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Evolution of the Protein Translocons of the Chloroplast Envelope

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Endosymbiosis

Abstract

It is widely accepted that chloroplasts originated through the endosymbiotic uptake of an ancestral cyanobacterium by a mitochondria-containing heterotrophic host cell. In the course of evolution these once autonomous bacteria became increasingly integrated into their host’s cellular environment. The permanent transfer of large portions of genetic information from the endosymbiont to the host’s genome was essential for the establishment of a truly symbiotic relationship. However, as a consequence, the import of now cytoplasmically synthesized proteins into these new organelles became essential and specific translocons for the import of these proteins had to evolve. Interestingly, evidence suggests that chloroplasts take advantage of already existing prokaryotic proteins as the import machinery evolved. Here, we discuss the phylogenetic relationships of known translocon components and try to reconstruct important steps in the evolution of the import machinery.

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References

  • Akita M, Nielsen E, Keegstra K (1997) Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J Cell Biol 136(5):983–994

    PubMed  CAS  Google Scholar 

  • Allen JF (2003) The function of genomes in bioenergetic organelles. Philos Trans R Soc Lond B Biol Sci 358(1429):19–37, discussion 37–38

    PubMed  CAS  Google Scholar 

  • Armbrust E, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306(5693):79–86

    PubMed  CAS  Google Scholar 

  • Bae W, Lee Y, Kim DH, Lee J, Kim S, Sohn EJ, Hwang I (2008) AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nat Cell Biol 10(2):220–227

    PubMed  CAS  Google Scholar 

  • Baldwin AJ, Inoue K (2006) The most C-terminal tri-glycine segment within the polyglycine stretch of the pea Toc75 transit peptide plays a critical role for targeting the protein to the chloroplast outer envelope membrane. FEBS J 273(7):1547–1555

    PubMed  CAS  Google Scholar 

  • Balsera M, Stengel A, Soll J, Bölter B (2007) Tic62: a protein family from metabolism to protein translocation. BMC Evol Biol 7:43

    PubMed  Google Scholar 

  • Beck K, Wu LF, Brunner J, Müller M (2000) Discrimination between SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J 19(1):134–143

    PubMed  CAS  Google Scholar 

  • Becker T, Jelic M, Vojta A, Radunz A, Soll J, Schleiff E (2004) Preprotein recognition by the Toc complex. EMBO J 23(3):520–530

    PubMed  CAS  Google Scholar 

  • Becker T, Qbadou S, Jelic M, Schleiff E (2005) Let’s talk about … chloroplast import. Plant Biol 7(1):1–14

    PubMed  CAS  Google Scholar 

  • Benz JP, Stengel A, Lintala M, Lee YH, Weber A, Philippar K, Gugel IL, Kaieda S, Ikegami T, Mulo P, Soll J, Bolter B (2009) Arabidopsis Tic62 and ferredoxin-NADP(H) oxidoreductase form light-regulated complexes that are integrated into the chloroplast redox poise. Plant Cell 21(12):3965–3983

    PubMed  CAS  Google Scholar 

  • Bionda T, Tillmann B, Simm S, Beilstein K, Ruprecht M, Schleiff E (2010) Chloroplast import signals: the length requirement for translocation in vitro and in vivo. J Mol Biol 402(3):510–523

    PubMed  CAS  Google Scholar 

  • Bodyl A, Mackiewicz P, Stiller JW (2010) Comparative genomic studies suggest that the cyanobacterial endosymbionts of the amoeba Paulinella chromatophora possess an import apparatus for nuclear-encoded proteins. Plant Biol 12(4):639–649

    PubMed  CAS  Google Scholar 

  • Bohnsack MT, Schleiff E (2010) The evolution of protein targeting and translocation systems. Biochim Biophys Acta 1803(10):1115–1130

    PubMed  CAS  Google Scholar 

  • Bonen L, Calixte S (2006) Comparative analysis of bacterial-origin genes for plant mitochondrial ribosomal proteins. Mol Biol Evol 23(3):701–712

    PubMed  CAS  Google Scholar 

  • Bräutigam A, Weber APM (2009) Proteomic analysis of the proplastid envelope membrane provides novel insights into small molecule and protein transport across proplastid membranes. Mol Plant 2(6):1247–1261

    PubMed  Google Scholar 

  • Bredemeier R, Schlegel T, Ertel F, Vojta A, Borissenko L, Bohnsack MT, Groll M, von Haeseler A, Schleiff E (2007) Functional and phylogenetic properties of the pore-forming beta-barrel transporters of the Omp85 family. J Biol Chem 282(3):1882–1890

    PubMed  CAS  Google Scholar 

  • Bruce BD (2000) Chloroplast transit peptides. Structure, function and evolution. Trends Cell Biol 10(10):440–447

    PubMed  CAS  Google Scholar 

  • Bruce BD (2001) The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochim Biophys Acta 1541(1–2):2–21

    PubMed  CAS  Google Scholar 

  • Bullmann L, Haarmann R, Mirus O, Bredemeier R, Hempel F, Maier UG, Schleiff E (2010) Filling the gap, evolutionarily conserved Omp85 in plastids of chromalveolates. J Biol Chem 285(9):6848–6856

    PubMed  CAS  Google Scholar 

  • Caliebe A, Grimm R, Kaiser G, Lubeck J, Soll J, Heins L (1997) The chloroplastic protein import machinery contains a Rieske-type iron-sulfur cluster and a mononuclear iron-binding protein. EMBO J 16(24):7342–7350

    PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2003) Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philos Trans R Soc Lond B Biol Sci 358(1429):109–133, discussion 133–134

    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(1–3):109–114

    PubMed  CAS  Google Scholar 

  • Chiu CC, Li HM (2008) Tic40 is important for reinsertion of proteins from the chloroplast stroma into the inner membrane. Plant J 56(5):793–801

    PubMed  CAS  Google Scholar 

  • Chou ML, Fitzpatrick LM, Tu SL, Budziszewski G, Potter-Lewis S, Akita M, Levin JZ, Keegstra K, Li HM (2003) Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J 22(12):2970–2980

    PubMed  CAS  Google Scholar 

  • Cline K, Dabney-Smith C (2008) Plastid protein import and sorting: different paths to the same compartments. Curr Opin Plant Biol 11(6):585–592

    PubMed  CAS  Google Scholar 

  • Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik KV, Allen JF, Martin W, Dagan T (2008) Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol Biol Evol 25(4):748–761

    PubMed  CAS  Google Scholar 

  • Driessen AJM, Nouwen N (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77:643–667

    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(6):492–498

    PubMed  CAS  Google Scholar 

  • du Plessis DJF, Nouwen N, Driessen AJM (2011) The Sec translocase. Biochim Biophys Acta 1808(3):851–865

    PubMed  Google Scholar 

  • Duy D, Wanner G, Meda AR, von Wiren N, Soll J, Philippar K (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19(3):986–1006

    PubMed  CAS  Google Scholar 

  • Eckart K, Eichacker L, Sohrt K, Schleiff E, Heins L, Soll J (2002) A Toc75-like protein import channel is abundant in chloroplasts. EMBO Rep 3(6):557–562

    PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300(4):1005–1016

    PubMed  CAS  Google Scholar 

  • Ertel F, Mirus O, Bredemeier R, Moslavac S, Becker T, Schleiff E (2005) The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. J Biol Chem 280(31):28281–28289

    PubMed  CAS  Google Scholar 

  • Fellerer C, Schweiger R, Schongruber K, Soll J, Schwenkert S (2011) Cytosolic HSP90 cochaperones HOP and FKBP interact with freshly synthesized chloroplast preproteins of Arabidopsis. Mol Plant 4(6):1133–1145

    PubMed  CAS  Google Scholar 

  • Field MC, Dacks JB (2009) First and last ancestors: reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. Curr Opin Cell Biol 21(1):4–13

    PubMed  CAS  Google Scholar 

  • Fulda S, Norling B, Schoor A, Hagemann M (2002) The Slr0924 protein of Synechocystis sp. strain PCC 6803 resembles a subunit of the chloroplast protein import complex and is mainly localized in the thylakoid lumen. Plant Mol Biol 49(1):107–118

    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(1):19–24

    PubMed  CAS  Google Scholar 

  • Gessmann D, Flinner N, Pfannstiel J, Schlosinger A, Schleiff E, Nussberger S, Mirus O (2011) Structural elements of the mitochondrial preprotein-conducting channel Tom40 dissolved by bioinformatics and mass spectrometry. Biochim Biophys Acta 1807(12):1647–1657

    PubMed  CAS  Google Scholar 

  • Gould SB, Sommer MS, Hadfi K, Zauner S, Kroth PG, Maier UG (2006) Protein targeting into the complex plastid of cryptophytes. J Mol Evol 62(6):674–681

    PubMed  CAS  Google Scholar 

  • Grosche C, Hempel F, Bolte K, Abram L, Maier UG, Zauner S (2013) Protein import into complex plastids: current findings and perspectives. In: Löffelhardt W (ed) Endosymbiosis. Springer, Wien New York, pp 215–232

    Google Scholar 

  • Grudnik P, Bange G, Sinning I (2009) Protein targeting by the signal recognition particle. Biol Chem 390(8):775–782

    PubMed  CAS  Google Scholar 

  • Gupta RS (1995) Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol Biol Evol 12(6):1063–1073

    PubMed  CAS  Google Scholar 

  • Gupta RS, Golding GB (1993) Evolution of HSP70 gene and its implications regarding relationships between archaebacteria, eubacteria, and eukaryotes. J Mol Evol 37(6):573–582

    PubMed  CAS  Google Scholar 

  • Hagan CL, Silhavy TJ, Kahne D (2011) beta-Barrel membrane protein assembly by the Bam complex. Annu Rev Biochem 80:189–210

    PubMed  CAS  Google Scholar 

  • Harb OS, Chatterjee B, Fraunholz MJ, Crawford MJ, Nishi M, Roos DS (2004) Multiple functionally redundant signals mediate targeting to the apicoplast in the apicomplexan parasite Toxoplasma gondii. Eukaryot Cell 3(3):663–674

    PubMed  CAS  Google Scholar 

  • Heins L, Mehrle A, Hemmler R, Wagner R, Kuchler M, Hormann F, Sveshnikov D, Soll J (2002) The preprotein conducting channel at the inner envelope membrane of plastids. EMBO J 21(11):2616–2625

    PubMed  CAS  Google Scholar 

  • Hinnah SC, Wagner R, Sveshnikova N, Harrer R, Soll J (2002) The chloroplast protein import channel Toc75: pore properties and interaction with transit peptides. Biophys J 83(2):899–911

    PubMed  CAS  Google Scholar 

  • Hirabayashi Y, Kikuchi S, Oishi M, Nakai M (2011) In vivo studies on the roles of two closely related Arabidopsis Tic20 proteins, AtTic20-I and AtTic20-IV. Plant Cell Physiol 52(3):469–478

    PubMed  CAS  Google Scholar 

  • Hirohashi T, Hase T, Nakai M (2001) Maize non-photosynthetic ferredoxin precursor is mis-sorted to the intermembrane space of chloroplasts in the presence of light. Plant Physiol 125(4):2154–2163

    PubMed  CAS  Google Scholar 

  • Hiss JA, Schneider G (2009) Architecture, function and prediction of long signal peptides. Brief Bioinform 10(5):569–578

    PubMed  CAS  Google Scholar 

  • Huang W, Ling Q, Bedard J, Lilley K, Jarvis P (2011) In vivo analyses of the roles of essential Omp85-related proteins in the chloroplast outer envelope membrane. Plant Physiol 157(1):147–159

    PubMed  CAS  Google Scholar 

  • Humphries AD, Streimann IC, Stojanovski D, Johnston AJ, Yano M, Hoogenraad NJ, Ryan MT (2005) Dissection of the mitochondrial import and assembly pathway for human Tom40. J Biol Chem 280(12):11535–11543

    PubMed  CAS  Google Scholar 

  • Ieva R, Tian P, Peterson JH, Bernstein HD (2011) Sequential and spatially restricted interactions of assembly factors with an autotransporter beta domain. Proc Natl Acad Sci USA 108(31):E383–E391

    PubMed  CAS  Google Scholar 

  • Inoue K, Keegstra K (2003) A polyglycine stretch is necessary for proper targeting of the protein translocation channel precursor to the outer envelope membrane of chloroplasts. Plant J 34(5):661–669

    PubMed  CAS  Google Scholar 

  • Inoue K, Potter D (2004) The chloroplastic protein translocation channel Toc75 and its paralog OEP80 represent two distinct protein families and are targeted to the chloroplastic outer envelope by different mechanisms. Plant J 39(3):354–365

    PubMed  CAS  Google Scholar 

  • Inoue K, Demel R, de Kruijff B, Keegstra K (2001) The N-terminal portion of the preToc75 transit peptide interacts with membrane lipids and inhibits binding and import of precursor proteins into isolated chloroplasts. Eur J Biochem 268(14):4036–4043

    PubMed  CAS  Google Scholar 

  • Inoue K, Baldwin AJ, Shipman RL, Matsui K, Theg SM, Ohme-Takagi M (2005) Complete maturation of the plastid protein translocation channel requires a type I signal peptidase. J Cell Biol 171(3):425–430

    PubMed  CAS  Google Scholar 

  • Jackson-Constan D, Akita M, Keegstra K (2001) Molecular chaperones involved in chloroplast protein import. Biochim Biophys Acta 1541(1–2):102–113

    PubMed  CAS  Google Scholar 

  • Jacob-Dubuisson F, Villeret V, Clantin B, Delattre AS, Saint N (2009) First structural insights into the TpsB/Omp85 superfamily. Biol Chem 390(8):675–684

    PubMed  CAS  Google Scholar 

  • Jarvis P (2008) Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol 179(2):257–285

    PubMed  CAS  Google Scholar 

  • Jürgens G (2004) Membrane trafficking in plants. Annu Rev Cell Dev Biol 20:481–504

    PubMed  Google Scholar 

  • Kalanon M, McFadden GI (2008) The chloroplast protein translocation complexes of Chlamydomonas reinhardtii. a bioinformatic comparison of Toc and Tic components in plants, green algae and red algae. Genetics 179(1):95–112

    PubMed  CAS  Google Scholar 

  • Kessler F, Schnell D (2009) Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Curr Opin Cell Biol 21(4):494–500

    PubMed  CAS  Google Scholar 

  • Kikuchi S, Oishi M, Hirabayashi Y, Lee DW, Hwang I, Nakai M (2009) A 1-megadalton translocation complex containing Tic20 and Tic21 mediates chloroplast protein import at the inner envelope membrane. Plant Cell 21(6):1781–1797

    PubMed  CAS  Google Scholar 

  • Kikuchi S, Bédard J, Hirano M, Hirabayashi Y, Oishi M, Imai M, Takase M, Ide T, Nakai M (2013) Uncovering the protein translocon at the chloroplast inner envelope membrane. Science 339(6119):571–574

    PubMed  CAS  Google Scholar 

  • Kilian O, Kroth PG (2005) Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 41(2):175–183

    PubMed  CAS  Google Scholar 

  • Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjolander K, Gruissem W, Baginsky S (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14(5):354–362

    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(3):206–214

    PubMed  CAS  Google Scholar 

  • Koenig P, Mirus O, Haarmann R, Sommer MS, Sinning I, Schleiff E, Tews I (2010) Conserved properties of polypeptide transport-associated (POTRA) domains derived from cyanobacterial Omp85. J Biol Chem 285(23):18016–18024

    PubMed  CAS  Google Scholar 

  • Kouranov A, Chen X, Fuks B, Schnell DJ (1998) Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane. J Cell Biol 143(4):991–1002

    PubMed  CAS  Google Scholar 

  • Kovacheva S, Bedard J, Patel R, Dudley P, Twell D, Rios G, Koncz C, Jarvis P (2005) In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J 41(3):412–428

    PubMed  CAS  Google Scholar 

  • Kovacheva S, Bedard J, Wardle A, Patel R, Jarvis P (2007) Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant J 50(2):364–379

    PubMed  CAS  Google Scholar 

  • Kovacs-Bogdan E, Benz JP, Soll J, Bölter B (2011) Tic20 forms a channel independent of Tic110 in chloroplasts. BMC Plant Biol 11:133

    PubMed  CAS  Google Scholar 

  • Koyanagi T, Katayama T, Suzuki H, Kumagai H (2004) Identification of the LIV-I/LS system as the third phenylalanine transporter in Escherichia coli K-12. J Bacteriol 186(2):343–350

    PubMed  CAS  Google Scholar 

  • Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N (2003) An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 278(49):48520–48523

    PubMed  CAS  Google Scholar 

  • Kuchler M, Decker S, Hormann F, Soll J, Heins L (2002) Protein import into chloroplasts involves redox-regulated proteins. EMBO J 21(22):6136–6145

    PubMed  Google Scholar 

  • Ladig R, Sommer MS, Hahn A, Leisegang MS, Papasotiriou DG, Ibrahim M, Elkehal R, Karas M, Zickermann V, Gutensohn M, Brandt U, Klosgen RB, Schleiff E (2011) A high-definition native polyacrylamide gel electrophoresis system for the analysis of membrane complexes. Plant J 67(1):181–194

    PubMed  CAS  Google Scholar 

  • Lee DW, Lee S, Lee GJ, Lee KH, Kim S, Cheong GW, Hwang I (2006) Functional characterization of sequence motifs in the transit peptide of Arabidopsis small subunit of Rubisco. Plant Physiol 140(2):466–483

    PubMed  CAS  Google Scholar 

  • Lee DW, Kim JK, Lee S, Choi S, Kim S, Hwang I (2008) Arabidopsis nuclear-encoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 20(6):1603–1622

    PubMed  CAS  Google Scholar 

  • Lee S, Lee DW, Lee Y, Mayer U, Stierhof YD, Lee S, Jürgens G, Hwang I (2009) Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. Plant Cell 21(12):3984–4001

    PubMed  CAS  Google Scholar 

  • Leipe DD, Wolf YI, Koonin EV, Aravind L (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317(1):41–72

    PubMed  CAS  Google Scholar 

  • Li HM, Chiu CC (2010) Protein transport into chloroplasts. Annu Rev Plant Biol 61:157–180

    PubMed  CAS  Google Scholar 

  • Li M, Schnell DJ (2006) Reconstitution of protein targeting to the inner envelope membrane of chloroplasts. J Cell Biol 175(2):249–259

    PubMed  CAS  Google Scholar 

  • Löffelhardt W, von Haeseler A, Schleiff E (2007) The beta-barrel shaped polypeptide transporter, an old concept for precursor protein transfer across membranes. Symbiosis 44:33–42

    Google Scholar 

  • Lubeck J, Soll J, Akita M, Nielsen E, Keegstra K (1996) Topology of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane. EMBO J 15(16):4230–4238

    PubMed  CAS  Google Scholar 

  • Lubeck J, Heins L, Soll J (1997) A nuclear-coded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle. J Cell Biol 137(6):1279–1286

    PubMed  CAS  Google Scholar 

  • Lv HX, Guo GQ, Yang ZN (2009) Translocons on the inner and outer envelopes of chloroplasts share similar evolutionary origin in Arabidopsis thaliana. J Evol Biol 22(7):1418–1428

    PubMed  CAS  Google Scholar 

  • Mandon EC, Trueman SF, Gilmore R (2009) Translocation of proteins through the Sec61 and SecYEG channels. Curr Opin Cell Biol 21(4):501–507

    PubMed  CAS  Google Scholar 

  • Marshall JS, DeRocher AE, Keegstra K, Vierling E (1990) Identification of heat shock protein hsp70 homologues in chloroplasts. Proc Natl Acad Sci USA 87(1):374–378

    PubMed  CAS  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99(19):12246–12251

    PubMed  CAS  Google Scholar 

  • Mergaert P, Nikovics K, Kelemen Z, Maunoury N, Vaubert D, Kondorosi A, Kondorosi E (2003) A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 132(1):161–173

    PubMed  CAS  Google Scholar 

  • Miras S, Salvi D, Ferro M, Grunwald D, Garin J, Joyard J, Rolland N (2002) Non-canonical transit peptide for import into the chloroplast. J Biol Chem 277(49):47770–47778

    PubMed  CAS  Google Scholar 

  • Miras S, Salvi D, Piette L, Seigneurin-Berny D, Grunwald D, Reinbothe C, Joyard J, Reinbothe S, Rolland N (2007) Toc159- and Toc75-independent import of a transit sequence-less precursor into the inner envelope of chloroplasts. J Biol Chem 282(40):29482–29492

    PubMed  CAS  Google Scholar 

  • Mirus O, Schleiff E (2009) The evolution of tetratricopeptide repeat domain containing receptors involved in protein translocation. Endocytobiosis Cell Res 19:31–50

    Google Scholar 

  • Mirus O, Schleiff E (2012) Recycling and tinkering - the evolution of protein transport to and into endosymbiotically derived organelles. In: Bullerwell CE (ed) Organelle genetics - evolution of organelle genomes and gene expression. Springer, Berlin

    Google Scholar 

  • Mirus O, Bionda T, von Haeseler A, Schleiff E (2009) Evolutionarily evolved discriminators in the 3-TPR domain of the Toc64 family involved in protein translocation at the outer membrane of chloroplasts and mitochondria. J Mol Model 15(8):971–982

    PubMed  CAS  Google Scholar 

  • Mirus O, Hahn A, Schleiff E (2010) Outer membrane proteins. In: König H, Claus H, Varma A (eds) Prokaryotic cell wall compounds. Structure and biochemistry. Springer, Berlin, pp 175–231

    Google Scholar 

  • Moslavac S, Mirus O, Bredemeier R, Soll J, von Haeseler A, Schleiff E (2005) Conserved pore-forming regions in polypeptide-transporting proteins. FEBS J 272(6):1367–1378

    PubMed  CAS  Google Scholar 

  • Natale P, Bruser T, Driessen AJM (2008) Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane - distinct translocases and mechanisms. Biochim Biophys Acta 1778(9):1735–1756

    PubMed  CAS  Google Scholar 

  • Nazos PM, Antonucci TK, Landick R, Oxender DL (1986) Cloning and characterization of livH, the structural gene encoding a component of the leucine transport system in Escherichia coli. J Bacteriol 166(2):565–573

    PubMed  CAS  Google Scholar 

  • Nicolaisen K, Mariscal V, Bredemeier R, Pernil R, Moslavac S, Lopez-Igual R, Maldener I, Herrero A, Schleiff E, Flores E (2009) The outer membrane of a heterocyst-forming cyanobacterium is a permeability barrier for uptake of metabolites that are exchanged between cells. Mol Microbiol 74(1):58–70

    PubMed  CAS  Google Scholar 

  • Nielsen E, Akita M, Davila-Aponte J, Keegstra K (1997) Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J 16(5):935–946

    PubMed  CAS  Google Scholar 

  • Nowack EC, Grossman AR (2012) Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci USA 109:5340–5345

    PubMed  CAS  Google Scholar 

  • Oreb M, Reger K, Schleiff E (2006) Chloroplast protein import. Reverse genetic approaches. Curr Genomics 7:235–244

    CAS  Google Scholar 

  • Oreb M, Tews I, Schleiff E (2008) Policing Tic ‘n’ Toc, the doorway to chloroplasts. Trends Cell Biol 18(1):19–27

    PubMed  CAS  Google Scholar 

  • Palmer T, Sargent F, Berks BC (2005) Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol 13(4):175–180

    PubMed  CAS  Google Scholar 

  • Paschen SA, Waizenegger T, Stan T, Preuss M, Cyrklaff M, Hell K, Rapaport D, Neupert W (2003) Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 426(6968):862–866

    PubMed  CAS  Google Scholar 

  • Patel R, Hsu SC, Bedard J, Inoue K, Jarvis P (2008) The Omp85-related chloroplast outer envelope protein OEP80 is essential for viability in Arabidopsis. Plant Physiol 148(1):235–245

    PubMed  CAS  Google Scholar 

  • Patron NJ, Waller RF (2007) Transit peptide diversity and divergence: a global analysis of plastid targeting signals. Bioessays 29(10):1048–1058

    PubMed  CAS  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8(10):785–786

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Price DC, Chan CX, Yoon HS, Yang E, Qiu H, Weber AP, Schwacke R, Gross J, Blouin N, Lane C, Reyes-Prieto A, Durnford D, Neilson J, Lang B, Burger G, Steiner J, Loffelhardt W, Meuser J, Posewitz M, Ball S, Arias M, Henrissat B, Coutinho P, Rensing S, Symeonidi A, Doddapaneni H, Green B, Rajah V, Boore J, Bhattacharya D (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335(6070):843–847

    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(9):1836–1847

    PubMed  CAS  Google Scholar 

  • Qbadou S, Becker T, Bionda T, Reger K, Ruprecht M, Soll J, Schleiff E (2007) Toc64–a preprotein-receptor at the outer membrane with bipartide function. J Mol Biol 367(5):1330–1346

    PubMed  CAS  Google Scholar 

  • Ralph SA, Foth BJ, Hall N, McFadden GI (2004) Evolutionary pressures on apicoplast transit peptides. Mol Biol Evol 21(12):2183–2194

    PubMed  CAS  Google Scholar 

  • Reinbothe S, Quigley F, Gray J, Schemenewitz A, Reinbothe C (2004) Identification of plastid envelope proteins required for import of protochlorophyllide oxidoreductase A into the chloroplast of barley. Proc Natl Acad Sci USA 101(7):2197–2202

    PubMed  CAS  Google Scholar 

  • Richardson LGI, Jelokhani-Niaraki M, Smith MD (2009) The acidic domains of the Toc159 chloroplast preprotein receptor family are intrinsically disordered protein domains. BMC Biochem 10:35

    PubMed  Google Scholar 

  • Robinson C, Bolhuis A (2001) Protein targeting by the twin-arginine translocation pathway. Nat Rev Mol Cell Biol 2(5):350–356

    PubMed  CAS  Google Scholar 

  • Rolland N, Job D, Douce R (1993) Common sequence motifs coding for higher-plant and prokaryotic O-acetylserine (thiol)-lyases: bacterial origin of a chloroplast transit peptide? Biochem J 293(Pt 3):829–833

    PubMed  CAS  Google Scholar 

  • Ruiz N, Kahne D, Silhavy T (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4(1):57–66

    PubMed  Google Scholar 

  • Ruprecht M, Bionda T, Sato T, Sommer MS, Endo T, Schleiff E (2010) On the impact of precursor unfolding during protein import into chloroplasts. Mol Plant 3(3):499–508

    PubMed  CAS  Google Scholar 

  • Rusch SL, Kendall DA (2007) Interactions that drive Sec-dependent bacterial protein transport. Biochemistry 46(34):9665–9673

    PubMed  CAS  Google Scholar 

  • Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I (2000) Structure of TPR domain-peptide complexes. Critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101(2):199–210

    PubMed  CAS  Google Scholar 

  • Schlegel T, Mirus O, von Haeseler A, Schleiff E (2007) The tetratricopeptide repeats of receptors involved in protein translocation across membranes. Mol Biol Evol 24(12):2763–2774

    PubMed  Google Scholar 

  • Schleiff E, Becker T (2011) Common ground for protein translocation. Access control for mitochondria and chloroplasts. Nat Rev Mol Cell Biol 12(1):48–59

    PubMed  CAS  Google Scholar 

  • Schleiff E, Soll J (2000) Travelling of proteins through membranes: translocation into chloroplasts. Planta 211(4):449–456

    PubMed  CAS  Google Scholar 

  • Schleiff E, Soll J (2005) Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep 6(11):1023–1027

    PubMed  CAS  Google Scholar 

  • Schleiff E, Eichacker LA, Eckart K, Becker T, Mirus O, Stahl T, Soll J (2003) Prediction of the plant beta-barrel proteome. A case study of the chloroplast outer envelope. Protein Sci 12(4):748–759

    PubMed  CAS  Google Scholar 

  • Schleiff E, Maier UG, Becker T (2011) Omp85 in eukaryotic systems: one protein family with distinct functions. Biol Chem 392(1–2):21–27

    PubMed  CAS  Google Scholar 

  • Schnell DJ, Kessler F, Blobel G (1994) Isolation of components of the chloroplast protein import machinery. Science 266(5187):1007–1012

    PubMed  CAS  Google Scholar 

  • Schwenkert S, Soll J, Bölter B (2011) Protein import into chloroplasts–how chaperones feature into the game. Biochim Biophys Acta 1808(3):901–911

    PubMed  CAS  Google Scholar 

  • Scott SV, Theg SM (1996) A new chloroplast protein import intermediate reveals distinct translocation machineries in the two envelope membranes: energetics and mechanistic implications. J Cell Biol 132(1–2):63–75

    PubMed  CAS  Google Scholar 

  • Shi L, Theg S (2010) A stromal heat shock protein 70 system functions in protein import into chloroplasts in the moss Physcomitrella patens. Plant Cell 22(1):205–220

    PubMed  CAS  Google Scholar 

  • Skalitzky CA, Martin JR, Harwood JH, Beirne JJ, Adamczyk BJ, Heck GR, Cline K, Fernandez DE (2011) Plastids contain a second sec translocase system with essential functions. Plant Physiol 155(1):354–369

    PubMed  CAS  Google Scholar 

  • Sklar JG, Wu T, Kahne D, Silhavy TJ (2007) Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 21(19):2473–2484

    PubMed  CAS  Google Scholar 

  • Sohrt K, Soll J (2000) Toc64, a new component of the protein translocon of chloroplasts. J Cell Biol 148(6):1213–1221

    PubMed  CAS  Google Scholar 

  • Soll J, Schleiff E (2004) Protein import into chloroplasts. Nat Rev Mol Cell Biol 5(3):198–208

    PubMed  CAS  Google Scholar 

  • Sommer MS, Schleiff E (2009) Molecular interactions within the plant TOC complex. Biol Chem 390(8):739–744

    PubMed  CAS  Google Scholar 

  • Sommer MS, Daum B, Gross LE, Weis BL, Mirus O, Abram L, Maier UG, Kühlbrandt W, Schleiff E (2011) Chloroplast Omp85 proteins change orientation during evolution. Proc Natl Acad Sci USA 108(33):13841–13846

    PubMed  CAS  Google Scholar 

  • Spence E, Sarcina M, Ray N, Møller SG, Mullineaux CW, Robinson C (2003) Membrane-specific targeting of green fluorescent protein by the Tat pathway in the cyanobacterium Synechocystis PCC6803. Mol Microbiol 48(6):1481–1489

    PubMed  CAS  Google Scholar 

  • Stahl T, Glockmann C, Soll J, Heins L (1999) Tic40, a new “old” subunit of the chloroplast protein import translocon. J Biol Chem 274(52):37467–37472

    PubMed  CAS  Google Scholar 

  • Stegemann S, Bock R (2006) Experimental reconstruction of functional gene transfer from the tobacco plastid genome to the nucleus. Plant Cell 18(11):2869–2878

    PubMed  CAS  Google Scholar 

  • Stegemann S, Hartmann S, Ruf S, Bock R (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci USA 100(15):8828–8833

    PubMed  CAS  Google Scholar 

  • Steiner JM, Löffelhardt W (2005) Protein translocation into and within cyanelles (Review). Mol Membr Biol 22(1–2):123–132

    PubMed  CAS  Google Scholar 

  • Steiner JM, Yusa F, Pompe JA, Löffelhardt W (2005) Homologous protein import machineries in chloroplasts and cyanelles. Plant J 44(4):646–652

    PubMed  CAS  Google Scholar 

  • Stirling PC, Bakhoum SF, Feigl AB, Leroux MR (2006) Convergent evolution of clamp-like binding sites in diverse chaperones. Nat Struct Mol Biol 13(10):865–870

    PubMed  CAS  Google Scholar 

  • Struyve M, Moons M, Tommassen J (1991) Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 218(1):141–148

    PubMed  CAS  Google Scholar 

  • Stymest KH, Klappa P (2008) The periplasmic peptidyl prolyl cis-trans isomerases PpiD and SurA have partially overlapping substrate specificities. FEBS J 275(13):3470–3479

    PubMed  CAS  Google Scholar 

  • Su PH, Li HM (2010) Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 22(5):1516–1531

    PubMed  CAS  Google Scholar 

  • Teng Y, Su Y, Chen L, Lee Y, Hwang I, Li H (2006) Tic21 is an essential translocon component for protein translocation across the chloroplast inner envelope membrane. Plant Cell 18(9):2247–2257

    PubMed  CAS  Google Scholar 

  • Tranel PJ, Keegstra K (1996) A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope. Plant Cell 8(11):2093–2104

    PubMed  CAS  Google Scholar 

  • Tranel PJ, Froehlich J, Goyal A, Keegstra K (1995) A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway. EMBO J 14(11):2436–2446

    PubMed  CAS  Google Scholar 

  • Tripp J, Hahn A, Koenig P, Flinner N, Bublak D, Brouwer EM, Ertel F, Mirus O, Sinning I, Tews I, Schleiff E (2012) Structure and conservation of the periplasmic targeting factor Tic22 protein from plants and cyanobacteria. J Biol Chem 287(29):24164–24173

    PubMed  CAS  Google Scholar 

  • Tsukazaki T, Mori H, Fukai S, Ishitani R, Mori T, Dohmae N, Perederina A, Sugita Y, Vassylyev DG, Ito K, Nureki O (2008) Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455(7215):988–991

    PubMed  CAS  Google Scholar 

  • Ullers RS, Luirink J, Harms N, Schwager F, Georgopoulos C, Genevaux P (2004) SecB is a bona fide generalized chaperone in Escherichia coli. Proc Natl Acad Sci USA 101(20):7583–7588

    PubMed  CAS  Google Scholar 

  • van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H, Satiat-Jeunemaitre B, Alunni B, Bourge M, Kucho KI, Abe M, Kereszt A, Maroti G, Uchiumi T, Kondorosi E, Mergaert P (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327(5969):1122–1126

    PubMed  Google Scholar 

  • van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6(6):525–530

    PubMed  Google Scholar 

  • van der Laan M, Nouwen NP, Driessen AJM (2005) YidC - an evolutionary conserved device for the assembly of energy-transducing membrane protein complexes. Curr Opin Microbiol 8(2):182–187

    PubMed  Google Scholar 

  • van Dooren GG, Schwartzbach SD, Osafune T, McFadden GI (2001) Translocation of proteins across the multiple membranes of complex plastids. Biochim Biophys Acta 1541(1–2):34–53

    PubMed  Google Scholar 

  • Verma DP, Hong Z (1996) Biogenesis of the peribacteroid membrane in root nodules. Trends Microbiol 4(9):364–368

    PubMed  CAS  Google Scholar 

  • Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N, von Heijne G, Grebe M, Bako L, Samuelsson G (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7(12):1224–1231

    PubMed  Google Scholar 

  • Vothknecht UC, Soll J (2005) Chloroplast membrane transport: interplay of prokaryotic and eukaryotic traits. Gene 354:99–109

    PubMed  CAS  Google Scholar 

  • Wolf DH, Stolz A (2012) The Cdc48 machine in endoplasmic reticulum associated protein degradation. Biochim Biophys Acta 1823(1):117–124

    PubMed  CAS  Google Scholar 

  • Wunder T, Martin R, Löffelhardt W, Schleiff E, Steiner JM (2007) The invariant phenylalanine of precursor proteins discloses the importance of Omp85 for protein translocation into cyanelles. BMC Evol Biol 7:236

    PubMed  Google Scholar 

  • Yusa F, Steiner JM, Löffelhardt W (2008) Evolutionary conservation of dual Sec translocases in the cyanelles of Cyanophora paradoxa. BMC Evol Biol 8:304

    PubMed  Google Scholar 

  • Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB (2001) The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proc Natl Acad Sci USA 98(23):13443–13448

    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(1):14–21

    PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to Stefan Simm, Oliver Mirus, Martina Königer, Andreas Weber, and Arndt von Haeseler for open and critical discussions concerning this issue. Special thanks to Jürgen Steiner, who gave insights into the Cyanophora paradoxa genome content prior to publication, which was essential for the description of the evolutionary scenario. The work was supported by grants from the Deutsche Forschungsgemeinschaft SFB807 and from the Volkswagenstiftung to ES.

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  1. Cluster of Excellence Macromolecular Complexes, Centre of Membrane Proteomics and Institute for Molecular Biosciences, Department of Biosciences, Molecular Cell Biology of Plants, Goethe University Frankfurt am Main, Max-von-Laue Str. 9, 60438, Frankfurt, Germany

    Maik S. Sommer & Enrico Schleiff

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  1. Maik S. Sommer
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  2. Enrico Schleiff
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Correspondence to Enrico Schleiff .

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  1. Department of Biochemistry, University of Vienna, Vienna, Austria

    Wolfgang Löffelhardt

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Sommer, M.S., Schleiff, E. (2014). Evolution of the Protein Translocons of the Chloroplast Envelope. In: Löffelhardt, W. (eds) Endosymbiosis. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1303-5_5

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