Photosynthesis Research

, Volume 19, Issue 1–2, pp 153–184 | Cite as

Recent developments in chloroplast protein transport

  • Michael L. Mishkind
  • Scott E. Scioli
Protein Transport Minireview


Most proteins located in chloroplasts are encoded by nuclear genes, synthesized in the cytoplasm, and transported into the organelle. The study of protein uptake by chloroplasts has greatly expanded over the past few years. The increased activity in this field is due, in part, to the application of recombinant DNA methodology to the analysis of protein translocation. Added interest has also been gained by the realization that the transport mechanisms that mediate protein uptake by chloroplasts, mitochondria and the endoplasmic reticulum display certain characteristics in common. These include amino terminal sequences that target proteins to particular organelles, a transport process that is mechanistically independent from the events of translation, and an ATP-requiring transport step that is thought to involve partial unfolding of the protein to be translocated. In this review we examine recent studies on the binding of precursors to the chloroplast surface, the energy-dependent uptake of proteins into the stroma, and the targeting of proteins to the thylakoid lumen. These aspects of protein transport into chloroplasts are discussed in the context of recent studies on protein uptake by mitochondria.

Key words

mitochondria organelle biogenesis transit peptide chloroplast protein transport 



chloramphenicol acetyl transferase


carbonylcyanide m-chlorophenylhydrazone


dihydrofolate reductase




endoplasmic reticulum


light harvesting chlorophyll a/b apoprotein


neomycin phosphotransferase



P-inorganic phosphate Rubisco

ribulose-1,5-bisphosphate carboxylase/oxygenase


small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase


signal recognition particle


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  1. Allison, DS and Schatz, G (1986) Artificial mitochondrial presequences. Proc Natl Acad Sci USA 83: 9011–9015Google Scholar
  2. Anderson, S and Smith, SM (1986) Synthesis of the small subunit of ribulose-bisphosphate carboxylase from genes cloned into plasmids containing the SP6 promoter. Biochem J 240: 709–715Google Scholar
  3. Argan, C, Lusty, CJ and Shore, GC (1983) Membrane and cytosolic components affecting transport of the precursor for ornithine carbamyltransferase into mitochondria. J Biol Chem 258: 667–670Google Scholar
  4. Baker, A and Schatz, G (1987) Sequences from a prokaryotic genome or the mouse dihydrofolate reductase gene can restore the import of a truncated precursor protein into yeast mitochondria. Proc Natl Acad Sci USA 84: 3117–3121Google Scholar
  5. Bartlett, SG, Landry, SJ and Pomarico, SM (1986) Transport of proteins into chloroplasts. Curr Top Plant Biochem Physiol Vol 5, University of Missouri, Columbia, pp 105–115Google Scholar
  6. Bedwell, DM, Klionsky, DJ and Emr, SD (1987) The yeast F1-ATPase precursor B subunit contains functionally redundant mitochondrial import information. Mol Cell Biol 7: 4038–4047Google Scholar
  7. Bitsch, A and Kloppstech, K (1986) Transport of proteins into chloroplasts. Reconstitution of the binding capacity for nuclear-coded precursor proteins after solubilization of envelopes with detergents. Eur J Cell Biol 40: 160–166Google Scholar
  8. Blobel, G (1980) Intracellular protein topogenesis. Proc Natl Acad Sci USA 77: 1496–1500Google Scholar
  9. Blobel, G and Dobberstein, B (1975a) Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell biol 67: 835–851Google Scholar
  10. Blobel, G and Dobberstein, B (1975b) Transfer of proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components. J Cell Biol 67: 852–862Google Scholar
  11. Block, MA, Dorne, A-J, Joyard, J and douce, R (1983) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. I. Electrophoretic and immunochemical analysis. J Biol Chem 258: 13273–13280Google Scholar
  12. Boutry, M, Nagy, F, Poulsen, C, Aoyagi, K and Chua, N-H (1987) Targeting of bacterial chloramphenicol acetyltransferase to mitochondria in transgenic plants. Nature 328: 340–342Google Scholar
  13. Boyle, SA, Hemmingsen, SM and Dennis, DT (1986) Uptake and processing of the precursor to the small subunit of ribulose 1,5-bisphosphate carboxylase by leucoplasts from the endosperm of developing castor oil seeds. Plant Physiol 81: 817–822Google Scholar
  14. Carde, J-P, Joyard, J and Douce, R (1982) Electron microscopic studies of envelope membranes from spinach plastids. Biol Cell 44: 315–324Google Scholar
  15. Cashmore, A, Szabo, L, Timko, M, Kausch, A, Van den, Broeck, G, Schreier, P, Bohnert, H, Herrera-Estrella, L, Van, Montagu, M and Schell, J (1985) Import of polypeptides into chloroplasts. Biotechnology 3: 803–808Google Scholar
  16. Chen, W-J and Douglas, MG (1987) Phosphodiester bond cleavage outside mitochondria is required for the completion of protein import into the mitochondrial matrix. Cell 49: 651–658Google Scholar
  17. Chen, L and Tai, PC (1987) Evidence for the involvement of ATP in co-translational protein translocation. Nature 328: 164–166Google Scholar
  18. Chen, L, Rhoads, D and Tai, PC (1985) Alkaline phosphatase and OmpA protein can be translocated posttranslationally into membrane vesicles of Escherichia coli. J Bacteriol 161: 973–980Google Scholar
  19. Cheung, AV, Bogorad, L, Van, Montagu, M and Schell, J (1988) Relocating a gene for herbicide tolerance: A chloroplast gene is converted into a nuclear gene. Proc Natl Acad Sci 85: 391–395Google Scholar
  20. Chia, CP and Arntzen, CJ (1986) Evidence for two-step processing of nuclear-encoded chloroplast proteins during membrane assembly. J Cell Biol 103: 725–731Google Scholar
  21. Chitnis, PR, Harel, E, Kohorn, BD, Tobin, EM and Thornber, JP (1986) Assembly of the precursor and processed light-harvesting chlorophyll a/b-protein of Lemna into the light-harvesting complex II of barley etiochloroplasts. J Cell Biol 102: 982–988Google Scholar
  22. Chitnis, PR, Nechushtai, R and Thornber, JP (1987) Insertion of the precursor of the light-harvestig chlorophyll a/b-protein into the thylakoids requires the presence of a developmentally regulated stromal factor. Plant Mol biol 10: 3–11Google Scholar
  23. Chua, N-H and Schmidt, GW (1978) Post-translational transport into intact chloroplasts of a precursor to the small subunit of ribulose-1,5-bisphosphate carboxylase. Proc Natl Acad Sci USA 75: 6110–6114Google Scholar
  24. Chua, N-H and Schmidt, GW (1979) Transport of proteins into mitochondria and chloroplasts. J Cell Biol 81: 461–483Google Scholar
  25. Cline, K (1986) Import of proteins into chloroplasts: membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J Biol Chem 261: 14804–14810Google Scholar
  26. Cline, K, Werner-Washburne, M, Lubben, TH and Keegstra, K (1985a) Precursors to two nuclear-encoded chloroplast proteins bind to the outer envelope membrane before being imported into chloroplasts. J Biol Chem 260: 3691–3696Google Scholar
  27. Cline, K, Keegstra, K and Staehelin, LA (1985b) Freeze-fracture electron microscopic analysis of ultrarapidly frozen envelope membranes on intact chloroplasts and after purification. Protoplasma 125: 111–123Google Scholar
  28. Colman, A and Robinson, C (1986) Protein import into organelles: hierarchical targeting signals. Cell 46: 321–322Google Scholar
  29. Cornwell, KLK and Keegstra, K (1987) Evidence that a chloroplast surface protein is associated with a specific binding site for the precursor to the small subunit of ribulose-1,5-bisphosphate carboxylase. Plant Physiol 85: 780–785Google Scholar
  30. della-Cioppa, G, Bauer, SC, Klein, BK, Shah, DM, Fraley, RT and Kishore, GM (1986) Translocation of the precursor of 5-enolpyruvylshikimate-3-phosphate (EDSP) synthase into chloroplasts of higher plants in vitro. Proc Natl Acad Sci USA 83: 6873–6877Google Scholar
  31. della-Cioppa, G, Kishore, GM, Beachy, RN and Fraley, RT (1987) Protein trafficking in plant cells. Plant Physiol 84: 965–968Google Scholar
  32. Dobberstein, B, Blobel, G and Chua, N-H (1977) In vitro synthesis and processing of a putative precursor for the small subunit of ribulose-1,5-bisphosphate carboxylase of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 74: 1082–1085Google Scholar
  33. Douglas, MG (1987) Hydrophobic and hydrophilic signals in protein sorting. Protein Engineering 1: 80–81Google Scholar
  34. Douglas, MG, McCammon, M and Vassarotti, A (1986) Targeting proteins into mitochondria. Microbiol Rev 50: 166–178Google Scholar
  35. Duffaud, GD, Lehnhardt, SK, March, PE and Inouye, M (1986) Structure and function of the signal peptide. In Current Topics in Membranes and Transport, Vol 24, Academic Press, London, pp 65–104Google Scholar
  36. Eilers, M and Schatz, G (1986) Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 322: 228–232Google Scholar
  37. Eilers, M, Oppliger, W and Schatz, G (1987) Both ATP and an energized inner membrane are required to import a purified precursor protein into mitochondria. EMBO J 6: 1073–1077Google Scholar
  38. Eilers, M and Schatz, G (1988) Protein unfolding and the energeties of protein translocation across biological membranes. Cell 52: 481–483Google Scholar
  39. Ellis, RJ (1981) Chloroplast proteins: synthesis, transport and assembly. Ann Rev Plant Physiol 32: 111–137Google Scholar
  40. Ellis, RJ and Robinson, C (1985) Post-translational transport and processing of cytoplasmically-synthesized precursors of organellar proteins. In the Enzymology of Post-translational Modification of Proteins, Vol 2, Academic Press, London, pp 25–39Google Scholar
  41. Flugge, UI and Hinz, G (1986) Energy dependence of protein translocation into chloroplasts. Eur J Biochem 160: 563–570Google Scholar
  42. Gillespie, LL (1987) Identification of an outer mitochondrial membrane protein that interacts with a synthetic signal peptide. J Biol Chem 262: 7939–7942Google Scholar
  43. Gillespie, LL, Argan, C, Taneja, AT, Hodges, RS, Freeman, KB and Shore, GC (1985) A synthetic signal peptide blocks import of precursor proteins destined for the mitochondrial inner membrane or matrix. J Biol Chem 260: 16045–16048Google Scholar
  44. Grossman, A, Bartlett, SG and Chua, N-H (1980) Energy-dependent uptake of cytoplasmically- synthesized polypeptides by chloroplasts. Nature 285: 625–628Google Scholar
  45. Hageman, J, Robinson, C, Smeekens, S and Weisbeek, P (1986) A thylakoid processing protease is required for complete maturation of the lumen protein plastocyanin. Nature 324: 567–569Google Scholar
  46. Hansen, W, Garcia, PD and Walter, P (1986) In vitro protein translocation across the yeast endoplasmic reticulum: ATP-dependent post-translation translocation of the prepro-α-factor. Cell 45: 397–406Google Scholar
  47. Hartl, F-U, Schmidt, B, Wachter, E, Weiss, H and Neupert, W (1986) Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase. Cell 47: 939–951Google Scholar
  48. Highfield, PE and Ellis, RJ (1978) Synthesis and transport of the small subunit of chloroplast ribulose bisphosphate carboxylase. Nature 271: 420–424Google Scholar
  49. Horwich, AL, Kalousek, F, Fenton, WA, Pollock, RA and Rosenberg, LI (1986) Targeting of pre-ornithine transcarbamylase to mitochondria: Definition of critical regions and residues in the leader peptide. Cell 44: 451–459Google Scholar
  50. Hurt, EC (1987) Unravelling the role of ATP in post-translational protein translocation. Trends Biochem Sci 12: 369–370Google Scholar
  51. Hurt, EC and van, Loon, APGM (1986) How proteins find mitochondria and intramitochondrial compartments. Trends in Biochem Sci 11: 204–207Google Scholar
  52. Hurt, EC, Pesold-Hurt, B, Suda, K, Oppliger, W and Schatz, G (1985) The first twelve amino acids (less than half of the pre-sequence) of an imported mitochondrial protein can direct mouse cytosolic dihydrofolate reductase into the yeast mitochondrial matrix. EMBO J 4: 2061–2068Google Scholar
  53. Hurt, EC, Soltanifar, N, Goldschmidt-Clermont, M, Rochaix, J-D and Schatz, G (1986) The cleavable pre-sequence of an imported chloroplast protein directs attached polypeptides into yeast mitochondria. EMBO J 5: 1343–1350Google Scholar
  54. Hurt, EC and Schatz, G (1987) A cytosolic protein contains a cryptic mitochondrial targeting signal. Nature 325: 499–503Google Scholar
  55. Hurt, EC, Allison, DS, Muller, U and Schatz, G (1987) Amino-terminal deletions in the presequence of an imported mitochondrial protein block, the targeting function and proteolytic cleavage of the presequence at the carboxy terminus. J Biol Chem 262: 1420–1424Google Scholar
  56. Jansen, T, Rother, C, Steppuhn, J, Reinke, H, Beyreuther, K, Jansson, C, Andersson, B and Herrmann, RG (1987) Nucleotide sequence of cDNA clones encoding the complete ‘23 kDa’ and ‘16 kDa’ precursor proteins associated with the photosynthetic oxygen-evolving complex from spinach. FEBS Lett 216: 234–240Google Scholar
  57. Josefsson, L-G and Randall, LL (1981) Differential exported protein in E. coli show differences in the temporal mode of processing in vivo. Cell 25: 151–157Google Scholar
  58. Karlin-Neumann, G and Tobin, EM (1986) Transit peptides of nuclear-encoded chloroplast proteins share a common amino acid framework. EMBO J 5: 1343–1350Google Scholar
  59. Kleene, R, Pfanner, N, Pfaller, R, Link, TA, Sebald, W, Neupert, W and Tropshug, M (1987) Mitochondrial porin of Neurospora crassa: cDNA cloning, in vitro expression and import into mitochondria. EMBO J 6: 2627–2633Google Scholar
  60. Klosgen, RB, Gierl, A, Schwarz-Sommer, Z and Saedler, H (1986) Molecular analysis of the waxy locus of Zea mays. Mol Gen Genet 203: 237–244Google Scholar
  61. Kohorn, BD and Tobin, EM (1986) Chloroplast import of light-harvesting chlorophyll a/b-proteins with different amino termini and transit peptides. Plant Physiol 82: 1172–1174Google Scholar
  62. Kohorn, BD, Harel, E, Chitnis, PR, Thornber, JP and Tobin, EM (1986) Functional and mutational analysis of the light-harvesting chlorophyll a/b protein of thylakoid membranes. J Cell Biol 102: 972–981Google Scholar
  63. Koshland, D and Botstein, D (1982) Evidence for posttranslational translocation of β-lactamase across the bacterial inner membrane. Cell 30: 893–902Google Scholar
  64. Kuntz, M, Simons, A, Schell, J and Schreier, PH (1986) Targeting of protein to chloroplasts in transgenic tobacco by fusion to mutated transit peptide. Mol Gen Genet 205: 454–460Google Scholar
  65. Lamppa, GK and Abad, MS (1987) Processing of a wheat light-harvesting chlorophyll a/b protein precursor by a soluble enzyme from higher plant chloroplasts. J Cell Biol 105: 2641–2648Google Scholar
  66. Lazarow, PB and Fujiki, Y (1985) Biogenesis of peroxisomes. Ann Rev Cell Biol 1: 489–530Google Scholar
  67. Lubben, TH and Keegstra, K (1986) Efficient in vitro import of a cytosolic heat shock protein into pea chloroplasts. Proc Natl Acad Sci USA 83: 5502–5506Google Scholar
  68. Lubben, TH, Bansberg, J and Keegstra, K (1987) Stop transfer regions do not halt translocation of proteins into chloroplasts. Science 238: 112–114Google Scholar
  69. Maher, PA and Singer, SJ (1986) Disulfide bonds and the translocation of proteins across membranes. Proc Natl Acad Sci USA 83: 9001–9005Google Scholar
  70. Marks, DB, Keller, BJ and Hoober, JK (1985) In vitro processing of precursors of thylakoid membrane proteins of Chlamydomonas reinhardtii y-1. Plant Physiol 79: 108–113Google Scholar
  71. Mayfield, SP, Rahire, M, Frank, G, Zuber, H and Rochaix, J-D (1987) Expression of the nuclear gene encoding oxygen-evolving enhancer protein 2 is required for high levels of photosynthetic oxygen evolution in Chlamydomonas reinhardtii. Proc Natl Acad Sci USQA 84: 749–753Google Scholar
  72. Melton, DA, Krieg, PA, Rebagliatiai, MR, Maniatis, T, Zinn, K and Green, MR (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucl Acids Res 12: 7035–7056Google Scholar
  73. Merchant, S and Bogorad, L (1987) The Cu(II)-repressible plastidic cytochrome c. Cloning and sequence of a complementary DNA for the pre-apoprotein. J biol Chem 262: 9062Google Scholar
  74. Mishkind, ML, Wessler, SR and Schmidt, GW (1985) Functional determinants in transit sequences: Import and partial maturation by vascular plant chloroplasts of the ribulose-1,5-bisphosphate carboxylase small subunit of Chlamydomonas. J Cell Biol 100: 226–234Google Scholar
  75. Mishkind, ML, Greer, KS and Schmidt, GW (1987) Cell-free reconstitution of protein transport into chloroplasts. Met Enzymol 148: 274–294Google Scholar
  76. Miura, S, Mori, M and Tatibana, M (1983) Transport of ornithine carbamyltransferase precursor into mitochondria. Stimulation by potassium ion, magnesium ion, and a reticulocyte cytosolic protein(s). J Biol Chem 258: 6671–6674Google Scholar
  77. Nguyen, M and Shore, GC (1987) Import of hybrid vesicular stomatitis G protein to the mitochondrial inner membrane. J Biol Chem 262: 3929–3931Google Scholar
  78. Nguyen, M, Argan, C, Sheffield, W, Bell, A, Shields, D and Shore, G (1987) A signal sequence domain essential for processing, but not import, of mitochondrial pre-ornithine carbamyl transferase. J Cell Biol 104: 1193–1198Google Scholar
  79. Ohba, M and Schatz, G (1987a) Protein import into yeast mitochondria is inhibited by antibodies raised against 45-kD proteins of the outer membrane. EMBO J 6: 2109–2115Google Scholar
  80. Ohba, M and Schatz, G (1987b) Disruption of the outer membrane restores protein import to trypsin-treated yeast mitochondria. EMBO J 6: 2117–2122Google Scholar
  81. Ohta, S and Schatz, B (1984) A purified precursor polypeptide requires a cytosolic protein fraction for import into mitochondria. EMBO J 3: 651–657Google Scholar
  82. Pain, D and Blobel, G (1987) Protein import into chloroplasts requires a chloroplast ATPase. Proc Natl Acad Sci USA 84: 3288–3292Google Scholar
  83. Pain, D, Kanwar, YS and Blobel, G (1988) Identification of a receptor for protein import into chloroplasts and its localization to envelope contact zones. Nature 3313: 232–237Google Scholar
  84. Pfaller, R and Neupert, W (1987) High affinity binding sites involved in the import of porin into mitochondria. EMBO J 6: 2635–2642Google Scholar
  85. Pfanner, N and Neupert, W (1986) Transport of F1-ATPase subunit beta into mitochondria depends on both a membrane potential and nucleoside triphosphates. FEBS Lett 209: 152–156Google Scholar
  86. Pfanner, N and Neupert, W (1987) Distinct steps in the import of ADP/ATP carrier in mitochondria. J Biol Chem 262: 7528–7536Google Scholar
  87. Pfanner, N, Tropschug, M and Neupert, W (1987) Mitochondrial protein import: nucleoside triphosphates are involved in conferring import-competence to precursors. Cell 49: 815–823Google Scholar
  88. Pfisterer, J, Lachmann, P and Kloppstech, K (1982) Transport of proteins into chloroplasts. Binding of nuclear-coded chloroplast proteins to the chloroplast envelope. Eur J Biochem 126: 143–148Google Scholar
  89. Randall, LL (1983) Translocation of domains of nascent periplasmic proteins across the cytoplasmic membrane is independent of elongation. Cell 33: 231–240Google Scholar
  90. Reiss, B, Wasmann, CC and Bohnert, H (1987) Regions in the transit peptide of SSU essential for transport into chloroplasts. Mol Gen Genet 209: 116–121Google Scholar
  91. Riezman, H, Hay, R, Witte, C, Nelson, N and Schatz, G (1983) Yeast mitochondrial outer membrane specifically binds cytoplasmically-synthesized precursors of mitochondrial proteins. EMBO J 2: 1113–1118Google Scholar
  92. Robinson, C and Ellis, RJ (1984a) Transport of proteins into chloroplasts. Partial purification of a chloroplast protease involved in the processing of imported precursor polypeptides. Eur J Biochem 142: 337–342Google Scholar
  93. Robinson, C and Ellis, RJ (1984b) Transport of protein into chloroplasts. The precursor of small subunit of ribulose bisphosphate carboxylase is processed to the mature size in two steps. Eur J Biochem 142: 343–346Google Scholar
  94. Robinson, C and Ellis, RJ (1985) Transport of proteins into chloroplasts. The effect of incorporation of amino acid analogues on the import and processing of chloroplast polypeptides. Eur J Biochem 152: 67–73Google Scholar
  95. Roise, D, Horvath, SJ, Tomich, JM, Richards, JH and Schatz, G (1986) A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers. EMBO J 5: 1327–1334Google Scholar
  96. Rothblatt, JA and Meyer, DI (1986) Secretion in yeast: translocation and glycosylation of prepro-α-factor in vitro can occur via an ATP-dependent post-translational mechanism, EMBO J 5: 1031–1036Google Scholar
  97. Rother, C, Jansen, T, Tyagi, A, Tittgen, J and Hermann, RG (1986) Plastocyanin is encoded by an uninterrupted nuclear gene in spinach. Curr Genet 11: 171–176Google Scholar
  98. Rothman, JE and Kornberg, RD (1986) An unfolding story of protein translocation. Nature 322: 209–210Google Scholar
  99. Rothstein, SJ, Gatenby, AA, Willey, DL and Gray, JC (1985) Binding of pea cytochrome f to the inner membrane of Escherichia coli requires the bacterial secA gene product. Proc Natl Acad Sci USA 82: 7955–7959Google Scholar
  100. Schatz, G (1986) Protein translocation. A common mechanism for different membrane systems? Nature 321: 108–109Google Scholar
  101. Schatz, G (1987) Signals guiding proteins to their correct locations in mitochondria. Eur J Biochem 165: 1–6Google Scholar
  102. Schindler, C and Soll, J (1986) Protein transport in intact, purified pea etioplasts. Arch Biochem Biophys 247: 211–220Google Scholar
  103. Schleyer, M and Neupert, W (1985) Transport of proteins into mitochondria: translocational intermediates spanning contact sites between outer and inner membranes. Cell 43: 339–350Google Scholar
  104. Schmidt, GW and Mishkind, ML (1986) The transport of proteins into chloroplasts. Ann Rev Biochem 55: 879–912Google Scholar
  105. Schreier, PH, Seftor, EA, Schell, J and Bohnert, HJ (1985) The use of nuclear-encoded sequence to direct the light-regulated synthesis and transport of a foreign protein into plant chloroplasts. EMBO J 4: 25–32Google Scholar
  106. Schwaiger, M, Herzog, V and Neupert, W (1987) Characterization of translocation contact sites involved in the import of mitochondrial proteins. J Cell Biol 105: 235–246Google Scholar
  107. Singer, SJ, Maher, PA and Yaffe, MP (1987) On the translocation of proteins across membranes. Proc Natl Acad Sci USA 84: 1015–1019Google Scholar
  108. Smeekens, S, de, Groot, M, van, Binsbergen, J and Weisbeek, P (1985) Sequence of the precursor of the chloroplast thylakoid lumen protein plastocyanin. Nature 317: 456–458Google Scholar
  109. Smeekens, S, Bauerle, H, Hageman, J, Keegstra, K and Weisbeek, P (1986) The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell 46: 365–375Google Scholar
  110. Smeekens, S, van, Steeg, H, Bauerle, C, Bettenbroek, H, Keegstra, K and Weisbeek, P (1987) Import into chloroplasts of a yeast mitochondrial protein directed by ferredoxin and plastocyanin transit peptides. Plant Mol Biol 9: 377–388Google Scholar
  111. Strzalka, K, Ngernprasirtsiri, J, Watanabe, A and Akazawa, T (1988) Sycamore amylopalsts can import and process precursors of nuclear encoded chloroplast proteins. Biochem Biophys Res Commun, 149: 799–806Google Scholar
  112. Sztul, ES, Hendrick, JP, Kraus, JP, Wall, D, Kalousek, F and Rosenberg, LE (1987) Import of pre-ornithine transcarbamylase into mitochondria: Two step processing of the leader peptide. J Cell Biol 105: 2631–2639Google Scholar
  113. Tamm, LK (1986) Incorporation of a synthetic mitochondrial signal peptide into charged and uncharged phospholipid monolayers. Biochemistry 25: 7470Google Scholar
  114. Tyagi, A, Hermans, J, Steppuhn, J, Hansson, C, Vater, F and Herrmann, RG (1987) Nucleotide sequence of cDNA clones encoding the complete ‘33 kDa’ precursor protein associated with the photosynthetic oxygen-evolving complex from spinach. Mol Gen Genet 207: 288–293Google Scholar
  115. Van den, Broeck, G, Timko, MP, Kausch, AP, Cashmore, AR, Van, Montagu, M and 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: 358–363Google Scholar
  116. van, Loon, APGM and Schatz, G (1987) Transport of proteins to the mitochondrial intermembrane space: the ‘sorting’ domain of the cytochrome cl presequence is a stop-transfer sequence specific for the mitochondrial inner membrane. EMBO J 6: 2441–2448Google Scholar
  117. Van, Steeg, H, Oudshoorn, P, Van, Hell, B, Polman, JEM and Grivell, LA (1986) Targeting efficiency of a mitochondrial pre-sequence is dependent on the passenger protein. EMBO J 5: 3643–3650Google Scholar
  118. Vassarotti, A, Chen, W-J, Smagula, C and Douglas, MG (1987a) Sequences distal to the mitochondrial targeting sequences are necessary for the maturation of the F1-ATPase beta-subunit precursor in mitochondria. J Biol Chem 262: 411–418Google Scholar
  119. Vassarotti, A, Storoud, R and Douglas, M (1987b) Independent mutations at the amino terminus of a protein act as surrogate signals for mitochondrial import. EMBO J 6: 705–711Google Scholar
  120. Verner, K and Schatz, G (1987) Import of an incompletely folded precursor protein into isolated mitochondria requires an energized inner membrane, but no added. EMBO J 6: 2449–2456Google Scholar
  121. von, Heijne, G (1985) Structural and thermodynamic aspects of the transfer of proteins into and across membranes. In Current Topics in Membranes and Transport, Vol 24, Academic Press, New York, pp 151–179Google Scholar
  122. von, Heijne, G (1986a) Why mitochondria need a genome. FEBS Lett 198: 1–4Google Scholar
  123. von, Heijne, G (1986b) Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 5: 1335–1342Google Scholar
  124. Walter, P and Lingappa, VR (1986) Mechanisms of protein translocation across the endoplasmic reticulum membrane. Ann Rev Cell Biol 2: 499–516Google Scholar
  125. Walter, P, Gilmore, R and Blobel, G (1984) Protein translocation across the endoplasmic reticulum. Cell 38: 5–8Google Scholar
  126. Wasmann, CC, Reiss, B, Bartlett, SG and Bohnert, HJ (1986) The importance of the transit peptide and the transported protein for protein import into chloroplasts. Mol Gen Genet 205: 446–463Google Scholar
  127. Waters, MG and Blobel, G (1986) Secretory protein translocation in a yeast cell-free system can occur posttranslationally and requires ATP hydrolysis. J Cell Biol 102: 1543–1550Google Scholar
  128. Weisbeek, P and Smeekens, S (1988) Protein transport toward the thylakoid lumen: Posttranslational translocation in tandem. Photosyn Res 16: 177–186Google Scholar
  129. Weisbeek, P, Hageman, J, Cremers, F, Keegstra, K, Bauerle, C and Smeekens, S (1986) Nuclear-encoded chloroplast proteins: genes, transport and localization. Curr Top Plant Biochem Physiol, Vol 5. University of Missouri, Columbia, pp 88–104Google Scholar
  130. Werner-Washburne, M, Cline, K and Keegstra, K (1983) Analysis of pea chloroplast inner and outer envelope membrane proteins by two-dimensional gel electrophoresis and their comparison with stromal proteins. Plant Physiol 73: 569–575Google Scholar
  131. Wiedmann, M, Kurzchalia, TV, Hartmann, E and Rapoport, TA (1987) A signal sequence receptor in the endoplasmic reticulum membrane. Nature 328: 831–833Google Scholar
  132. Zimmermann, R, Hennig, B and Neupert, W (1981) Different transport pathways of individual precursor proteins in mitochondria. Eur J Biochem 116: 455–460Google Scholar

Copyright information

© Kluwer Academic Publishers 1988

Authors and Affiliations

  • Michael L. Mishkind
    • 1
  • Scott E. Scioli
    • 1
  1. 1.Department of Biochemistry and MicrobiologyCook College, Rutgers UniversityNew BrunswickUSA

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