C, Pfanner N (2004) Biogenesis of the protein import channel Tom40 of the mitochondrial outer membrane: intermembrane space components are involved in an early stage of the assembly pathway. J Biol Chem 279:18188–18194

    Article  PubMed  CAS  Google Scholar 

  • Yen MR, Tseng YH, Nguyen EH, Wu LF, Saier MH Jr (2002) Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch Microbiol 177:441–450

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Trevor Lithgow or Ross F. Waller .

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Hewitt, V., Lithgow, T., Waller, R.F. (2014). Modifications and Innovations in the Evolution of Mitochondrial Protein Import Pathways. In: Löffelhardt, W. (eds) Endosymbiosis. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1303-5_2

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