Chloroplast quest: A journey from the cytosol into the chloroplast and beyond

  • Ute C. Vothknecht
  • J. Soll
Part of the Reviews of Physiology, Biochemistry and Pharmacology book series (REVIEWS, volume 145)


Chloroplasts are characteristic organelles of plants and algae and the site of oxygenic photosynthesis. They are surrounded by a double membrane and possess an internal membrane system, the thylakoids, on which the photosynthetic machinery is located. They originated more than 1.2 billion years ago from an endosymbiotic event between an already photosynthetic ancestor of present day cyanobacteria and a mitochondriate host cell. During the transformation of the internalized cyanobacterium into a cell organelle most of the genetic information of the endosymbiot got lost or was transferred into the nucleus of the host. Chloroplast proteins encoded by nuclear genes are synthesized on cytoplasmic ribosomes and have to be relocated into the organelle. This is achieved by a proteinaceous import machinery in the outer and inner envelope of the chloroplasts. Proteins destined for the thylakoid membrane and the thylakoid lumen are further translocated by several different pathways into or across this membrane. The subject of this review is the quest of nuclear encoded chloroplast proteins into the organelle and to their final suborganellar location.


Thylakoid Membrane Transit Peptide Signal Recognition Particle Envelope Membrane Outer Envelope 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Akita M, Nielsen E, Keegstra K (1997) Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J Cell Biol 136:983–994PubMedCrossRefGoogle Scholar
  2. Alefsen H, Waegemann K, Keegstra K (1997) Analysis of the chloroplast protein import machinery. J Plant Physiol 144:339–345Google Scholar
  3. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  4. Bartling D, Clausmeyer S, Oelmüller R, Herrmann RG (1990) Towards epitope models for chloroplast transit sequences Bot Mag 2:119–144Google Scholar
  5. Bauer J, Chen K, Hiltbunner A, Wehrli E, Eugster M, Schnell D, Kessler F (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403:203–207PubMedCrossRefGoogle Scholar
  6. Bendich AJ (1987) Why do chloroplasts and mitochondria contain so many copies of their genomes? BioEssays 6:279–282PubMedCrossRefGoogle Scholar
  7. Bhaya D, Grosman A (1991) Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol Gen Genet 229:400–404PubMedCrossRefGoogle Scholar
  8. 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 441:59–62PubMedCrossRefGoogle Scholar
  9. Bruce B (1998) The role of lipids in plastid protein transport. Plant Mol Biol 38:223–246PubMedCrossRefGoogle Scholar
  10. Buvinger WE, Michel H, Bennett J (1989) A truncated analog of a pre-light-harvesting chlorophyll a/b protein II transit peptide inhibits protein import into chloroplasts. J Biol Chem 264:1195–1202PubMedGoogle Scholar
  11. Caliebe A, Grimm R, Kaiser G, Lübeck 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 16:7342–7350PubMedCrossRefGoogle Scholar
  12. Cavalier-Smith T (1987) The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann NY Acad Sci 503:55–71PubMedCrossRefGoogle Scholar
  13. Cavalier-Smith T (2000) Membrane heredity and early chloroplast evolution. Trends Plant Sci 5:174–182PubMedCrossRefGoogle Scholar
  14. Chaddock AM, Mant A, Karnauchov I, Brink S, Herrmann RG, Klösgen RB, Robinson C (1995) A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the delta pH-dependent thylakoidal protein translocase. EMBO J 14:2715–2722PubMedGoogle Scholar
  15. Chen K, Li HM (1998) A mutant deficient in the plastid lipid DGD is defective in protein import into chloroplasts. Plant J 16:33–39PubMedCrossRefGoogle Scholar
  16. Chen K, Chen X, Schnell DJ (2000) Initial binding of preproteins involving the Toc160 receptor can be bypassed during protein import into chloroplasts. Plant Physiol 122:813–822PubMedCrossRefGoogle Scholar
  17. Cline K, Mori H (2001) Thylakoid DeltapH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J Cell Biol 154:719–729PubMedCrossRefGoogle Scholar
  18. Dalbey RE, Robinson C (1999) Protein translocation into and across the bacterial plasma membrane and the plant thylakoid membrane. Trends Biochem Sci 24:17–22PubMedCrossRefGoogle Scholar
  19. deCastro Silva Filho M, Wieerst MC, Flügge UI, Chaumont F, Boutry M (1996): Different in vitro and in vivo targeting properties of the transit peptide of a chloroplast envelope inner membrane Protein. J Biol Chem 272:15264–15269CrossRefGoogle Scholar
  20. DeLille J, Peterson EC, Johnson T, Moore M, Kight A, Henry R (2000) A novel precursor recognition element facilitates posttranslational binding to the signal recognition particle in chloroplasts. Proc Natl Acad Sci USA 97:1926–1931PubMedCrossRefGoogle Scholar
  21. Dobberstein B, Blobel G, Chua NH (1977) In vitro synthesis and processing of a putative precursor for the small subunit of ribulose-1,5-bisphosphate carboxylase in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 74:1028–1085CrossRefGoogle Scholar
  22. Eichacker LA, Henry R (2001) Function of a chloroplast SRP in thylakoid protein export, Biochem Biophys Acta 1541:120–134PubMedCrossRefGoogle Scholar
  23. Ellis RJ, van der Vies SM (1991) Molecular chaperones. Annu Rev Biochem 60:321–347PubMedCrossRefGoogle Scholar
  24. Fichera ME, Roos DS (1997) A plastid organelle as a drug target in apicomplexan parasites. Nature 390:407–409PubMedCrossRefGoogle Scholar
  25. Fischer K, Weber A, Arbinger B, Brink S, Eckerskorn C, Flügge U-I (1994) The 24 kDa outer envelope membrane protein from spinach chloroplasts: Molecular cloning, in vivo expression and import pathway of a protein with unusual properties. Plant Mol Biol 25, 167–177PubMedCrossRefGoogle Scholar
  26. Flügge UI, Hinz G (1986) Energy dependence of protein translocation into chloroplasts. Eur J Biochem 160:563–567PubMedCrossRefGoogle Scholar
  27. Flügge UI, Fischer K, Gross A, Sebald W, Lottspeich F, Eckerskorn C (1989) The triose phosphate-3-phosphoglycerate-phosphate translocator from spinach chloroplasts: nucleotide sequence of a full-length cDNA clone and import of the in vitro synthesized precursor protein into chloroplasts. EMBO J 1:39–46.Google Scholar
  28. Franklin AE, Hoffman NE (1993) Characterization of a chloroplast homolog of the 54-kda subunit of the signal recognition particle. J Biol Chem 268:22175–22180PubMedGoogle Scholar
  29. Fröderberg L, Röhl T, van Wijk K-J, de Gier J-WL (2001) Complementation of bacterial SecE by a chloroplastic homologue. FEBS Lett 498:52–56PubMedCrossRefGoogle Scholar
  30. Groehlich JE, Benning C, Dormann P (2001) The digalactosyldiacylglycerol (DGDG) synthase DGD1 is inserted into the outer envelope membrane of chloroplasts in a manner independent of the general import pathway and does not depend on direct interaction with monogalactosyldiacylglycerol synthase for DGDG biosynthesis. J Biol Chem 276:31806–31812CrossRefGoogle Scholar
  31. Fulgosi H, Soll J (2002) The chloroplast protein import receptors Toc34 and Toc159 are phosphorylated by distinct protein kinases. J Biol Chem in pressGoogle Scholar
  32. Gibbs SP (1978) The chloroplast of Euglena may have evolved from symbiotic green algae. Can J Bot 56 2883–2889Google Scholar
  33. Goldschmidt-Clermont M (1998) Coordination of nuclear and chloroplast gene expression in plant cells. Int Rev Cytol 177:115–180PubMedCrossRefGoogle Scholar
  34. Groves MR, Mant A, Kuhn A, Koch J, Dubel S, Robinson C, Sinning I (2001) Functional characterization of recombinant chloroplast signal recognition particle. J Biol Chem 276:27778–277786PubMedCrossRefGoogle Scholar
  35. Gutensohn M, Schulz B, Nicolay P, Flügge U-I (2000) Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. Plant J 23:771–783PubMedCrossRefGoogle Scholar
  36. Hachiya N, Mihara K, Suda K, Horst M, Schatz G, Lithgow T (1995) Reconstitution of the initial steps of mitochondrial protein import. Nature 376:705–709PubMedCrossRefGoogle Scholar
  37. Hansmann P, Eschbach S (1990) Isolation and preliminary characterization of the nucleus and the nucleomorph of a cryptomonad, Pyrenomonas salina. Eur J Cell Biol 52:373–378PubMedGoogle Scholar
  38. Haward SR, Napier JA, Gray JC (1997) Chloroplast SecA functions as a membrane-associated component of the Sec-like protein translocase of pea chloroplasts. Eur J Biochem 248:724–30PubMedCrossRefGoogle Scholar
  39. Hase T, Kimata Y, Yonekura, K, Matsumura T, Sakakibara H (1991) Molecular cloning and differential expression of the maize ferredoxin gene family. Plant Physiol 96:77–83PubMedGoogle Scholar
  40. Herrmann RG (1999) Biogenesis and evolution of photosynthetic (thylakoid) membranes. Biosci Rep 19:355–365PubMedCrossRefGoogle Scholar
  41. Herrmann JM, Neupert W (2000) What fuels polypeptide translocation? An energetical view on mitochondrial protein sorting. Biochim Biophys Acta 1459:331–338PubMedCrossRefGoogle Scholar
  42. High S, Henry R, Mould RM, Valent Q, Meacock S, Cline K, Gray JC, Luirink J (1997) Chloroplast SRP54 interacts with a specific subset of thylakoid precursor proteins. J Biol Chem 272:11622–11628PubMedCrossRefGoogle Scholar
  43. Hiltbrunner A, Bauer J, Alvarez-Huerta M, Kessler F (2001) Protein translocon at the Arabidopsis outer chloroplast membrane. Biochem Cell Biol 79:629–635PubMedCrossRefGoogle Scholar
  44. Hinnah SC, Hill K, Wagner R, Schlicher T, Soll J (1997) Reconstitution of a chloroplast protein import channel. EMBO J 16:7351–7360PubMedCrossRefGoogle Scholar
  45. 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 125:2154–2163PubMedCrossRefGoogle Scholar
  46. Hirsch S, Muckel E, Heemeyer F, Heijne Gv, Soll J (1994) A receptor component of the chloroplast protein translocation machinery. Science 266:1989–1992PubMedCrossRefGoogle Scholar
  47. Hoffman NE, Franklin AE (1994) Evidence for a stromal GTP requirement for the integration of a chlorophyll a/b-binding polypeptide into thylakoid membranes. Plant Physiol 105:295–304PubMedCrossRefGoogle Scholar
  48. Ivey RA 3rd, Subramanian C, Bruce B (2000) Identification of a Hsp70 recognition domain within the rubisco small subunit transit peptide. Plant Physiol 122:1289–1299PubMedCrossRefGoogle Scholar
  49. Jackson DT, Froehlich JE, Keegstra K (1998) The hydrophobic domain of Tic110, an inner envelope membrane component of the chloroplastic protein translocation apparatus, faces the stromal compartment. J Biol Chem 273:16583–16588PubMedCrossRefGoogle Scholar
  50. Jackson-Constan DT, Keegstra K (2001) Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol 125:1567–1576PubMedCrossRefGoogle Scholar
  51. Jarvis P, Chen L-M, Li H-m, Peto CA, Chory J (1998) An Arabidopsis mutant defective in the plastid general import apparatus. Science 282:100–103PubMedCrossRefGoogle Scholar
  52. Jarvis P (2001) Intracellular signalling: the chloroplast talks. Curr Biol 11:307–310CrossRefGoogle Scholar
  53. Kerber B, Soll J (1992) Transfer of a chloroplast-bound precursor protein into the translocation apparatus is impaired after phospholipase C treatment. FEBS Lett 306:71–74PubMedCrossRefGoogle Scholar
  54. Kessler F, Blobel G, Patel HA, Schnell DJ (1994) Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 266:1035–1039PubMedCrossRefGoogle Scholar
  55. Kessler F, Blobel G (1996) Interaction of the protein import and folding machineries in the chloroplast. Proc Natl Acad Sci USA 93:7684–7689PubMedCrossRefGoogle Scholar
  56. Klösgen RB, Brock IW, Herrmann RG, Robinson C (1992) Proton gradient-driven import of the 16 kDa oxygen-evolving complex protein as the full precursor protein by isolated thylakoids. Plant Mol Biol 18:1031–1034PubMedCrossRefGoogle Scholar
  57. 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 9:1421–32CrossRefGoogle Scholar
  58. Ko K, Ko ZW (1992) Carboxyl-terminal sequences can influence the in vitro import and intraorganellar targeting of chloroplast protein precursors. J Biol Chem 267:13910–13916PubMedGoogle Scholar
  59. Ko K, Budd D, Wu C, Seibert F, Kourtz L, Ko ZW (1995) Isolation and characterization of a cDNA clone encoding a member of the Com44/Cim44 envelope components of the chloroplast protein import apparatus. J Biol Chem 270:28601–28608PubMedCrossRefGoogle Scholar
  60. Köhler S, Delwiche CF, Denny PW, Tilney LG, Webster P, Wilson RJ, Palmer JD, Roos DS (1997) A plastid of probable green algal origin in Apicomplexan parasites. Science 275:1485–1489PubMedCrossRefGoogle Scholar
  61. Kogata N, Nishio K, Hirohashi T, Kikuchi S, Nakai M (1999) Involvement of a chloroplast homologue of the signal recognition particle receptor protein, FtsY, in protein targeting to thylakoids. FEBS Lett 447:329–333PubMedCrossRefGoogle Scholar
  62. Komiya T, Rospert S, Koehler C, Looser R, Schatz G, Mihara K (1998) Interaction of mitochondrial targeting signals with acidic receptor domains along the protein import pathway: evidence for the ‘acid chain’ hypothesis. EMBO J 17:3886–3898PubMedCrossRefGoogle Scholar
  63. 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 139:1677–1685PubMedCrossRefGoogle Scholar
  64. 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 143:991–1002PubMedCrossRefGoogle Scholar
  65. Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J, Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Natl Acad Sci USA 98:4238–4242PubMedCrossRefGoogle Scholar
  66. Lang M, Apt KE, Kroth PG (1998) Protein transport into “complex” diatom plastids utilizes two different targeting signals. J Biol Chem 273:30973–30978PubMedCrossRefGoogle Scholar
  67. Lang M, Kroth PG (2001) Diatom fucoxanthin chlorophyll a/c-binding protein (FCP) and land plant light-harvesting proteins use a similar pathway for thylakoid membrane insertion. J Biol Chem 276:7985–7991PubMedCrossRefGoogle Scholar
  68. Li HM, Moore T, Keegstra K (1991) Targeting of proteins to the outer envelope membrane uses a different pathway than transport into chloroplasts. Plant Cell 3:709–717PubMedCrossRefGoogle Scholar
  69. Li HM, Sullivan TD, Keegstra K (1992) Information for targeting to the chloroplastic inner envelope membrane is contained in the mature region of the maize Btl-encoded protein. J Biol Chem 267:18999–9004PubMedGoogle Scholar
  70. Li HM, and Chen L-J (1996) Protein targeting and integration signal for the chloroplastic outer envelope membrane. Plant Cell 8:2117–2126PubMedCrossRefGoogle Scholar
  71. Li XX, Henry R, Yuan JG, Cline K, Hoffman NE (1995) A chloroplast homolog of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes. Proc Natl Acad Sci USA 92:3789–3793PubMedCrossRefGoogle Scholar
  72. Lübeck J, Soll J, Akita M, Nielsen E, Keegstra K (1996) Topoplogy of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane. EMBO J 15:4230–4238PubMedGoogle Scholar
  73. 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 137:1279–86PubMedCrossRefGoogle Scholar
  74. Lubben TH, Donaldson GK, Viitanen PV, Gatenby AA (1989) Several proteins imported into chloroplasts form stable complexes with the GroEL-related chloroplast molecular chaperone. Plant Cell 1:1223–1230PubMedCrossRefGoogle Scholar
  75. Mant A, Woolhead CA, Moore M, Henry R, Robinson C (2001) Insertion of PsaK into the thylakoid membrane in a “Horseshoe” conformation occurs in the absence of signal recognition particle, nucleoside triphosphates, or functional albino3. J Biol Chem 276: 36200–36206PubMedCrossRefGoogle Scholar
  76. Margulis L (1970) Origin of Eukaryotic Cells. New Haven, CT, USA; Yale University PressGoogle Scholar
  77. Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9–17PubMedCrossRefGoogle Scholar
  78. Marshall JS, DeRocher AE, Keegstra K, Vierling E (1990) Identification of heat shock protein hsp70 homologues in chloroplasts. Proc Natl Acad Sci USA 87:374–378PubMedCrossRefGoogle Scholar
  79. Martienssen RA, Barkan A, Freeling M, Taylor WC (1989) Molecular cloning of a maize gene involved in photosynthetic membrane organization that is regulated by Roberson's Mutator. EMBO J 8:1633–1639PubMedGoogle Scholar
  80. May T, Soll J (2000) 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12:53–64PubMedCrossRefGoogle Scholar
  81. McFadden GI, Gilson PR, Douglas SE (1994) The photosynthetic endosymbiont in cryptomonad cells produces both chloroplast and cytoplasmic-type ribosomes. J Cell Sci 107:649–657PubMedGoogle Scholar
  82. McFadden GI, Reith ME, Munholland J, Lang-Unnasch N (1996) Plastid in human parasites. Nature 381:482PubMedCrossRefGoogle Scholar
  83. McFadden GI, Roos DS (1999) Apicomplexan plastids as drug targets. Trends Microbiol 7:328–333PubMedCrossRefGoogle Scholar
  84. Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol. Centralbl. 25:593–604Google Scholar
  85. Molik S, Karnauchov I, Weidlich C, Herrmann RG, Klösgen RB (2001) The Rieske Fe/S protein of the cytochrom b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J Biol Chem 276:42761–42766PubMedCrossRefGoogle Scholar
  86. Moore M, Harrison MS, Peterson EC, Henry R (2000) Clloroplast Oxa1 phomolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 275:1529–1532PubMedCrossRefGoogle Scholar
  87. Mori H, Cline K (1998) A signal peptide that directs non-Sec transport in bacteria also directs efficient and exclusive transport on the thylakoid delta pH pathway. J Biol Chem 273:11404–11408Google Scholar
  88. Mori H, Cline K (2001) Post-translational protein translocation into thylakoids by the Sec and pH-dependent pathways, Biochem Biophys Acta 1541:80–90PubMedCrossRefGoogle Scholar
  89. Mould RM, Robinson C (1991) A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane. J Biol Chem 266:12189–93PubMedGoogle Scholar
  90. Motohashi R, Nagata N, Ito T, Takahashi S, Hobo T, Yoshida S, Shinozaki K (2001) An essential role of a TatC homologue of a DpH-dependent protein transporter in thylakoid membrane formation during chloroplast development in Arabidopsis thaliana. Proc Natl Adac Sci USA 98:10499–10504CrossRefGoogle Scholar
  91. Muckel E, Soll J (1996) A protein import receptor of chloroplasts is inserted into the outer envelope membrane by a novel pathway. J Biol Chem 271:23864–23852Google Scholar
  92. 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 Hsp 100 molecular chaperone. EMBO J 16:935–46PubMedCrossRefGoogle Scholar
  93. Oblong JE, Lamppa GK (1992) Precursor for the light-harvesting chlorophyll a/b-binding protein synthesized in Escherichia coli blocks import of the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. J Biol Chem 267:14328–14334PubMedGoogle Scholar
  94. Pain D, Blobel G (1987) Protein import into chloroplasts requires a chloroplast AT-Pase. Proc Natl Acad Sci USA 84:3288–3292PubMedCrossRefGoogle Scholar
  95. Palmer JD (2000) A single birth of all plastids? Nature 405:32–33PubMedCrossRefGoogle Scholar
  96. Payan LA, Cline K (1991) A stromal protein factor maintains the solubility and insertion competence of an imported thylakoid membrane proteins. J Cell Biol 112:603–613PubMedCrossRefGoogle Scholar
  97. Peltier JB, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I, van Wijk KJ (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12:319–341PubMedCrossRefGoogle Scholar
  98. Perry SE, Buvinger WE, Bennett J, Keegstra K (1991) Synthetic analogues of a transit peptide inhibit binding or translocation of chloroplastic precursor proteins. J Biol Chem 266:11882–11889PubMedGoogle Scholar
  99. Perry SE, Keegstra K (1994) Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 6:93–105PubMedCrossRefGoogle Scholar
  100. Pfanner N, Geissler A (2001) Versatility of the mitochondrial protein import machinery. Nat Rev Mol Cell Biol 2:339–349PubMedCrossRefGoogle Scholar
  101. Pilon M, de Kruijff B, Weisbeek PJ (1992) New insights into the import mechanism of the ferredoxin precursor into chloroplast. J Biol Chem 267:2548–2556PubMedGoogle Scholar
  102. 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 270:3882–3893PubMedCrossRefGoogle Scholar
  103. Pilgrim ML, van Wijk K-J, Parry DH, Sy DAC, Hoffman NE (1998) Expression of a dominant negative form of cpSRP54 inhibits chloroplast biogenesis in Arabidopsis. Plant J 13:177–186PubMedCrossRefGoogle Scholar
  104. Pinnaduwage P, Bruce BD (1996) In vitro interaction between a chloroplast transit peptide and chloroplast outer envelope lipids is sequence-specific and lipid class-dependent. J Biol Chem 271:32907–32915PubMedCrossRefGoogle Scholar
  105. Rial DV, Arakaki AK, Ceccarelli (2000) Interaction of the targeting sequence of chloroplast precursors with Hsp70 molecular chaperones. Eur J Biochem 267:6239–6248PubMedCrossRefGoogle Scholar
  106. Richter S, Lamppa GK (1998) A chloroplast processing enzyme functions as the general stromal processing peptidase. Proc Natl Acad Sci USA 95:7463–7468PubMedCrossRefGoogle Scholar
  107. Rochaix JD (2001) Posttranscriptional control of chloroplast gene expression. From RNA to photosynthetic complex. Plant Physiol 125:142–144PubMedCrossRefGoogle Scholar
  108. Rodermel S (2001) Pathways of plastid-to-nuclear signalling. Trends in Plant Science 6:471–478PubMedCrossRefGoogle Scholar
  109. Roy LM, Barkan A (1998) A SecY homologue is required for the elaboration of the chloroplast thylakoid membrane and for normal chloroplast gene expression. J Cell Biol 141:385–395PubMedCrossRefGoogle Scholar
  110. Salomon M, Fischer K, Flügge U-I, Soll J (1990) Sequence analysis and protein import studies of an outer chloroplast envelope polypeptide. Proc Natl Acad Sci USA 87: 5778–5782PubMedCrossRefGoogle Scholar
  111. Schein AI, Kissinger JC, Ungar LH (2001) Chloroplast transit peptide prediction: a peek inside the black box. Nucleic Acids Res 29:E82PubMedCrossRefGoogle Scholar
  112. Schindler C, Hracky R, Soll J (1987) Protein transport in chloroplasts: ATP is prerequisite. Z Naturforsch 42c:103–108Google Scholar
  113. Schleiff E, Tien R, Salomon M, Soll J (2001) Lipid Composition of Outer Leaflet of Chloroplast Outer Envelope Determines Topology of OEP7. Mol Biol Cell 12:4090–4102PubMedGoogle Scholar
  114. Schleiff E, Klösgen RB (2001) Without a little help from ‘my’ friends: direct insertion of proteins into chloroplast membranes? Biochim Biophys Acta 1541:22–33PubMedCrossRefGoogle Scholar
  115. Schnell DJ, Kessler F, Blobel G (1994) Isolation of components of the chloroplast protein import machinery. Science 266:1007–1012PubMedCrossRefGoogle Scholar
  116. 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. Trend Cell Biol 7:303–304CrossRefGoogle Scholar
  117. Schubert M, Petersson UA, Haas BJ, Funk C, Schröder WP, Kieselbach T (2001) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem epub ahead of printGoogle Scholar
  118. Schuenemann D, Amin P, Hartmann E, Hoffman NE (1999) Chloroplast SecY is complexed to SecE and involved in the translocation of the 33-kDa but not the 23-kDa subunit of the oxygen-evolving complex. J Biol Chem 274:12177–12182PubMedCrossRefGoogle Scholar
  119. Seedorf M, Waegemann K, Soll J (1995) A constituent of the chloroplast import complex represents a new type GTP-binding protein. Plant J 7:401–411PubMedCrossRefGoogle Scholar
  120. Small I, Wintz H, Akashi K, Mireau H (1998) Tow birds with one stone: genes that encode products targeted to two or more compartments. Plant Mol Biol 38:265–277PubMedCrossRefGoogle Scholar
  121. Sohrt K, Soll J (2000) Toc64, a new component of the protein translocon of chloroplasts. J Cell Biol 148:1213–1221PubMedCrossRefGoogle Scholar
  122. Stahl T, Glockmann C, Soll J, Heins L (1999) Tic40, a new “old” subunit of the chloroplast protein import translocon. J Biol Chem 274:37467–37472PubMedCrossRefGoogle Scholar
  123. Strub A, Lim JH, Pfanner N, Voos W (2000) The mitochondrial protein import motor. Biol Chem 381:943–949PubMedCrossRefGoogle Scholar
  124. Sulli C, Schwartzbach SD (1995) The polyprotein precursor to the Euglena light-harvesting chlorophyll a/b-binding protein is transported to the Golgi apparatus prior to chloroplast import and polyprotein processing. J Biol Chem 270:13084–13090PubMedCrossRefGoogle Scholar
  125. Sun Y-J, Forouhar F, Li H-M, Tu S-L, Yeh Y-H, Kao S, Shr H-L, Chou C-C, Chen C, Hsiao C-D (2002) Crystal structure of pea Toc34, a novel GTPase of the chloroplast protein translocon. Nature Struct Biol epub ahead of printGoogle Scholar
  126. Suzuki S, Izumihara K, Hase T (1991) Plastid import of iron-sulfur cluster assembly of photosynthetic and non-photosynthetic ferredoxin isoproteins in maize. Plant Physiol 97:375–380PubMedGoogle Scholar
  127. Sveshnikov N, Soll J, Schleiff E (2000a) Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proc Natl Acad Sci USA 97:4973–4978CrossRefGoogle Scholar
  128. Sveshnikova N, Grimm R, Soll J, Schleiff E (2000b) Topology studies of the chloroplast protein import channel Toc75. Biol Chem 381:687–693PubMedCrossRefGoogle Scholar
  129. 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 264:6730–6736PubMedGoogle Scholar
  130. Theg SM, Geske FJ (1992) Biophysical characterization of a transit peptide directing chloroplast protein import. Biochemistry 31:5053–5060PubMedCrossRefGoogle Scholar
  131. Tranel PJ, Froehlich J, Goyal A, Keegstra K (1995) A component of the chloroplastic protein import apparatus is targeted to the outer envelope via a novel pathway. EMBO J 14:2436–2446PubMedGoogle Scholar
  132. Tsai L-Y, Tu S-L and Li H-M (1999) Insertion of atToc34 into the chloroplastic outer membrane is assisted by at least two proteinaceous components in the import system. J Biol Chem 274:18735–18740PubMedCrossRefGoogle Scholar
  133. Tsugeki R, Nishimura M (1993) Interaction of homologues of Hsp 70 and Cpn60 with ferredoxin-NADP+ reductase upon its import into chloroplasts. FEBS Lett 320:198–202PubMedCrossRefGoogle Scholar
  134. Tu CJ, Schuenemann D, Hoffman NE (1999) Chloroplast FtsY, chloroplast signal recognition particle, and GTP are required to reconstitute the soluble phase of light-harvesting chlorophyll protein transport into thylakoid membranes. J Biol Chem 274:27219–27224PubMedCrossRefGoogle Scholar
  135. Tu S-L, Li HM (2000) Insertion of OEP14 into the outer envelope membrane is mediated by proteinaceous components of chloroplasts. Plant Cell 12:1951–1959PubMedCrossRefGoogle Scholar
  136. 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 92:7177–7181PubMedCrossRefGoogle Scholar
  137. van't Hof R, van Klompenburg W, Pilon M, Kozubek A, de Korte-Kool G, Demel RA, Weisbeek PJ, de Kruijff B (1993) The transit sequence mediates the specific interactions of the precusor of ferredoxin with chloroplast envelope membrane lipids. J Biol Chem 268:4037–4042Google Scholar
  138. van't Hof R, de Kruijff (1995) Transit sequence-dependent binding of the chloroplast precursor protein ferredoxin to lipid vesicles and its implications for membrane stabilty. FEBS Lett 361:35–40CrossRefGoogle Scholar
  139. Voelker R, Barkan A (1995) Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. EMBO J 14:3905–3914PubMedGoogle Scholar
  140. von Heijne G, Steppuhn J, Herrmann RG (1989) Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180:535–545CrossRefGoogle Scholar
  141. Waegemann K, Paulsen H, Soll J (1990) Phosphorylation of the transit sequence of chloroplast precursor proteins. J Biol Chem 271:6545–6554Google Scholar
  142. Waegemann K, Soll J (1991) Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant J 1:149–158CrossRefGoogle Scholar
  143. Waegemann K, Soll J (1996) Phosphorylation of the transit sequence of chloroplast precursor proteins. J Biol Chem 271:6545–6554PubMedCrossRefGoogle Scholar
  144. Waller RF, Reed MB, Cowman AF, McFadden GI (2000) Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 19:1794–1802PubMedCrossRefGoogle Scholar
  145. Westphal S, Heins L, Soll J, Vothknecht UC (2001a) Vippl deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis? Proc Natl Acad Sci USA 98:4243–4248PubMedCrossRefGoogle Scholar
  146. Westphal S, Soll J, Vothknecht UC (2001b) A vesicle transport system inside chloroplasts. FEBS Lett 506:257–261PubMedCrossRefGoogle Scholar
  147. Woolhead CA, Thompson SJ, Moore M, Tissier C, Mant A, Rodger A, Henry R, Robinson C (2001) Distinct Albino3-dependent and-independent pathways for thylakoid membrane protein insertion. J Biol Chem 276:40841–40846PubMedCrossRefGoogle Scholar
  148. Wu C, Ko K (1993) Identification of an uncleavable targeting signal in the 70-kilodalton spinach chloroplast outer envelope membrane protein. J Biol Chem 268:19384–19391PubMedGoogle Scholar
  149. Zimmermann R, Sagstetter M, Lewis MJ, Pelham HR (1988) Seventy-kilodalton heat shock proteins and an additional component from reticulocyte lysate stimulate import of M13 pocoat protein into microsomes. EMBO J.9:2875–2880Google Scholar

Copyright information

© Springer-Verlag 2002

Authors and Affiliations

  • Ute C. Vothknecht
    • 1
  • J. Soll
    • 1
  1. 1.Botanisches Institut der Ludwig-Maximilian-Universität MünchenMünchenGermany

Personalised recommendations