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Arabidopsis thaliana Oxa proteins locate to mitochondria and fulfill essential roles during embryo development

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Abstract

Members of the Alb3/Oxa1/YidC protein family function as insertases in chloroplasts, mitochondria, and bacteria. Due to independent gene duplications, all organisms possess two isoforms, Oxa1 and Oxa2 except gram-negative bacteria, which encode only for one YidC-like protein. The genome of Arabidopsis thaliana however, encodes for eight different isoforms. The localization of three of these isoforms has been identified earlier: Alb3 and Alb4 located in thylakoid membranes of chloroplasts while AtOxa1 was found in the inner membrane of mitochondria. Here, we show that the second Oxa1 protein, Oxa1b as well as two Oxa2 proteins are also localized in mitochondria. The last two isoforms most likely encode truncated versions of Oxa-like proteins, which might be inoperable pseudogenes. Homozygous mutant lines were only obtained for Oxa1b, which did not reveal any significant phenotypes, while T-DNA insertion lines of Oxa1a, Oxa2a and Oxa2b resulted only in heterozygous plants indicating that these genes are indispensable for plant development. Phenotyping heterozygous lines showed that embryos are either retarded in growth, display an albino phenotype or embryo formation was entirely abolished suggesting that Oxa1a and both Oxa2 proteins function in embryo formation although at different developmental stages as indicated by the various phenotypes observed.

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Abbreviations

UTR:

Untranslated regions

Met:

Methionine

Val:

Valinomycin

IMS:

Intermembrane space

GFP:

Green fluorescence protein

References

  • Altamura N, Capitanio N, Bonnefoy N, Papa S, Dujardin G (1996) The Saccharomyces cerevisiae OXA1 gene is required for the correct assembly of cytochrome c oxidase and oligomycin-sensitive ATP synthase. FEBS Lett 382:111–115

    Article  PubMed  CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Bauer M, Behrens M, Esser K, Michaelis G, Pratje E (1994) PET1402, a nuclear gene required for proteolytic processing of cytochrome oxidase subunit 2 in yeast. Mol Gen Genet 245:272–278

    Article  PubMed  CAS  Google Scholar 

  • Benz M, Bals T, Gügel IL, Piotrowski M, Kuhn A, Schünemann D, Soll J, Ankele E (2009) Alb4 of Arabidopsis promotes assembly and stabilization of a non chlorophyll-binding photosynthetic complex, the CF1CF0-ATP synthase. Mol Plant 2:1410–1424

    Article  PubMed  CAS  Google Scholar 

  • Bonnefoy N, Chalvet F, Hamel P, Slonimski PP, Dujardin G (1994) OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis. J Mol Biol 239:201–212

    Article  PubMed  CAS  Google Scholar 

  • Bonnefoy N, Fiumera HL, Dujardin G, Fox TD (2009) Roles of Oxa1-related inner-membrane translocases in assembly of respiratory chain complexes. BBA 1793:60–70

    Article  PubMed  CAS  Google Scholar 

  • Carrie C, Murcha MW, Whelan J (2010) An in silico analysis of the mitochondrial protein import apparatus of plants. BMC Plant Biol 10:249 (open access)

    Google Scholar 

  • Chan NC, Likić 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 

  • Dalbey RE, Wang P, Kuhn A (2011) Assembly of bacterial inner membrane proteins. Annu Rev Biochem 7:161–187

    Article  Google Scholar 

  • Dereeper A, Guigon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guidon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36 (Suppl. 2):W465–W469

    Google Scholar 

  • Dereeper A, Audic S, Claverie JM, Banc G (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 12:8 (open access)

    Google Scholar 

  • Duncan O, Murcha MW, Whelan J (2012) Unique components of the plant mitochondrial protein import apparatus. Biochim Biophys Acta. doi:10.1016/j.bbamcr.2012.02.015

  • Dünschede B, Bals T, Funke S, Schünemann D (2011) Interaction studies between the chloroplast signal recognition particle subunit CpSRP43 and the full-length translocase Alb3 reveal a membrane-embedded binding region in Alb3. J Biol Chem 286:35187–35195

    Article  PubMed  Google Scholar 

  • Fiumera HL, Dunham MJ, Saracco SA, Butler CA, Kelly JA, Fox TD (2009) Translocation and assembly of mitochondrially coded Saccharomyces cerevisiae cytochrome c oxidase subunit Cox2 by Oxa1 and Yme1 in the absence of Cox18. Genetics 182:519–528

    Article  PubMed  CAS  Google Scholar 

  • Frazier AE, Chacinska A, Truscott KN, Guiard B, Pfanner N, Rehling P (2003) Mitochondria use different mechanisms for transport of multispanning membrane proteins through the intermembrane space. Mol Cell Biol 23:7818–7828

    Article  PubMed  CAS  Google Scholar 

  • Frydman J, Höhfeld J (1997) Chaperones get in touch: the Hip-Hop connection. Trends Biochem Sci 22:87–92

    Article  PubMed  CAS  Google Scholar 

  • Funes S, Nargang FE, Neupert W, Herrmann JM (2004a) The Oxa2 protein of Neurospora crassa plays a critical role in the biogenesis of cytochrome oxidase and defines a ubiquitous subbranch of the Oxa1/YidC/Alb3 protein family. Mol Biol Cell 15:1853–1861

    Article  PubMed  CAS  Google Scholar 

  • Funes S, Gerdes L, Inaba M, Soll J, Herrmann JM (2004b) The Arabidopsis thaliana chloroplast inner envelope protein ARTEMIS is a functional member of the Alb3/Oxa1/YidC family of proteins. FEBS Lett 569:89–93

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Funes S, Kauff F, van der Sluis EO, Ott M, Herrmann JM (2011) Evolution of YidC/Oxa1/Alb3 insertases: three independent gene duplications followed by functional specialization in bacteria, mitochondria and chloroplasts. Biol Chem 392:13–19

    Article  PubMed  CAS  Google Scholar 

  • Gava LM, Gonçalves DC, Borges JC, Ramos CH (2011) Stoichiometry and thermodynamics of the interaction between the C-terminus of human 90 kDa heat shock protein Hsp90 and the mitochondrial translocase of outer membrane Tom70. Arch Biochem Biophys 513:119–125

    Article  PubMed  CAS  Google Scholar 

  • Gebert N, Chacinska A, Wagner K, Guiard B, Koehler CM, Rehling P, Pfanner N, Wiedemann N (2008) Assembly of the three small Tim proteins precedes docking to the mitochondrial carrier translocase. EMBO Rep 9:548–554

    Article  PubMed  CAS  Google Scholar 

  • Gerdes L, Bals T, Klostermann E, Karl M, Philippar K, Hünken M, Soll J, Schünemann D (2006) A second thylakoid membrane-localized Alb3/OxaI/YidC homologue is involved in proper chloroplast biogenesis in Arabidopsis thaliana. J Biol Chem 281:16632–16642

    Article  PubMed  CAS  Google Scholar 

  • Hamel P, Sakamoto W, Wintz H, Dujardin G (1997) Functional complementation of an oxa1-yeast mutation identifies an Arabidopsis thaliana cDNA involved in the assembly of respiratory complexes. Plant J 12:1319–1327

    Article  PubMed  CAS  Google Scholar 

  • He K, Fox TD (1997) Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p. Mol Biol Cell 8:1449–1460

    PubMed  CAS  Google Scholar 

  • Hell K, Herrmmann J, Pratje E, Neupert W, Stuart RA (1997) Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space. FEBS Lett 418:367–370

    Article  PubMed  CAS  Google Scholar 

  • Hell K, Herrmann JM, Pratje E, Neupert W, Stuart RA (1998) Oxa1p, an essential component of the N-tail protein export machinery in mitochondria. Proc Natl Acad Sci USA 95:2250–2255

    Article  PubMed  CAS  Google Scholar 

  • Hell K, Neupert W, Stuart RA (2001) Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. EMBO J 20:1281–1288

    Article  PubMed  CAS  Google Scholar 

  • Hildenbeutel M, Theis M, Geier M, Haferkamp I, Ns HE, Herrmann JM, Ott M (2012) The membrane insertase Oxa1 is required for efficient import of carrier proteins into mitochondria. J Mol Biol 423:590–599

    Article  PubMed  CAS  Google Scholar 

  • Jia L, Dienhart M, Schramp M, McCauley M, Hell K, Stuart RA (2003) Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal region of Oxa1. EMBO J 22:6438–6447

    Article  PubMed  CAS  Google Scholar 

  • Jia L, Dienhart MK, Stuart RA (2007) Oxa1 directly interacts with Atp9 and mediates its assembly into the mitochondrial F1FO-ATP synthase complex. Mol Biol Cell 18:1897–1908

    Article  PubMed  CAS  Google Scholar 

  • Jia L, Kaur J, Stuart A (2009) Mapping of the Saccaromyces cerevisiae Oxa1-mitochondrial ribosome interface and identification of Mrp40, a ribosomal protein in close proximity to Oxa1 and critical for oxidative phosphorylation complex assembly. Eukaryot Cell 8:1792–1802

    Article  PubMed  CAS  Google Scholar 

  • Jiang F, Yi L, Moore M, Chen M, Rohl T, van Wijk KJ, de Gier JWL, Henry R, Dalbey RE (2002) Chloroplast YidC homolog albino3 can functionally complement the bacterial YidC depletion strain and promote membrane insertion of both bacterial and chloroplast thylakoid proteins. J Biol Chem 277:19281–19288

    Article  PubMed  CAS  Google Scholar 

  • Karl M, Soll J, Ankele E (2009) The role of Alb3/YidC-like proteins in the formation of photosynthetic membranes. Curr Topics Plant Biol 10:61–77

    Google Scholar 

  • Kermorgant M, Bonnefoy N, Dujardin G (1997) Oxa1p, which is required for cytochrome c oxidase and ATP synthase complex formation, is embedded in the mitochondrial inner membrane. Curr Genet 31:302–307

    Article  PubMed  CAS  Google Scholar 

  • Kerscher O, Holder J, Srinivasan M, Leung RS, Jensen RE (1997) The Tim54p-Tim22p complex mediates insertion of proteins into the mitochondrial inner membrane. J Cell Biol 139:1663–1675

    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 

  • Kuhn A, Stuart R, Henry R, Dalbey RE (2003) The Alb3/Oxa1/YidC protein family: membrane-localized chaperones facilitating membrane protein insertion? Trends Cell Biol 13:510–516

    Article  PubMed  CAS  Google Scholar 

  • Lewis NE, Marty NJ, Kathir KM, Rajalingam D, Knight AD, Daily A, Kumar TKS, Henry R, Goforth RL (2010) A dynamic CpSRP43-Albino3 interaction mediates translocase regulation of CpSRP targeting components. J Biol Chem 285:34220–34230

    Article  PubMed  CAS  Google Scholar 

  • Lu Y, Li C, Wang H, Chen H, Berg H, Xia Y (2011) AtPPR2, an Arabidopsis pentatricopeptide repeat protein, binds to plastid 23S rRNA and plays an important role in the first mitotic division during gametogenesis and in cell proliferation during embryogenesis. Plant J 67:13–25

    Article  PubMed  CAS  Google Scholar 

  • Luirink J, Samuelsson T, de Gier JW (2001) YidC/Oxa1p/Alb3: evolutionarily conserved mediators of membrane protein assembly. FEBS Lett 501:1–5

    Article  PubMed  CAS  Google Scholar 

  • Luirink J, von Heijne G, Houben E, de Gier JW (2005) Biogenesis of inner membrane proteins in Escherichia coli. Annu Rev Microbiol 59:329–355

    Article  PubMed  CAS  Google Scholar 

  • Manavski N, Guyon V, Meurer J, Wienand U, Brettschneider R (2012) An essential pentatricopeptide repeat protein facilitates 5′ maturation and translation initiation of rps3 mRNA in maize mitochondria. Plant Cell 24:3087–3105

    Article  PubMed  CAS  Google Scholar 

  • MdE Haque, Elmore KB, Tripathy A, Koc H, Koc EC, Spremulli LL (2010) Properties of the C-terminal tail of human mitochondrial inner membrane protein Oxa1L and its interactions with mammalian mitochondrial ribosomes. J Biol Chem 285:28353–28362

    Article  Google Scholar 

  • Moore M, Harrison MS, Peterson EC, Henry R (2000) Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 275:1529–1532

    Article  PubMed  CAS  Google Scholar 

  • Nagamori S, Smirnova IN, Kaback HR (2004) Role of YidC in folding of polytopic membrane proteins. J Cell Biol 165:53–62

    Article  PubMed  CAS  Google Scholar 

  • Oliver DC, Paetzel M (2008) Crystal structure of the major periplasmic domain of the bacterial membrane protein assembly facilitator YidC. J Biol Chem 283:5208–5216

    Article  PubMed  CAS  Google Scholar 

  • Palmer SR, Crowley PJ, Oli MW, Ruelf MA, Michalek SM, Brady LJ (2012) YidC1 and YidC2 are functionally distinct proteins involved in protein secretion, biofilm formation and cariogenicity of Streptococcus mutans. Microbiology 158:1702–1712

    Article  PubMed  CAS  Google Scholar 

  • Pierrel F, Bestwick ML, Cobine PA, Khalimonchuk O, Cricco JA, Winge DR (2007) Coa1 links the Mss51 post-translational function to Cox1 cofactor insertion in cytochrome c oxidase assembly. EMBO J 26:4335–4346

    Article  PubMed  CAS  Google Scholar 

  • Pohlschröder M, Hartmann E, Hand NJ, Dilks K, Haddad A (2005) Diversity and evolution of protein translocation. Annu Rev Microbiol 59:91–111

    Article  PubMed  Google Scholar 

  • Preuss M, Leonhard K, Helll K, Stuart RA, Neupert W, Herrmann JM (2001). Mba1, a novel component of the mitochondrial protein export machinery of the yeast Saccharomyces cerevisiae. J Cell Biol 153:1085–1096.

    Google Scholar 

  • Preuss M, Ott M, Funes S, Luirink J, Herrmann JM (2005) Evolution of mitochondrial Oxa proteins from bacterial YidC. Inherited and acquired functions of a conserved protein insertion machinery. J Biol Chem 280:13004–13011

    Article  PubMed  CAS  Google Scholar 

  • Qbadou S, Becker T, Mirus O, Tews I, Soll J, Schleiff E (2006) The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO J 25:1836–1847

    Article  PubMed  CAS  Google Scholar 

  • Ravaud S, Stjepanovic G, Wild K, Sinning I (2008) The crystal structure of the periplasmic domain of the Escherichia coli membrane protein insertase YidC contains a substrate binding cleft. J Biol Chem 283:9350–9358

    Article  PubMed  CAS  Google Scholar 

  • Richter CV, Bals T, Schünemann D (2010) Component interactions, regulation and mechanisms of chloroplast signal recognition particle-dependent protein transport. Eur J Cell Biol 89:965–973

    Article  PubMed  CAS  Google Scholar 

  • Sääf A, Monné M, de Gier JW, von Heijne G (1998) Membrane topology of the 60-kDa Oxa1p homologue from Escherichia coli. J Biol Chem 273:30415–30418

    Article  PubMed  Google Scholar 

  • Sakamoto W, Spielewoy N, Bonnard G, Murata M, Wintz H (2000) Mitochondrial localization of AtOxa1, an Arabidopsis homologue of yeast Oxa1p involved in the insertion and assembly of protein complexes in mitochondrial inner membrane. Plant Cell Physiol 41:1157–1163

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Saracco SA, Fox TD (2002) Cox18p is required for export of the mitochondrially encoded Saccaromyces cerevisiae Cox2p C-tail and interacts with Pnt1p and Mss2p in the inner membrane. Mol Biol Cell 13:1122–1131

    Article  PubMed  CAS  Google Scholar 

  • Sato T, Mihara K (2009) Topogenesis of mammalian Oxa1, a component of the mitochondrial inner membrane protein export machinery. J Biol Chem 284:14819–14827

    Article  PubMed  CAS  Google Scholar 

  • Schleyer M, Schmidt B, Neupert W (1982) Requirement of a membrane potential for the posttranslational transfer of proteins into mitochondria. Eur J Biochem 125:109–116

    Article  PubMed  CAS  Google Scholar 

  • Schwacke R, Schneider A, Van Der Graaff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flugge UI, Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131:16–26

    Article  PubMed  CAS  Google Scholar 

  • Scotti PA, Urbanus ML, Brunner J, de Gier JW, von Heijne G, can der Does C, Driessen AJ, Oudega B, Luirink J (2000) YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J 19:542–549

    Google Scholar 

  • Sørmo CG, Brembu T, Winge P, Bones AM (2011) Arabidopsis thaliana MIRO1 and MIRO2 GTPases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis. PLoS ONE 6:e18530

    Article  PubMed  Google Scholar 

  • Souza RL, Green-Willms NS, Fox TD, Tzagoloff A, Nobrega FG (2000) Cloning and characterization of COX18, a Saccharomyces cerevisiae PET gene required for the assembly of cytochrome oxidase. J Biol Chem 275:14898–14902

    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 

  • Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C, Coupland G (1997) ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9:717–730

    PubMed  CAS  Google Scholar 

  • Szyrach G, Ott M, Bonnefoy N, Neupert W, Herrmann JM (2003) Ribosome binding to the Oxa1 complex facilitates co-translational protein insertion in mitochondria. EMBO J 22:6448–6457

    Article  PubMed  CAS  Google Scholar 

  • Urbanus ML, Scotti PA, Froderberg L, Saaf A, de Gier JW, Brunner J, Samuelson JC, Dalbey RE, Oudega B, Luirink J (2001) Sec-dependent membrane protein insertion: sequential interaction of nascent FtsQ with SecY and YidC. EMBO Rep 2:524–529

    PubMed  CAS  Google Scholar 

  • Urbanus ML, Fröderberg L, Drew D, Björk P, de Gier JWL, Brunner J, Oudega B, Luirink J (2002) Targeting, insertion, and localization of Escherichia coli YidC. J Biol Chem 277:12718–12723

    Article  PubMed  CAS  Google Scholar 

  • Van Bloois E, Nagamore S, Koningstein G, Ullers RS, Preuss M, Oudega B, Harms N, Kaback HR, Herrmann JM, Luirink J (2005) The Sec-independent function of Escherichia coli YidC is evolutionary-conserved and essential. J Biol Chem 280:12996–13003

    Article  PubMed  Google Scholar 

  • Van Bloois E, Koningstein G, Bauerschmitt H, Herrmann JM, Luirink J (2007) Saccaromyces cerevisiae Cox18 complements the essential Sec-independent function of Escherichia coli YidC. FEBS J 274:5704–5713

    Article  PubMed  Google Scholar 

  • Van Der Laan M, Bechtluft P, Kol S, Nouwen N, Driessen AJ (2004) F1F0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis. J Cell Biol 165:213–222

    Article  PubMed  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 

  • Waegemann K, Soll J (1995) Characterization and isolation of the chloroplast protein import machinery. Methods Cell Biol 50:255–267

    Article  PubMed  CAS  Google Scholar 

  • Wang P, Dalbey RE (2011) Inserting membrane proteins: the YidC/Oxa1/Alb3 machinery in bacteria, mitochondria, and chloroplasts. Biochim Biophys Acta 1808:866–875

    Article  PubMed  CAS  Google Scholar 

  • Whelan J, Knorpp C, Glaser E (1990) Sorting of precursor proteins between isolated spinach leaf mitochondria and chloroplasts. Plant Mol Biol 14:977–982

    Article  PubMed  CAS  Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2:e718

    Article  PubMed  Google Scholar 

  • Xie K, Kiefer D, Nagler G, Dalbey RE, Kuhn A (2006) Different regions of the nonconserved large periplasmic domain of Escherichia coli YidC are involved in the SecF interaction and membrane insertase activity. Biochem 45:13401–13408

    Article  CAS  Google Scholar 

  • Yamaoka S, Leaver CJ (2008) EMB2473/MIRO1, an Arabidopsis Miro GTPase, is required for embryogenesis and influences mitochondrial morphology in pollen. Plant Cell 20:589–601

    Article  PubMed  CAS  Google Scholar 

  • Yen MR, Harley KT, Tseng YH, Saier MH Jr (2001) Phylogenetic and structural analyses of the oxa1 family of protein translocases. FEMS Microbiol Lett 204:223–231

    Article  PubMed  CAS  Google Scholar 

  • Yi L, Dalbey RE (2005) Oxa1/Alb3/YidC system for insertion of membrane proteins in mitochondria, chloroplasts and bacteria. Mol Membr Biol 22:101–111

    Article  PubMed  CAS  Google Scholar 

  • Yi L, Jiang F, Chen M, Cain B, Bolhuis A, Dalbey RE (2003) YidC is strictly required for membrane insertin of subunits a and c of the F(1)F(0)ATP synthase and SecE of the SecYEG translocase. Biochemistry 42:10537–10544

    Article  PubMed  CAS  Google Scholar 

  • Young JC, Hoogenraad NJ, Hartl FU (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112:41–50

    Article  PubMed  CAS  Google Scholar 

  • Yuan J, Zweers JC, van Dijl JM, Dalbey RE (2010) Protein transport across and into cell membranes in bacteria and archaea. Cell Mol Life Sci 67:179–199

    Article  PubMed  CAS  Google Scholar 

  • Zhang YJ, Tian HF, Wen JF (2009) The evolution of YidC/Oxa1/Alb3 family in the three domains of life: a phylogenomic analysis. BMC Evol Biol 9:137 (open access)

    Google Scholar 

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Acknowledgments

We thank Prof. Andreas Weber (University Düsseldorf, Germany) for the CFP-PTS1 clone, Dr. Chris Hawes (Bookes University, Osford, UK) for the ST-GFP clone and Dr. Barbara Pickard (Washington University, St. Luis, USA) for the SP + ER-GFP, dcp.r-GFP and mtio-d2r clones. This work was supported by the Deutsche Forschungsgemeinschaft SFB-TR1 project C4.

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  1. Monique Benz

    Present address: Energy Biosciences Institute, University of California, 2151 Berkeley Way, Berkeley, CA, 94720-5230, USA

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  1. Department Biologie I-Botanik, Ludwig-Maximilians-Universität München, Grosshadernerstrasse 2-4, Planegg-Martinsried, 85152, Munich, Germany

    Monique Benz, Jürgen Soll & Elisabeth Ankele

  2. Munich Center of Integrated Protein Science CIPSM, Ludwig-Maximilians-University, Feodor-Lynen-Strasse 25, 81377, Munich, Germany

    Elisabeth Ankele

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A contribution to the Special Issue on Evolution and Biogenesis of Chloroplasts and Mitochondria.

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Benz, M., Soll, J. & Ankele, E. Arabidopsis thaliana Oxa proteins locate to mitochondria and fulfill essential roles during embryo development. Planta 237, 573–588 (2013). https://doi.org/10.1007/s00425-012-1793-9

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