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The Ins and Outs of Chloroplast Protein Transport

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Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 36))

Summary

Much of the chloroplast proteome is encoded in the nuclear genome and needs to be imported post-translationally. Information for the organellar targeting of these imported proteins lies in an N-terminal leader sequence, the transit peptide, which is specifically bound by receptor components at the chloroplast surface. These receptor components are part of the TOC (translocon at the outer envelope membrane of chloroplasts) complex, which, together with the TIC (translocon at the inner envelope membrane of chloroplasts) machinery, mediates the translocation of precursor proteins into chloroplasts. Apart from the receptors, these complexes incorporate channel, motor and regulatory functions. Many components of this TOC/TIC apparatus have been identified. Multiple isoforms of the TOC receptors (and possibly of some other components) enable the operation of different import pathways with different substrate preferences, perhaps so that non-abundant proteins can be imported without serious competition from highly-abundant proteins of the photosynthetic apparatus. The different import pathways might also play a role in the differentiation of different plastid types. While much research has focused on these canonical TOC/TIC-mediated import routes, a number of studies have revealed alternative protein transport pathways to chloroplasts that employ different mechanisms; one of these passes through the endoplasmic reticulum and the Golgi apparatus. Other recent studies have revealed several protein targeting pathways leading to the envelope itself.

These authors contributed equally to the preparation of this chapter.

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Abbreviations

aaRS:

Aminoacyl-tRNA synthetase;

AKR2A:

Ankyrin repeat-containing protein 2A;

APG1:

Albino or pale green mutant 1;

BamA:

β-barrel assembly machinery A;

CAH1:

Carbonic anhydrase 1;

ceQORH:

Chloroplast envelope quinone oxidoreductase homologue;

CIA2 (-5):

Chloroplast import apparatus 2 (-5);

ClpC:

Caseinolytic protease, subunit C;

Com44/Cim44:

Chloroplast outer/inner membrane proteins, 44 kD;

Cpn60:

Chaperonin, 60 kD;

DEPC:

Diethylpyrocarbonate;

Fd:

Ferredoxin;

FNR:

Ferredoxin-NADP+ reductase;

GAP:

GTPase activating protein;

GEF:

Guanine nucleotide exchange factor;

Hip:

Hsp70-interacting protein;

Hop:

Hsp70/Hsp90-organizing protein;

Hsp70 (-93, -100):

Heat-shock protein, 70 kD (93 kD, 100 kD);

IDP:

Intrinsically disordered protein;

LHCII:

Light-harvesting complex protein of photosystem II;

MGD1:

Monogalactosyldiacylglycerol synthase 1;

OEP:

Outer envelope protein, kD;

PAGE:

Polyacrylamide gel electrophoresis;

PIC1:

Permease in chloroplasts 1;

POTRA:

Polypeptide transport associated;

ppi1 (-2, -3):

– Plastid protein import 1 (-2, -3);

PreP:

Presequence protease;

SAM (Sam):

Sorting and assembly machinery;

SP1 (sp1):

Suppressor of ppi1 locus 1;

SRP:

Signal recognition particle;

SSU (pSSU):

Rubisco small subunit (precursor of);

Sti1:

Stress-inducible 1;

Tat:

Twin-arginine translocase;

TIC (Tic):

Translocon at the inner envelope membrane of chloroplasts;

TIM (Tim):

Translocase of the inner mitochondrial membrane;

TOC (Toc):

Translocon at the outer envelope membrane of chloroplasts;

TOM (Tom):

Translocase of the outer mitochondrial membrane;

TPP:

Thylakoidal processing peptidase;

TPR:

Tetratricopeptide repeat;

TROL:

Thylakoid rhodanese-like protein;

VIPP1:

Vesicle-inducing protein in plastids 1

References

  • Abe Y, Shodai T, Muto T, Mihara K, Torii H, Nishikawa S, Endo T, Kohda D (2000) Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 100:551–560

    Article  PubMed  CAS  Google Scholar 

  • Agne B, Infanger S, Wang F, Hofstetter V, Rahim G, Martin M, Lee DW, Hwang I, Schnell D, Kessler F (2009) A Toc159 import receptor mutant, defective in hydrolysis of GTP, supports preprotein import into chloroplasts. J Biol Chem 284:8670–8679

    Article  PubMed  CAS  Google Scholar 

  • Agne B, Andres C, Montandon C, Christ B, Ertan A, Jung F, Infanger S, Bischof S, Baginsky S, Kessler F (2010) The acidic A-domain of Arabidopsis Toc159 occurs as a hyperphosphorylated protein. Plant Physiol 153:1016–1030

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Alte F, Stengel A, Benz JP, Petersen E, Soll J, Groll M, Bolter B (2010) Ferredoxin: NADPH oxidoreductase is recruited to thylakoids by binding to a polyproline type II helix in a pH-dependent manner. Proc Natl Acad Sci USA 107:19260–19265

    Article  PubMed  CAS  Google Scholar 

  • Andersson MX, Goksör M, Sandelius AS (2007) Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J Biol Chem 282:1170–1174

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Armbruster U, Hertle A, Makarenko E, Zuhlke J, Pribil M, Dietzmann A, Schliebner I, Aseeva E, Fenino E, Scharfenberg M, Voigt C, Leister D (2009) Chloroplast proteins without cleavable transit peptides: rare exceptions or a major constituent of the chloroplast proteome? Mol Plant 2:1325–1335

    Article  PubMed  CAS  Google Scholar 

  • Aronsson H, Jarvis P (2011) Dimerization of TOC ­rece­ptor GTPases and its implementation for the control of chloroplast protein import. Biochem J 436:e1–e2

    Article  PubMed  CAS  Google Scholar 

  • Aronsson H, Boij P, Patel R, Wardle A, Töpel M, Jarvis P (2007) Toc64/OEP64 is not essential for the efficient import of proteins into chloroplasts in Arabidopsis thaliana. Plant J 52:53–68

    Article  PubMed  CAS  Google Scholar 

  • Aronsson H, Combe J, Patel R, Agne B, Martin M, Kessler F, Jarvis P (2010) Nucleotide binding and dimerization at the chloroplast pre-protein import receptor, atToc33, are not essential in vivo but do increase import efficiency. Plant J 63:297–311

    Article  PubMed  CAS  Google Scholar 

  • Asatsuma S, Sawada C, Itoh K, Okito M, Kitajima A, Mitsui T (2005) Involvement of alpha-amylase I-1 in starch degradation in rice chloroplasts. Plant Cell Physiol 46:858–869

    Article  PubMed  CAS  Google Scholar 

  • Bae W, Lee YJ, 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 10:220–227

    Article  PubMed  CAS  Google Scholar 

  • Baldwin A, Wardle A, Patel R, Dudley P, Park SK, Twell D, Inoue K, Jarvis P (2005) A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiol 138:715–733

    Article  PubMed  CAS  Google Scholar 

  • Balsera M, Goetze TA, Kovács-Bogdán E, Schürmann P, Wagner R, Buchanan BB, Soll J, Bölter B (2009) Characterization of Tic110, a channel-forming protein at the inner envelope membrane of chloroplasts, unveils a response to Ca2+ and a stromal regulatory disulfide bridge. J Biol Chem 284:2603–2616

    Article  PubMed  CAS  Google Scholar 

  • Balsera M, Soll J, Buchanan BB (2010) Redox extends its regulatory reach to chloroplast protein import. Trends Plant Sci 15:515–521

    Article  PubMed  CAS  Google Scholar 

  • Bartsch S, Monnet J, Selbach K, Quigley F, Gray J, von Wettstein D, Reinbothe S, Reinbothe C (2008) Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism. Proc Natl Acad Sci USA 105:4933–4938

    Article  PubMed  CAS  Google Scholar 

  • Bauer J, Chen K, Hiltbrunner A, Wehrli E, Eugster M, Schnell D, Kessler F (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403:203–207

    Article  PubMed  CAS  Google Scholar 

  • Bauer J, Hiltbrunner A, Weibel P, Vidi PA, Alvarez-Huerta M, Smith MD, Schnell DJ, Kessler F (2002) Essential role of the G-domain in targeting of the protein import receptor atToc159 to the chloroplast outer membrane. J Cell Biol 159:845–854

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Becker T, Hritz J, Vogel M, Caliebe A, Bukau B, Soll J, Schleiff E (2004b) Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts. Mol Biol Cell 15:5130–5144

    Article  PubMed  CAS  Google Scholar 

  • Bédard J, Jarvis P (2005) Recognition and envelope translocation of chloroplast preproteins. J Exp Bot 56:2287–2320

    Article  PubMed  CAS  Google Scholar 

  • Bédard J, Jarvis P (2008) Green light for chloroplast outer-membrane proteins. Nat Cell Biol 10:120–122

    Article  PubMed  CAS  Google Scholar 

  • Bédard J, Kubis S, Bimanadham S, Jarvis P (2007) Functional similarity between the chloroplast translocon component, Tic40, and the human co-chaperone, Hsp70-interacting protein (Hip). J Biol Chem 282:21404–21414

    Article  PubMed  CAS  Google Scholar 

  • Benning C (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 25:71–91

    Article  PubMed  CAS  Google Scholar 

  • Benning C, Xu C, Awai K (2006) Non-vesicular and vesicular lipid trafficking involving plastids. Curr Opin Plant Biol 9:241–247

    Article  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, Bölter B (2009) Arabidopsis Tic62 and ferredoxin-NADP(H) oxidoreductase form light-regulated complexes that are integrated into the chloroplast redox poise. Plant Cell 21:3965–3983

    Article  PubMed  CAS  Google Scholar 

  • Berglund AK, Pujol C, Duchene AM, Glaser E (2009a) Defining the determinants for dual targeting of amino acyl-tRNA synthetases to mitochondria and chloroplasts. J Mol Biol 393:803–814

    Article  PubMed  CAS  Google Scholar 

  • Berglund AK, Spanning E, Biverstahl H, Maddalo G, Tellgren-Roth C, Maler L, Glaser E (2009b) Dual targeting to mitochondria and chloroplasts: characterization of Thr–tRNA synthetase targeting peptide. Mol Plant 2:1298–1309

    Article  PubMed  CAS  Google Scholar 

  • Bhushan S, Kuhn C, Berglund AK, Roth C, Glaser E (2006) The role of the N-terminal domain of chloroplast targeting peptides in organellar protein import and miss-sorting. FEBS Lett 580:3966–3972

    Article  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 402:510–523

    Article  PubMed  CAS  Google Scholar 

  • Block MA, Dorne AJ, Joyard J, Douce R (1983) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. I. Electrophoretic and immunochemical analyses. J Biol Chem 258:13273–13280

    PubMed  CAS  Google Scholar 

  • Boij P, Patel R, Garcia C, Jarvis P, Aronsson H (2009) In vivo studies on the roles of Tic55-related proteins in chloroplast protein import in Arabidopsis thaliana. Mol Plant 2:1397–1409

    Article  PubMed  CAS  Google Scholar 

  • Bölter B, May T, Soll J (1998) A protein import receptor in pea chloroplasts, Toc86, is only a proteolytic fragment of a larger polypeptide. FEBS Lett 441:59–62

    Article  PubMed  Google Scholar 

  • Bourne HR, Sanders DA, McCormick F (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349:117–127

    Article  PubMed  CAS  Google Scholar 

  • Brink S, Fischer K, Klösgen RB, Flügge UI (1995) Sorting of nuclear-encoded chloroplast membrane proteins to the envelope and the thylakoid membrane. J Biol Chem 270:20808–20815

    Article  PubMed  CAS  Google Scholar 

  • Brix J, Dietmeier K, Pfanner N (1997) Differential recognition of preproteins by the purified cytosolic domains of the mitochondrial import receptors Tom20, Tom22, and Tom70. J Biol Chem 272:20730–20735

    Article  PubMed  CAS  Google Scholar 

  • Bruce BD (1998) The role of lipids in plastid protein transport. Plant Mol Biol 38:223–246

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  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 16:7342–7350

    Article  PubMed  CAS  Google Scholar 

  • Carrie C, Giraud E, Whelan J (2009) Protein transport in organelles: dual targeting of proteins to mitochondria and chloroplasts. FEBS J 276:1187–1195

    Article  PubMed  CAS  Google Scholar 

  • Chen LJ, Li HM (1998) A mutant deficient in the plastid lipid DGD is defective in protein import into chloroplasts. Plant J 16:33–39

    Article  PubMed  Google Scholar 

  • Chen KY, Li HM (2007) Precursor binding to an 880-kDa Toc complex as an early step during active import of protein into chloroplasts. Plant J 49:149–158

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Schnell DJ (1997) Insertion of the 34-kDa chloroplast protein import component, IAP34, into the chloroplast outer membrane is dependent on its intrinsic GTP-binding capacity. J Biol Chem 272:6614–6620

    Article  PubMed  CAS  Google Scholar 

  • Chen K, Chen X, Schnell DJ (2000) Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts. Plant Physiol 122:813–822

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Smith MD, Fitzpatrick L, Schnell DJ (2002) In vivo analysis of the role of atTic20 in protein import into chloroplasts. Plant Cell 14:641–654

    Article  PubMed  CAS  Google Scholar 

  • Chen MH, Huang LF, Li HM, Chen YR, Yu SM (2004) Signal peptide-dependent targeting of a rice alpha-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiol 135:1367–1377

    Article  PubMed  CAS  Google Scholar 

  • Chew O, Whelan J (2004) Just read the message: a model for sorting of proteins between mitochondria and chloroplasts. Trends Plant Sci 9:318–319

    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 

  • Chigri F, Soll J, Vothknecht UC (2005) Calcium regulation of chloroplast protein import. Plant J 42:821–831

    Article  PubMed  CAS  Google Scholar 

  • Chigri F, Hörmann F, Stamp A, Stammers DK, Bölter B, Soll J, Vothknecht UC (2006) Calcium regulation of chloroplast protein translocation is mediated by calmodulin binding to Tic32. Proc Natl Acad Sci USA 103:16051–16056

    Article  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 56:793–801

    Article  PubMed  CAS  Google Scholar 

  • Chiu CC, Chen LJ, Li HM (2011) Pea chloroplast DnaJ-J8 and Toc12 are encoded by the same gene and localized in the stroma. Plant Physiol 154:1172–1182

    Article  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 22:2970–2980

    Article  PubMed  CAS  Google Scholar 

  • Chou ML, Chu CC, Chen LJ, Akita M, Li HM (2006) Stimulation of transit-peptide release and ATP hydrolysis by a cochaperone during protein import into chloroplasts. J Cell Biol 175:893–900

    Article  PubMed  CAS  Google Scholar 

  • Cleary SP, Tan FC, Nakrieko KA, Thompson SJ, Mullineaux PM, Creissen GP, von Stedingk E, Glaser E, Smith AG, Robinson C (2002) Isolated plant mitochondria import chloroplast precursor proteins in vitro with the same efficiency as chloroplasts. J Biol Chem 277:5562–5569

    Article  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 11:585–592

    Article  PubMed  CAS  Google Scholar 

  • Cline K, Werner-Washburne M, Andrews J, Keegstra K (1984) Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiol 75:675–678

    Article  PubMed  CAS  Google Scholar 

  • Cline K, Werner-Washburne M, Lubben TH, Keegstra K (1985) Precursors to two nuclear-encoded chloroplast proteins bind to the outer envelope membrane before being imported into chloroplasts. J Biol Chem 260:3691–3696

    PubMed  CAS  Google Scholar 

  • Constan D, Patel R, Keegstra K, Jarvis P (2004a) An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J 38:93–106

    Article  PubMed  CAS  Google Scholar 

  • Constan D, Froehlich JE, Rangarajan S, Keegstra K (2004b) A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiol 136:3605–3615

    Article  PubMed  CAS  Google Scholar 

  • Crotty WJ, Ledbetter MC (1973) Membrane continuities involving chloroplasts and other organelles in plant cells. Science 182:839–841

    Article  PubMed  CAS  Google Scholar 

  • Dabney-Smith C, van Den Wijngaard PW, Treece Y, Vredenberg WJ, Bruce BD (1999) The C terminus of a chloroplast precursor modulates its interaction with the translocation apparatus and PIRAC. J Biol Chem 274:32351–32359

    Article  PubMed  CAS  Google Scholar 

  • Dahlin C, Cline K (1991) Developmental regulation of the plastid protein import apparatus. Plant Cell 3:1131–1140

    PubMed  CAS  Google Scholar 

  • Dhanoa PK, Richardson LG, Smith MD, Gidda SK, Henderson MP, Andrews DW, Mullen RT (2010) Distinct pathways mediate the sorting of tail-anchored proteins to the plastid outer envelope. PLoS One 5:e10098

    Article  PubMed  CAS  Google Scholar 

  • Duchêne AM, Giritch A, Hoffmann B, Cognat V, Lancelin D, Peeters NM, Zaepfel M, Marechal-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

    Article  PubMed  CAS  Google Scholar 

  • Dutta S, Mohanty S, Tripathy BC (2009) Role of temperature stress on chloroplast biogenesis and protein import in pea. Plant Physiol 150:1050–1061

    Article  PubMed  CAS  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 19:986–1006

    Article  PubMed  CAS  Google Scholar 

  • Duy D, Stube R, Wanner G, Philippar K (2011) The chloroplast permease PIC1 regulates plant growth and development by directing homeostasis and transport of iron. Plant Physiol 155:1709–1722

    Article  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 3:557–562

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971

    Article  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 280:28281–28289

    Article  PubMed  CAS  Google Scholar 

  • Ferro M, Salvi D, Brugiere S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2:325–345

    PubMed  CAS  Google Scholar 

  • Friedman AL, Keegstra K (1989) Chloroplast protein import: quantitative analysis of precursor binding. Plant Physiol 89:993–999

    Article  PubMed  CAS  Google Scholar 

  • Gaikwad A, Tewari KK, Kumar D, Chen W, Mukherjee SK (1999) Isolation and characterisation of the cDNA encoding a glycosylated accessory protein of pea chloroplast DNA polymerase. Nucleic Acids Res 27:3120–3129

    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 

  • Glover JR, Tkach JM (2001) Crowbars and ratchets: Hsp100 chaperones as tools in reversing protein aggregation. Biochem Cell Biol 79:557–568

    Article  PubMed  CAS  Google Scholar 

  • Gokirmak T, Paul AL, Ferl RJ (2010) Plant phosphopeptide-binding proteins as signaling mediators. Curr Opin Plant Biol 13:527–532

    Article  PubMed  CAS  Google Scholar 

  • Gross J, Bhattacharya D (2009) Revaluating the evolution of the Toc and Tic protein translocons. Trends Plant Sci 14:13–20

    Article  PubMed  CAS  Google Scholar 

  • Gutensohn M, Schulz B, Nicolay P, Flügge UI (2000) Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. Plant J 23:771–783

    Article  PubMed  CAS  Google Scholar 

  • Gutensohn M, Pahnke S, Kolukisaoglu U, Schulz B, Schierhorn A, Voigt A, Hust B, Rollwitz I, Stockel J, Geimer S, Albrecht V, Flügge UI, Klösgen RB (2004) Characterization of a T–DNA insertion mutant for the protein import receptor atToc33 from chloroplasts. Mol Genet Genomics 272:379–396

    Article  PubMed  CAS  Google Scholar 

  • Gutensohn M, Fan E, Frielingsdorf S, Hanner P, Hou B, Hust B, Klösgen RB (2006) Toc, Tic, Tat et al.: structure and function of protein transport machineries in chloroplasts. J Plant Physiol 163:333–347

    Article  PubMed  CAS  Google Scholar 

  • Haas BJ, Wortman JR, Ronning CM, Hannick LI, Smith RK Jr, Maiti R, Chan AP, Yu C, Farzad M, Wu D, White O, Town CD (2005) Complete reannotation of the Arabidopsis genome: methods, tools, protocols and the final release. BMC Biol 3:7

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hiltbrunner A, Bauer J, Vidi PA, Infanger S, Weibel P, Hohwy M, Kessler F (2001) Targeting of an abundant cytosolic form of the protein import receptor at Toc159 to the outer chloroplast membrane. J Cell Biol 154:309–316

    Article  PubMed  CAS  Google Scholar 

  • Hiltbrunner A, Grunig K, Alvarez-Huerta M, Infanger S, Bauer J, Kessler F (2004) AtToc90, a new GTP-binding component of the Arabidopsis chloroplast protein import machinery. Plant Mol Biol 54:427–440

    Article  PubMed  CAS  Google Scholar 

  • Hines V, Brandt A, Griffiths G, Horstmann H, Brutsch H, Schatz G (1990) Protein import into yeast mitochondria is accelerated by the outer membrane protein MAS70. EMBO J 9:3191–3200

    PubMed  CAS  Google Scholar 

  • Hinnah SC, Hill K, Wagner R, Schlicher T, Soll J (1997) Reconstitution of a chloroplast protein import channel. EMBO J 16:7351–7360

    Article  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 83:899–911

    Article  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 52:469–478

    Article  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 125:2154–2163

    Article  PubMed  CAS  Google Scholar 

  • Hirsch S, Muckel E, Heemeyer F, von Heijne G, Soll J (1994) A receptor component of the chloroplast protein translocation machinery. Science 266:1989–1992

    Article  PubMed  CAS  Google Scholar 

  • Hofmann NR, Theg SM (2005a) Protein- and energy-mediated targeting of chloroplast outer envelope membrane proteins. Plant J 44:917–927

    Article  PubMed  CAS  Google Scholar 

  • Hofmann NR, Theg SM (2005b) Toc64 is not required for import of proteins into chloroplasts in the moss Physcomitrella patens. Plant J 43:675–687

    Article  CAS  Google Scholar 

  • Hofmann NR, Theg SM (2005c) Chloroplast outer membrane protein targeting and insertion. Trends Plant Sci 10:450–457

    Article  PubMed  CAS  Google Scholar 

  • Hörmann F, Küchler M, Sveshnikov D, Oppermann U, Li Y, Soll J (2004) Tic32, an essential component in chloroplast biogenesis. J Biol Chem 279:34756–34762

    Article  PubMed  CAS  Google Scholar 

  • Hsu SC, Inoue K (2009) Two evolutionarily conserved essential beta-barrel proteins in the chloroplast outer envelope membrane. Biosci Trends 3:168–178

    PubMed  CAS  Google Scholar 

  • Huang W, Ling Q, Bédard 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 157:147–159

    Article  PubMed  CAS  Google Scholar 

  • Hust B, Gutensohn M (2006) Deletion of core components of the plastid protein import machinery causes differential arrest of embryo development in Arabidopsis thaliana. Plant Biol (Stuttg) 8:18–30

    Article  CAS  Google Scholar 

  • Inaba T, Schnell DJ (2008) Protein trafficking to plastids: one theme, many variations. Biochem J 413:15–28

    Article  PubMed  CAS  Google Scholar 

  • Inaba T, Li M, Alvarez-Huerta M, Kessler F, Schnell DJ (2003) atTic110 functions as a scaffold for coordinating the stromal events of protein import into chloroplasts. J Biol Chem 278:38617–38627

    Article  PubMed  CAS  Google Scholar 

  • Inaba T, Alvarez-Huerta M, Li M, Bauer J, Ewers C, Kessler F, Schnell DJ (2005) Arabidopsis Tic110 is essential for the assembly and function of the protein import machinery of plastids. Plant Cell 17:1482–1496

    Article  PubMed  CAS  Google Scholar 

  • Infanger S, Bischof S, Hiltbrunner A, Agne B, Baginsky S, Kessler F (2010) The chloroplast import receptor Toc90 partially restores the accumulation of Toc159 client proteins in the Arabidopsis thaliana pp i2 mutant. Mol Plant 4:252–263

    Article  CAS  Google Scholar 

  • Inoue H, Akita M (2008) Three sets of translocation intermediates are formed during the early stage of protein import into chloroplasts. J Biol Chem 283:7491–7502

    Article  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 34:661–669

    Article  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 39:354–365

    Article  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 171:425–430

    Article  PubMed  CAS  Google Scholar 

  • Inoue H, Rounds C, Schnell DJ (2010) The molecular basis for distinct pathways for protein import into Arabidopsis chloroplasts. Plant Cell 22:1947–1960

    Article  PubMed  CAS  Google Scholar 

  • Ivanova Y, Smith MD, Chen K, Schnell DJ (2004) Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol Biol Cell 15:3379–3392

    Article  PubMed  CAS  Google Scholar 

  • Ivey RA 3rd, Subramanian C, Bruce BD (2000) Identification of a Hsp70 recognition domain within the rubisco small subunit transit peptide. Plant Physiol 122:1289–1299

    Article  PubMed  CAS  Google Scholar 

  • Jackson DT, Froehlich JE, Keegstra K (1998) The hydrophilic domain of Tic110, an inner envelope membrane component of the chloroplastic protein translocation apparatus, faces the stromal compartment. J Biol Chem 273:16583–16588

    Article  PubMed  CAS  Google Scholar 

  • Jackson-Constan D, Keegstra K (2001) Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol 125:1567–1576

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jarvis P, Robinson C (2004) Mechanisms of protein import and routing in chloroplasts. Curr Biol 14:R1064–R1077

    Article  PubMed  CAS  Google Scholar 

  • Jarvis P, Chen LJ, Li H, Peto CA, Fankhauser C, Chory J (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282:100–103

    Article  PubMed  CAS  Google Scholar 

  • Jelic M, Sveshnikova N, Motzkus M, Horth P, Soll J, Schleiff E (2002) The chloroplast import receptor Toc34 functions as preprotein-regulated GTPase. Biol Chem 383:1875–1883

    Article  PubMed  CAS  Google Scholar 

  • Jelic M, Soll J, Schleiff E (2003) Two Toc34 homologues with different properties. Biochemistry 42:5906–5916

    Article  PubMed  CAS  Google Scholar 

  • Jouhet J, Gray JC (2009a) Interaction of actin and the chloroplast protein import apparatus. J Biol Chem 284:19132–19141

    Article  PubMed  CAS  Google Scholar 

  • Jouhet J, Gray JC (2009b) Is chloroplast import of photosynthesis proteins facilitated by an actin–TOC-TIC-VIPP1 complex? Plant Signal Behav 4:986–988

    Article  PubMed  CAS  Google Scholar 

  • Juric S, Hazler-Pilepic K, Tomasic A, Lepedus H, Jelicic B, Puthiyaveetil S, Bionda T, Vojta L, Allen JF, Schleiff E, Fulgosi H (2009) Tethering of ferredoxin: NADP+ oxidoreductase to thylakoid membranes is mediated by novel chloroplast protein TROL. Plant J 60:783–794

    Article  PubMed  CAS  Google Scholar 

  • Kakizaki T, Matsumura H, Nakayama K, Che FS, Terauchi R, Inaba T (2009) Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiol 151:1339–1353

    Article  PubMed  CAS  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 179:95–112

    Article  PubMed  CAS  Google Scholar 

  • Kasmati AR, Töpel M, Patel R, Murtaza G, Jarvis P (2011) Molecular and genetic analyses of Tic20 homologues in Arabidopsis thaliana chloroplasts. Plant J 66:877–889

    Article  PubMed  CAS  Google Scholar 

  • Keegstra K, Cline K (1999) Protein import and routing systems of chloroplasts. Plant Cell 11:557–570

    PubMed  CAS  Google Scholar 

  • Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B Biol Sci 365:729–748

    Article  PubMed  CAS  Google Scholar 

  • Keenan RJ, Freymann DM, Stroud RM, Walter P (2001) The signal recognition particle. Annu Rev Biochem 70:755–775

    Article  PubMed  CAS  Google Scholar 

  • Kessler F, Blobel G (1996) Interaction of the protein import and folding machineries of the chloroplast. Proc Natl Acad Sci USA 93:7684–7689

    Article  PubMed  CAS  Google Scholar 

  • Kessler F, Schnell DJ (2006) The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids. Traffic 7:248–257

    Article  PubMed  CAS  Google Scholar 

  • Kessler F, Blobel G, Patel HA, Schnell DJ (1994) Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 266:1035–1039

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi S, Hirohashi T, Nakai M (2006) Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE. Plant Cell Physiol 47:363–371

    Article  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 21:1781–1797

    Article  PubMed  CAS  Google Scholar 

  • Kitajima A, Asatsuma S, Okada H, Hamada Y, Kaneko K, Nanjo Y, Kawagoe Y, Toyooka K, Matsuoka K, Takeuchi M, Nakano A, Mitsui T (2009) The rice alpha-amylase glycoprotein is targeted from the Golgi apparatus through the secretory pathway to the plastids. Plant Cell 21:2844–2858

    Article  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 14:354–362

    Article  PubMed  CAS  Google Scholar 

  • Knight JS, Gray JC (1995) The N-terminal hydrophobic region of the mature phosphate translocator is sufficient for targeting to the chloroplast inner envelope membrane. Plant Cell 7:1421–1432

    PubMed  CAS  Google Scholar 

  • Koenig P, Oreb M, Hofle A, Kaltofen S, Rippe K, Sinning I, Schleiff E, Tews I (2008) The GTPase cycle of the chloroplast import receptors Toc33/Toc34: implications from monomeric and dimeric structures. Structure 16:585–596

    Article  PubMed  CAS  Google Scholar 

  • Kouranov A, Schnell DJ (1997) Analysis of the interactions of preproteins with the import machinery over the course of protein import into chloroplasts. J Cell Biol 139:1677–1685

    Article  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 143:991–1002

    Article  PubMed  CAS  Google Scholar 

  • Kouranov A, Wang H, Schnell DJ (1999) Tic22 is targeted to the intermembrane space of chloroplasts by a novel pathway. J Biol Chem 274:25181–25186

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kovacheva S, Bédard 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 50:364–379

    Article  PubMed  CAS  Google Scholar 

  • Kovacs-Bogdan E, Soll J, Bölter B (2010) Protein import into chloroplasts: the Tic complex and its regulation. Biochim Biophys Acta 1803:740–747

    Article  PubMed  CAS  Google Scholar 

  • Krause K, Krupinska K (2009) Nuclear regulators with a second home in organelles. Trends Plant Sci 14:194–199

    Article  PubMed  CAS  Google Scholar 

  • Kriechbaumer V, von Loffelholz O, Abell BM (2011) Chaperone receptors: guiding proteins to intracellular compartments. Protoplasma 249:21–30

    Google Scholar 

  • Krimm I, Gans P, Hernandez JF, Arlaud GJ, Lancelin JM (1999) A coil-helix instead of a helix-coil motif can be induced in a chloroplast transit peptide from Chlamydomonas reinhardtii. Eur J Biochem 265:171–180

    Article  PubMed  CAS  Google Scholar 

  • Kubis S, Baldwin A, Patel R, Razzaq A, Dupree P, Lilley K, Kurth J, Leister D, Jarvis P (2003) The Arabidopsis pp i1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. Plant Cell 15:1859–1871

    Article  PubMed  CAS  Google Scholar 

  • Kubis S, Patel R, Combe J, Bédard J, Kovacheva S, Lilley K, Biehl A, Leister D, Ríos G, Koncz C, Jarvis P (2004) Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16:2059–2077

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Larkum AW, Lockhart PJ, Howe CJ (2007) Shopping for plastids. Trends Plant Sci 12:189–195

    Article  PubMed  CAS  Google Scholar 

  • Lee YJ, Kim DH, Kim YW, Hwang I (2001) Identification of a signal that distinguishes between the chloroplast outer envelope membrane and the endomembrane system in vivo. Plant Cell 13:2175–2190

    PubMed  CAS  Google Scholar 

  • Lee KH, Kim DH, Lee SW, Kim ZH, Hwang I (2002) In vivo import experiments in protoplasts reveal the importance of the overall context but not specific amino acid residues of the transit peptide during import into chloroplasts. Mol Cells 14:388–397

    PubMed  CAS  Google Scholar 

  • Lee KH, Kim SJ, Lee YJ, Jin JB, Hwang I (2003) The M domain of atToc159 plays an essential role in the import of proteins into chloroplasts and chloroplast biogenesis. J Biol Chem 278:36794–36805

    Article  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 140:466–483

    Article  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 20:1603–1622

    Article  PubMed  CAS  Google Scholar 

  • Lee DW, Lee S, Oh YJ, Hwang I (2009a) Multiple sequence motifs in the rubisco small subunit transit peptide independently contribute to Toc159-dependent import of proteins into chloroplasts. Plant Physiol 151:129–141

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Wang F, Schnell DJ (2009b) Toc receptor dimerization participates in the initiation of membrane translocation during protein import into chloroplasts. J Biol Chem 284:31130–31141

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Lee DW, Lee Y, Mayer U, Stierhof YD, Jurgens G, Hwang I (2009c) 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 21:3984–4001

    Article  PubMed  CAS  Google Scholar 

  • Leheny EA, Theg SM (1994) Apparent inhibition of chloroplast protein import by cold temperatures is due to energetic considerations not membrane fluidity. Plant Cell 6:427–437

    PubMed  CAS  Google Scholar 

  • Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19:47–56

    Article  PubMed  CAS  Google Scholar 

  • Levitan A, Trebitsh T, Kiss V, Pereg Y, Dangoor I, Danon A (2005) Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum. Proc Natl Acad Sci USA 102:6225–6230

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ling Q, Huang W, Baldwin A, Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system. Science 338:655–659

    Article  PubMed  CAS  Google Scholar 

  • Lister R, Carrie C, Duncan O, Ho LH, Howell KA, Murcha MW, Whelan J (2007) Functional definition of outer membrane proteins involved in preprotein import into mitochondria. Plant Cell 19:3739–3759

    Article  PubMed  CAS  Google Scholar 

  • López-Juez E (2007) Plastid biogenesis, between light and shadows. J Exp Bot 58:11–26

    Article  PubMed  CAS  Google Scholar 

  • López-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49:557–577

    Article  PubMed  CAS  Google Scholar 

  • Lübeck 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 15:4230–4238

    PubMed  Google Scholar 

  • Lübeck 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 137:1279–1286

    Article  PubMed  Google Scholar 

  • Ma Y, Kouranov A, LaSala SE, Schnell DJ (1996) Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and translocation of precursor proteins at the outer envelope. J Cell Biol 134:315–327

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Mackenzie SA (2005) Plant organellar protein targeting: a traffic plan still under construction. Trends Cell Biol 15:548–554

    Article  PubMed  CAS  Google Scholar 

  • Madueño F, Napier JA, Gray JC (1993) Newly imported Rieske iron-sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma. Plant Cell 5:1865–1876

    PubMed  Google Scholar 

  • Marc P, Margeot A, Devaux F, Blugeon C, Corral-Debrinski M, Jacq C (2002) Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep 3:159–164

    Article  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 87:374–378

    Article  PubMed  CAS  Google Scholar 

  • Martin W (2010) Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B 365:847–855

    Article  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 99:12246–12251

    Article  PubMed  CAS  Google Scholar 

  • Mata-Cabana A, Florencio FJ, Lindahl M (2007) Membrane proteins from the cyanobacterium Synechocystis sp. PCC 6803 interacting with thioredoxin. Proteomics 7:3953–3963

    Article  PubMed  CAS  Google Scholar 

  • May T, Soll J (2000) 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12:53–64

    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 277:47770–47778

    Article  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 282:29482–29492

    Article  PubMed  CAS  Google Scholar 

  • Mitschke J, Fuss J, Blum T, Hoglund A, Reski R, Kohlbacher O, Rensing SA (2009) Prediction of dual protein targeting to plant organelles. New Phytol 183:224–235

    Article  PubMed  CAS  Google Scholar 

  • Moberg P, Stahl A, Bhushan S, Wright SJ, Eriksson A, Bruce BD, Glaser E (2003) Characterization of a novel zinc metalloprotease involved in degrading targeting peptides in mitochondria and chloroplasts. Plant J 36:616–628

    Article  PubMed  CAS  Google Scholar 

  • Nada A, Soll J (2004) Inner envelope protein 32 is imported into chloroplasts by a novel pathway. J Cell Sci 117:3975–3982

    Article  PubMed  CAS  Google Scholar 

  • Nakai K, Horton P (2007) Computational prediction of subcellular localization. Methods Mol Biol 390:429–466

    Article  PubMed  CAS  Google Scholar 

  • Nakrieko KA, Mould RM, Smith AG (2004) Fidelity of targeting to chloroplasts is not affected by removal of the phosphorylation site from the transit peptide. Eur J Biochem 271:509–516

    Article  PubMed  CAS  Google Scholar 

  • Nanjo Y, Oka H, Ikarashi N, Kaneko K, Kitajima A, Mitsui T, Muñoz FJ, Rodríguez-López M, Baroja-Fernández E, Pozueta-Romero J (2006) Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-golgi to the chloroplast through the secretory pathway. Plant Cell 18:2582–2592

    Article  PubMed  CAS  Google Scholar 

  • Nassoury N, Morse D (2005) Protein targeting to the chloroplasts of photosynthetic eukaryotes: getting there is half the fun. Biochim Biophys Acta 1743:5–19

    Article  PubMed  CAS  Google Scholar 

  • Nelson N, Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5:971–982

    Article  PubMed  CAS  Google Scholar 

  • Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 51:111–140

    Article  PubMed  CAS  Google Scholar 

  • Neupert W, Brunner M (2002) The protein import motor of mitochondria. Nat Rev Mol Cell Biol 3:555–565

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997b) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6

    Article  PubMed  CAS  Google Scholar 

  • Olsen LJ, Keegstra K (1992) The binding of precursor proteins to chloroplasts requires nucleoside triphosphates in the intermembrane space. J Biol Chem 267:433–439

    PubMed  CAS  Google Scholar 

  • Olsen LJ, Theg SM, Selman BR, Keegstra K (1989) ATP is required for the binding of precursor proteins to chloroplasts. J Biol Chem 264:6724–6729

    PubMed  CAS  Google Scholar 

  • Oreb M, Hofle A, Koenig P, Sommer MS, Sinning I, Wang F, Tews I, Schnell D, Schleiff E (2011) Substrate binding disrupts dimerization and induces nucleotide exchange of the chloroplast GTPase Toc33. Biochem J 436:313–319

    Article  PubMed  CAS  Google Scholar 

  • Pain D, Blobel G (1987) Protein import into chloroplasts requires a chloroplast ATPase. Proc Natl Acad Sci USA 84:3288–3292

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Peeters N, Small I (2001) Dual targeting to mitochondria and chloroplasts. Biochim Biophys Acta 1541:54–63

    Article  PubMed  CAS  Google Scholar 

  • Perry SE, Keegstra K (1994) Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 6:93–105

    PubMed  CAS  Google Scholar 

  • Pilon M, de Kruijff B, Weisbeek PJ (1992) New insights into the import mechanism of the ferredoxin precursor into chloroplasts. J Biol Chem 267:2548–2556

    PubMed  CAS  Google Scholar 

  • Pilon M, Wienk H, Sips W, de Swaaf M, Talboom I, Van’t Hof R, de Korte-Kool G, Demel R, Weisbeek P, de Kruijff B (1995) Functional domains of the ferredoxin transit sequence involved in chloroplast import. J Biol Chem 270:3882–3893

    Article  PubMed  CAS  Google Scholar 

  • Pollmann S, Neu D, Weiler EW (2003) Molecular cloning and characterization of an amidase from Arabidopsis thaliana capable of converting indole-3-acetamide into the plant growth hormone, indole-3-acetic acid. Phytochemistry 62:293–300

    Article  PubMed  CAS  Google Scholar 

  • Pollmann S, Neu D, Lehmann T, Berkowitz O, Schafer T, Weiler EW (2006) Subcellular localization and tissue specific expression of amidase 1 from Arabidopsis thaliana. Planta 224:1241–1253

    Article  PubMed  CAS  Google Scholar 

  • Pujol C, Marechal-Drouard L, Duchene 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

    Article  PubMed  CAS  Google Scholar 

  • Qbadou S, Tien R, Soll J, Schleiff E (2003) Membrane insertion of the chloroplast outer envelope protein, Toc34: constrains for insertion and topology. J Cell Sci 116:837–846

    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 

  • 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 367:1330–1346

    Article  PubMed  CAS  Google Scholar 

  • Radhamony RN, Theg SM (2006) Evidence for an ER to Golgi to chloroplast protein transport pathway. Trends Cell Biol 16:385–387

    Article  PubMed  CAS  Google Scholar 

  • Rahim G, Bischof S, Kessler F, Agne B (2009) In vivo interaction between atToc33 and atToc159 GTP-binding domains demonstrated in a plant split-ubiquitin system. J Exp Bot 60:257–267

    Article  PubMed  CAS  Google Scholar 

  • Rapaport D (2005) How does the TOM complex mediate insertion of precursor proteins into the mitochondrial outer membrane? J Cell Biol 171:419–423

    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 

  • Ratnayake RM, Inoue H, Nonami H, Akita M (2008) Alternative processing of Arabidopsis Hsp70 precursors during protein import into chloroplasts. Biosci Biotechnol Biochem 72:2926–2935

    Article  PubMed  CAS  Google Scholar 

  • Reddick LE, Vaughn MD, Wright SJ, Campbell IM, Bruce BD (2007) In vitro comparative kinetic analysis of the chloroplast Toc GTPases. J Biol Chem 282:11410–11426

    Article  PubMed  CAS  Google Scholar 

  • Reiss B, Wasmann CC, Schell J, Bohnert HJ (1989) Effect of mutations on the binding and translocation functions of a chloroplast transit peptide. Proc Natl Acad Sci USA 86:886–890

    Article  PubMed  CAS  Google Scholar 

  • Rensink WA, Pilon M, Weisbeek P (1998) Domains of a transit sequence required for in vivo import in Arabidopsis chloroplasts. Plant Physiol 118:691–699

    Article  PubMed  CAS  Google Scholar 

  • Rensink WA, Schnell DJ, Weisbeek PJ (2000) The transit sequence of ferredoxin contains different domains for translocation across the outer and inner membrane of the chloroplast envelope. J Biol Chem 275:10265–10271

    Article  PubMed  CAS  Google Scholar 

  • Reumann S, Keegstra K (1999) The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci 4:302–307

    Article  PubMed  Google Scholar 

  • Reumann S, Inoue K, Keegstra K (2005) Evolution of the general protein import pathway of plastids. Mol Membr Biol 22:73–86

    Article  PubMed  CAS  Google Scholar 

  • Reyes-Prieto A, Weber AP, Bhattacharya D (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41:147–168

    Article  PubMed  CAS  Google Scholar 

  • Rial DV, Arakaki AK, Ceccarelli EA (2000) Interaction of the targeting sequence of chloroplast precursors with Hsp70 molecular chaperones. Eur J Biochem 267:6239–6248

    Article  PubMed  CAS  Google Scholar 

  • Rial DV, Lombardo VA, Ceccarelli EA, Ottado J (2002) The import of ferredoxin-NADP+ reductase precursor into chloroplasts is modulated by the region between the transit peptide and the mature core of the protein. Eur J Biochem 269:5431–5439

    Article  PubMed  CAS  Google Scholar 

  • Richardson LG, 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

    Article  PubMed  CAS  Google Scholar 

  • Richly E, Leister D (2004) An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329:11–16

    Article  PubMed  CAS  Google Scholar 

  • Richter S, Lamppa GK (1998) A chloroplast processing enzyme functions as the general stromal processing peptidase. Proc Natl Acad Sci USA 95:7463–7468

    Article  PubMed  CAS  Google Scholar 

  • Richter S, Lamppa GK (2002) Determinants for removal and degradation of transit peptides of chloroplast precursor proteins. J Biol Chem 277:43888–43894

    Article  PubMed  CAS  Google Scholar 

  • Richter S, Lamppa GK (2003) Structural properties of the chloroplast stromal processing peptidase required for its function in transit peptide removal. J Biol Chem 278:39497–39502

    Article  PubMed  CAS  Google Scholar 

  • Richter S, Zhong R, Lamppa G (2005) Function of the stromal processing peptidase in the chloroplast import pathway. Physiol Plant 123:362–368

    Article  CAS  Google Scholar 

  • Ross JL, Ali MY, Warshaw DM (2008) Cargo transport: molecular motors navigate a complex cytoskeleton. Curr Opin Cell Biol 20:41–47

    Article  PubMed  CAS  Google Scholar 

  • Row PE, Gray JC (2001) The effect of amino acid-modifying reagents on chloroplast protein import and the formation of early import intermediates. J Exp Bot 52:57–66

    Article  PubMed  CAS  Google Scholar 

  • Rudhe C, Clifton R, Chew O, Zemam K, Richter S, Lamppa G, Whelan J, Glaser E (2004) Processing of the dual targeted precursor protein of glutathione reductase in mitochondria and chloroplasts. J Mol Biol 343:639–647

    Article  PubMed  CAS  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 3:499–508

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Pulido L, Devos D, Genevrois S, Vicente M, Valencia A (2003) POTRA: a conserved domain in the FtsQ family and a class of beta-barrel outer membrane proteins. Trends Biochem Sci 28:523–526

    Article  PubMed  CAS  Google Scholar 

  • Sapir-Mir M, Mett A, Belausov E, Tal-Meshulam S, Frydman A, Gidoni D, Eyal Y (2008) Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol 148:1219–1228

    Article  PubMed  CAS  Google Scholar 

  • Schirmer EC, Glover JR, Singer MA, Lindquist S (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21:289–296

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Schleiff E, Motzkus M, Soll J (2002) Chloroplast protein import inhibition by a soluble factor from wheat germ lysate. Plant Mol Biol 50:177–185

    Article  PubMed  CAS  Google Scholar 

  • Schleiff E, Jelic M, Soll J (2003a) A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proc Natl Acad Sci USA 100:4604–4609

    Article  PubMed  CAS  Google Scholar 

  • Schleiff E, Soll J, Küchler M, Kuhlbrandt W, Harrer R (2003b) Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol 160:541–551

    Article  PubMed  CAS  Google Scholar 

  • Schmidt O, Pfanner N, Meisinger C (2010) Mitochondrial protein import: from proteomics to functional mechanisms. Nat Rev Mol Cell Biol 11:655–667

    Article  PubMed  CAS  Google Scholar 

  • Schnell DJ, Blobel G (1993) Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites. J Cell Biol 120:103–115

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Schnell DJ, Blobel G, Keegstra K, Kessler F, Ko K, Soll J (1997) A consensus nomenclature for the protein-import components of the chloroplast envelope. Trends Cell Biol 7:303–304

    Article  PubMed  CAS  Google Scholar 

  • Schreier PH, Seftor EA, Schell J, Bohnert HJ (1985) The use of nuclear-encoded sequences to direct the light-regulated synthesis and transport of a foreign protein into plant chloroplasts. EMBO J 4:25–32

    PubMed  CAS  Google Scholar 

  • Schünemann D (2007) Mechanisms of protein import into thylakoids of chloroplasts. Biol Chem 388:907–915

    Article  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 132:63–75

    Article  PubMed  CAS  Google Scholar 

  • Seedorf M, Soll J (1995) Copper chloride, an inhibitor of protein import into chloroplasts. FEBS Lett 367:19–22

    Article  PubMed  CAS  Google Scholar 

  • Seedorf M, Waegemann K, Soll J (1995) A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J 7:401–411

    Article  PubMed  CAS  Google Scholar 

  • Shanklin J, DeWitt ND, Flanagan JM (1995) The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: an archetypal two-component ATP-dependent protease. Plant Cell 7:1713–1722

    PubMed  CAS  Google Scholar 

  • Shen G, Kuppu S, Venkataramani S, Wang J, Yan J, Qiu X, Zhang H (2010) Ankyrin repeat-containing protein 2A is an essential molecular chaperone for peroxisomal membrane-bound ascorbate peroxidase3 in Arabidopsis. Plant Cell 22:811–831

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Shipman RL, Inoue K (2009) Suborganellar localization of plastidic type I signal peptidase 1 depends on chloroplast development. FEBS Lett 583:938–942

    Article  PubMed  CAS  Google Scholar 

  • Shipman-Roston RL, Ruppel NJ, Damoc C, Phinney BS, Inoue K (2010) The significance of protein maturation by plastidic type I signal peptidase 1 for thylakoid development in Arabidopsis chloroplasts. Plant Physiol 152:1297–1308

    Article  PubMed  CAS  Google Scholar 

  • Silva-Filho MC (2003) One ticket for multiple destinations: dual targeting of proteins to distinct subcellular locations. Curr Opin Plant Biol 6:589–595

    Article  PubMed  CAS  Google Scholar 

  • Sjögren LL, MacDonald TM, Sutinen S, Clarke AK (2004) Inactivation of the clpC1 gene encoding a chloroplast Hsp100 molecular chaperone causes growth retardation, leaf chlorosis, lower photosynthetic activity, and a specific reduction in photosystem content. Plant Physiol 136:4114–4126

    Article  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 155:354–369

    Article  PubMed  CAS  Google Scholar 

  • Smith MD, Hiltbrunner A, Kessler F, Schnell DJ (2002) The targeting of the atToc159 preprotein receptor to the chloroplast outer membrane is mediated by its GTPase domain and is regulated by GTP. J Cell Biol 159:833–843

    Article  PubMed  CAS  Google Scholar 

  • Smith MD, Rounds CM, Wang F, Chen K, Afitlhile M, Schnell DJ (2004) atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J Cell Biol 165:323–334

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  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 274:37467–37472

    Article  PubMed  CAS  Google Scholar 

  • Stanga JP, Boonsirichai K, Sedbrook JC, Otegui MS, Masson PH (2009) A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiol 149:1896–1905

    Article  PubMed  CAS  Google Scholar 

  • Stengel A, Benz P, Balsera M, Soll J, Bölter B (2008) Tic62 – redox-regulated translocon composition and dynamics. J Biol Chem 283:6656–6667

    Article  PubMed  CAS  Google Scholar 

  • Stengel A, Benz JP, Buchanan BB, Soll J, Bölter B (2009) Preprotein import into chloroplasts via the Toc and Tic complexes is regulated by redox signals in Pisum sativum. Mol Plant 2:1181–1197

    Article  PubMed  CAS  Google Scholar 

  • Su PH, Li HM (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol 146:1231–1241

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sun CW, Chen LJ, Lin LC, Li HM (2001) Leaf-specific upregulation of chloroplast translocon genes by a CCT motif-containing protein, CIA 2. Plant Cell 13:2053–2061

    PubMed  CAS  Google Scholar 

  • Sun YJ, Forouhar F, Li Hm HM, Tu SL, Yeh YH, Kao S, Shr HL, Chou CC, Chen C, Hsiao CD (2002) Crystal structure of pea Toc34, a novel GTPase of the chloroplast protein translocon. Nat Struct Biol 9:95–100

    Article  PubMed  CAS  Google Scholar 

  • Sun CW, Huang YC, Chang HY (2009) CIA2 coordinately up-regulates protein import and synthesis in leaf chloroplasts. Plant Physiol 150:879–888

    Article  PubMed  CAS  Google Scholar 

  • Sveshnikova N, Soll J, Schleiff E (2000) Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proc Natl Acad Sci USA 97:4973–4978

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Theg SM, Bauerle C, Olsen LJ, Selman BR, Keegstra K (1989) Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes. J Biol Chem 264:6730–6736

    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 

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

    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 14:2436–2446

    PubMed  CAS  Google Scholar 

  • Tripp J, Inoue K, Keegstra K, Froehlich JE (2007) A novel serine/proline-rich domain in combination with a transmembrane domain is required for the insertion of AtTic40 into the inner envelope membrane of chloroplasts. Plant J 52:824–838

    Article  PubMed  CAS  Google Scholar 

  • Trösch R, Jarvis P (2011) The stromal processing peptidase of chloroplasts is essential in Arabidopsis, with knockout mutations causing embryo arrest after the 16-cell stage. PLoS One 6:e23039

    Article  PubMed  CAS  Google Scholar 

  • Tsai LY, Tu SL, Li HM (1999) Insertion of atToc34 into the chloroplastic outer membrane is assisted by at least two proteinaceous components in the import system. J Biol Chem 274:18735–18740

    Article  PubMed  CAS  Google Scholar 

  • Tu SL, Li HM (2000) Insertion of OEP14 into the outer envelope membrane is mediated by proteinaceous components of chloroplasts. Plant Cell 12:1951–1960

    PubMed  CAS  Google Scholar 

  • Tu SL, Chen LJ, Smith MD, Su YS, Schnell DJ, Li HM (2004) Import pathways of chloroplast interior proteins and the outer-membrane protein OEP14 converge at Toc75. Plant Cell 16:2078–2088

    Article  PubMed  CAS  Google Scholar 

  • Ueda M, Nishikawa T, Fujimoto M, Takanashi H, Arimura S, Tsutsumi N, Kadowaki K (2008) Substitution of the gene for chloroplast RPS16 was assisted by generation of a dual targeting signal. Mol Biol Evol 25:1566–1575

    Article  PubMed  CAS  Google Scholar 

  • Uniacke J, Zerges W (2009) Chloroplast protein targeting involves localized translation in Chlamydomonas. Proc Natl Acad Sci USA 106:1439–1444

    Article  PubMed  CAS  Google Scholar 

  • Van den Broeck G, Timko MP, Kausch AP, Cashmore AR, Van Montagu M, Herrera-Estrella L (1985) Targeting of a foreign protein to chloroplasts by fusion to the transit peptide from the small subunit of ribulose 1,5-bisphosphate carboxylase. Nature 313:358–363

    Article  PubMed  Google Scholar 

  • Vandervere PS, Bennett TM, Oblong JE, Lamppa GK (1995) A chloroplast processing enzyme involved in precursor maturation shares a zinc-binding motif with a recently recognized family of metalloendopeptidases. Proc Natl Acad Sci USA 92:7177–7181

    Article  PubMed  CAS  Google Scholar 

  • Viana AA, Li M, Schnell DJ (2010) Determinants for stop-transfer and post-import pathways for protein targeting to the chloroplast inner envelope membrane. J Biol Chem 285:12948–12960

    Article  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 7:1124–1131

    Article  CAS  Google Scholar 

  • Vojta A, Alavi M, Becker T, Hörmann F, Küchler M, Soll J, Thomson R, Schleiff E (2004) The protein translocon of the plastid envelopes. J Biol Chem 279:21401–21405

    Article  PubMed  CAS  Google Scholar 

  • Vojta L, Soll J, Bölter B (2007a) Protein transport in chloroplasts – targeting to the intermembrane space. FEBS J 274:5043–5054

    Article  PubMed  CAS  Google Scholar 

  • Vojta L, Soll J, Bölter B (2007b) Requirements for a conservative protein translocation pathway in chloroplasts. FEBS Lett 581:2621–2624

    Article  PubMed  CAS  Google Scholar 

  • von Heijne G, Nishikawa K (1991) Chloroplast transit peptides. The perfect random coil? FEBS Lett 278:1–3

    Article  Google Scholar 

  • Waegemann K, Soll J (1991) Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant J 1:149–158

    Article  Google Scholar 

  • Walker D, Chaddock AM, Chaddock JA, Roberts LM, Lord JM, Robinson C (1996) Ricin A chain fused to a chloroplast-targeting signal is unfolded on the chloroplast surface prior to import across the envelope membranes. J Biol Chem 271:4082–4085

    Article  PubMed  CAS  Google Scholar 

  • Wallas TR, Smith MD, Sanchez-Nieto S, Schnell DJ (2003) The roles of Toc34 and Toc75 in targeting the Toc159 preprotein receptor to chloroplasts. J Biol Chem 278:44289–44297

    Article  PubMed  CAS  Google Scholar 

  • Wan J, Blakeley SD, Dennis DT, Ko K (1996) Transit peptides play a major role in the preferential import of proteins into leucoplasts and chloroplasts. J Biol Chem 271:31227–31233

    Article  PubMed  CAS  Google Scholar 

  • Wan J, Bringloe D, Lamppa GK (1998) Disruption of chloroplast biogenesis and plant development upon down-regulation of a chloroplast processing enzyme involved in the import pathway. Plant J 15:459–468

    Article  CAS  Google Scholar 

  • Wang F, Agne B, Kessler F, Schnell DJ (2008) The role of GTP binding and hydrolysis at the atToc159 preprotein receptor during protein import into chloroplasts. J Cell Biol 183:87–99

    Article  PubMed  CAS  Google Scholar 

  • Weibel P, Hiltbrunner A, Brand L, Kessler F (2003) Dimerization of Toc-GTPases at the chloroplast protein import machinery. J Biol Chem 278:37321–37329

    Article  PubMed  CAS  Google Scholar 

  • Whatley JM (1978) A suggested cycle of plastid developmental interrelationships. New Phytol 80:489–502

    Article  Google Scholar 

  • Whatley JM, McLean B, Juniper BE (1991) Continuity of chloroplast and endoplasmic reticulum membranes in Phaseolus vulgaris. New Phytol 117:209–217

    Article  Google Scholar 

  • Wickner W, Schekman R (2005) Protein translocation across biological membranes. Science 310:1452–1456

    Article  PubMed  CAS  Google Scholar 

  • Wickner S, Maurizi MR, Gottesman S (1999) Posttranslational quality control: folding, refolding, and degrading proteins. Science 286:1888–1893

    Article  PubMed  CAS  Google Scholar 

  • Wienk HL, Wechselberger RW, Czisch M, de Kruijff B (2000) Structure, dynamics, and insertion of a chloroplast targeting peptide in mixed micelles. Biochemistry 39:8219–8227

    Article  PubMed  CAS  Google Scholar 

  • Wu C, Seibert FS, Ko K (1994) Identification of chloroplast envelope proteins in close physical proximity to a partially translocated chimeric precursor protein. J Biol Chem 269:32264–32271

    PubMed  CAS  Google Scholar 

  • Yalovsky S, Paulsen H, Michaeli D, Chitnis PR, Nechushtai R (1992) Involvement of a chloroplast HSP70 heat shock protein in the integration of a protein (light-harvesting complex protein precursor) into the thylakoid membrane. Proc Natl Acad Sci USA 89:5616–5619

    Article  PubMed  CAS  Google Scholar 

  • Yan X, Khan S, Hase T, Emes MJ, Bowsher CG (2006) Differential uptake of photosynthetic and non-photosynthetic proteins by pea root plastids. FEBS Lett 580:6509–6512

    Article  PubMed  CAS  Google Scholar 

  • Yeh YH, Kesavulu MM, Li HM, Wu SZ, Sun YJ, Konozy EH, Hsiao CD (2007) Dimerization is important for the GTPase activity of chloroplast translocon components atToc33 and psToc159. J Biol Chem 282:13845–13853

    Article  PubMed  CAS  Google Scholar 

  • Young ME, Keegstra K, Froehlich JE (1999) GTP promotes the formation of early-import intermediates but is not required during the translocation step of protein import into chloroplasts. Plant Physiol 121:237–244

    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 

  • Yu TS, Li H (2001) Chloroplast protein translocon components atToc159 and atToc33 are not essential for chloroplast biogenesis in guard cells and root cells. Plant Physiol 127:90–96

    Article  PubMed  CAS  Google Scholar 

  • Yue R, Wang X, Chen J, Ma X, Zhang H, Mao C, Wu P (2010) A rice stromal processing peptidase regulates chloroplast and root development. Plant Cell Physiol 51:475–485

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Li X, Zhang Y, Kuppu S, Shen G (2010) Is AKR2A an essential molecular chaperone for a class of membrane-bound proteins in plants? Plant Signal Behav 5:1520–1522

    Article  PubMed  CAS  Google Scholar 

  • Zhong R, Wan J, Jin R, Lamppa G (2003) A pea antisense gene for the chloroplast stromal processing peptidase yields seedling lethals in Arabidopsis: survivors show defective GFP import in vivo. Plant J 34:802–812

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge the support of a Gatsby Charitable Foundation Sainsbury PhD Studentship (to RT), and of Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/D016541/1 and BB/H008039/1 (to QL and PJ).

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Ling, Q., Trösch, R., Jarvis, P. (2013). The Ins and Outs of Chloroplast Protein Transport. In: Biswal, B., Krupinska, K., Biswal, U. (eds) Plastid Development in Leaves during Growth and Senescence. Advances in Photosynthesis and Respiration, vol 36. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5724-0_12

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