Skip to main content
SpringerLink
Log in

Recent developments in chloroplast protein transport

  • Protein Transport
  • Minireview
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

CAT:

chloramphenicol acetyl transferase

CCCP:

carbonylcyanide m-chlorophenylhydrazone

DHFR:

dihydrofolate reductase

EPSP:

5-enol-pyruvylshikimate-3-phosphate

ER:

endoplasmic reticulum

LHCP:

light harvesting chlorophyll a/b apoprotein

NPT:

neomycin phosphotransferase

oATP:

adenosine-2′,3′-dialdehyde-5′-triphosphate

P-inorganic phosphate Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

SSU:

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

SRP:

signal recognition particle

References

  • Allison, DS and Schatz, G (1986) Artificial mitochondrial presequences. Proc Natl Acad Sci USA 83: 9011–9015

    Google Scholar 

  • 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: 709–715

    Google Scholar 

  • 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: 667–670

    Google Scholar 

  • 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: 3117–3121

    Google Scholar 

  • 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 105–115

    Google Scholar 

  • 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: 4038–4047

    Google Scholar 

  • 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: 160–166

    Google Scholar 

  • Blobel, G (1980) Intracellular protein topogenesis. Proc Natl Acad Sci USA 77: 1496–1500

    Google Scholar 

  • 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: 835–851

    Google Scholar 

  • Blobel, G and Dobberstein, B (1975b) Transfer of proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components. J Cell Biol 67: 852–862

    Google Scholar 

  • 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: 13273–13280

    Google Scholar 

  • 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: 340–342

    Google Scholar 

  • 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: 817–822

    Google Scholar 

  • Carde, J-P, Joyard, J and Douce, R (1982) Electron microscopic studies of envelope membranes from spinach plastids. Biol Cell 44: 315–324

    Google Scholar 

  • 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: 803–808

    Google Scholar 

  • 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: 651–658

    Google Scholar 

  • Chen, L and Tai, PC (1987) Evidence for the involvement of ATP in co-translational protein translocation. Nature 328: 164–166

    Google Scholar 

  • 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: 973–980

    Google Scholar 

  • 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: 391–395

    Google Scholar 

  • Chia, CP and Arntzen, CJ (1986) Evidence for two-step processing of nuclear-encoded chloroplast proteins during membrane assembly. J Cell Biol 103: 725–731

    Google Scholar 

  • 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: 982–988

    Google Scholar 

  • 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: 3–11

    Google Scholar 

  • 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: 6110–6114

    Google Scholar 

  • Chua, N-H and Schmidt, GW (1979) Transport of proteins into mitochondria and chloroplasts. J Cell Biol 81: 461–483

    Google Scholar 

  • Cline, K (1986) Import of proteins into chloroplasts: membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J Biol Chem 261: 14804–14810

    Google Scholar 

  • 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: 3691–3696

    Google Scholar 

  • 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: 111–123

    Google Scholar 

  • Colman, A and Robinson, C (1986) Protein import into organelles: hierarchical targeting signals. Cell 46: 321–322

    Google Scholar 

  • 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: 780–785

    Google Scholar 

  • 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: 6873–6877

    Google Scholar 

  • della-Cioppa, G, Kishore, GM, Beachy, RN and Fraley, RT (1987) Protein trafficking in plant cells. Plant Physiol 84: 965–968

    Google Scholar 

  • 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: 1082–1085

    Google Scholar 

  • Douglas, MG (1987) Hydrophobic and hydrophilic signals in protein sorting. Protein Engineering 1: 80–81

    Google Scholar 

  • Douglas, MG, McCammon, M and Vassarotti, A (1986) Targeting proteins into mitochondria. Microbiol Rev 50: 166–178

    Google Scholar 

  • 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 65–104

    Google Scholar 

  • Eilers, M and Schatz, G (1986) Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 322: 228–232

    Google Scholar 

  • 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: 1073–1077

    Google Scholar 

  • Eilers, M and Schatz, G (1988) Protein unfolding and the energeties of protein translocation across biological membranes. Cell 52: 481–483

    Google Scholar 

  • Ellis, RJ (1981) Chloroplast proteins: synthesis, transport and assembly. Ann Rev Plant Physiol 32: 111–137

    Google Scholar 

  • 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 25–39

    Google Scholar 

  • Flugge, UI and Hinz, G (1986) Energy dependence of protein translocation into chloroplasts. Eur J Biochem 160: 563–570

    Google Scholar 

  • Gillespie, LL (1987) Identification of an outer mitochondrial membrane protein that interacts with a synthetic signal peptide. J Biol Chem 262: 7939–7942

    Google Scholar 

  • 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: 16045–16048

    Google Scholar 

  • Grossman, A, Bartlett, SG and Chua, N-H (1980) Energy-dependent uptake of cytoplasmically- synthesized polypeptides by chloroplasts. Nature 285: 625–628

    Google Scholar 

  • 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: 567–569

    Google Scholar 

  • 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: 397–406

    Google Scholar 

  • 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: 939–951

    Google Scholar 

  • Highfield, PE and Ellis, RJ (1978) Synthesis and transport of the small subunit of chloroplast ribulose bisphosphate carboxylase. Nature 271: 420–424

    Google Scholar 

  • 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: 451–459

    Google Scholar 

  • Hurt, EC (1987) Unravelling the role of ATP in post-translational protein translocation. Trends Biochem Sci 12: 369–370

    Google Scholar 

  • Hurt, EC and van, Loon, APGM (1986) How proteins find mitochondria and intramitochondrial compartments. Trends in Biochem Sci 11: 204–207

    Google Scholar 

  • 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: 2061–2068

    Google Scholar 

  • 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: 1343–1350

    Google Scholar 

  • Hurt, EC and Schatz, G (1987) A cytosolic protein contains a cryptic mitochondrial targeting signal. Nature 325: 499–503

    Google Scholar 

  • 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: 1420–1424

    Google Scholar 

  • 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: 234–240

    Google Scholar 

  • 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: 151–157

    Google Scholar 

  • Karlin-Neumann, G and Tobin, EM (1986) Transit peptides of nuclear-encoded chloroplast proteins share a common amino acid framework. EMBO J 5: 1343–1350

    Google Scholar 

  • 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: 2627–2633

    Google Scholar 

  • Klosgen, RB, Gierl, A, Schwarz-Sommer, Z and Saedler, H (1986) Molecular analysis of the waxy locus of Zea mays. Mol Gen Genet 203: 237–244

    Google Scholar 

  • 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: 1172–1174

    Google Scholar 

  • 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: 972–981

    Google Scholar 

  • Koshland, D and Botstein, D (1982) Evidence for posttranslational translocation of β-lactamase across the bacterial inner membrane. Cell 30: 893–902

    Google Scholar 

  • 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: 454–460

    Google Scholar 

  • 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: 2641–2648

    Google Scholar 

  • Lazarow, PB and Fujiki, Y (1985) Biogenesis of peroxisomes. Ann Rev Cell Biol 1: 489–530

    Google Scholar 

  • 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: 5502–5506

    Google Scholar 

  • Lubben, TH, Bansberg, J and Keegstra, K (1987) Stop transfer regions do not halt translocation of proteins into chloroplasts. Science 238: 112–114

    Google Scholar 

  • Maher, PA and Singer, SJ (1986) Disulfide bonds and the translocation of proteins across membranes. Proc Natl Acad Sci USA 83: 9001–9005

    Google Scholar 

  • 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: 108–113

    Google Scholar 

  • 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: 749–753

    Google Scholar 

  • 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: 7035–7056

    Google Scholar 

  • 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: 9062

    Google Scholar 

  • 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: 226–234

    Google Scholar 

  • Mishkind, ML, Greer, KS and Schmidt, GW (1987) Cell-free reconstitution of protein transport into chloroplasts. Met Enzymol 148: 274–294

    Google Scholar 

  • 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: 6671–6674

    Google Scholar 

  • Nguyen, M and Shore, GC (1987) Import of hybrid vesicular stomatitis G protein to the mitochondrial inner membrane. J Biol Chem 262: 3929–3931

    Google Scholar 

  • 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: 1193–1198

    Google Scholar 

  • 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: 2109–2115

    Google Scholar 

  • Ohba, M and Schatz, G (1987b) Disruption of the outer membrane restores protein import to trypsin-treated yeast mitochondria. EMBO J 6: 2117–2122

    Google Scholar 

  • Ohta, S and Schatz, B (1984) A purified precursor polypeptide requires a cytosolic protein fraction for import into mitochondria. EMBO J 3: 651–657

    Google Scholar 

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

    Google Scholar 

  • 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: 232–237

    Google Scholar 

  • Pfaller, R and Neupert, W (1987) High affinity binding sites involved in the import of porin into mitochondria. EMBO J 6: 2635–2642

    Google Scholar 

  • 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: 152–156

    Google Scholar 

  • Pfanner, N and Neupert, W (1987) Distinct steps in the import of ADP/ATP carrier in mitochondria. J Biol Chem 262: 7528–7536

    Google Scholar 

  • Pfanner, N, Tropschug, M and Neupert, W (1987) Mitochondrial protein import: nucleoside triphosphates are involved in conferring import-competence to precursors. Cell 49: 815–823

    Google Scholar 

  • 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: 143–148

    Google Scholar 

  • Randall, LL (1983) Translocation of domains of nascent periplasmic proteins across the cytoplasmic membrane is independent of elongation. Cell 33: 231–240

    Google Scholar 

  • Reiss, B, Wasmann, CC and Bohnert, H (1987) Regions in the transit peptide of SSU essential for transport into chloroplasts. Mol Gen Genet 209: 116–121

    Google Scholar 

  • 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: 1113–1118

    Google Scholar 

  • 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: 337–342

    Google Scholar 

  • 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: 343–346

    Google Scholar 

  • 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: 67–73

    Google Scholar 

  • 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: 1327–1334

    Google Scholar 

  • 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: 1031–1036

    Google Scholar 

  • 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: 171–176

    Google Scholar 

  • Rothman, JE and Kornberg, RD (1986) An unfolding story of protein translocation. Nature 322: 209–210

    Google Scholar 

  • 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: 7955–7959

    Google Scholar 

  • Schatz, G (1986) Protein translocation. A common mechanism for different membrane systems? Nature 321: 108–109

    Google Scholar 

  • Schatz, G (1987) Signals guiding proteins to their correct locations in mitochondria. Eur J Biochem 165: 1–6

    Google Scholar 

  • Schindler, C and Soll, J (1986) Protein transport in intact, purified pea etioplasts. Arch Biochem Biophys 247: 211–220

    Google Scholar 

  • Schleyer, M and Neupert, W (1985) Transport of proteins into mitochondria: translocational intermediates spanning contact sites between outer and inner membranes. Cell 43: 339–350

    Google Scholar 

  • Schmidt, GW and Mishkind, ML (1986) The transport of proteins into chloroplasts. Ann Rev Biochem 55: 879–912

    Google Scholar 

  • 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: 25–32

    Google Scholar 

  • Schwaiger, M, Herzog, V and Neupert, W (1987) Characterization of translocation contact sites involved in the import of mitochondrial proteins. J Cell Biol 105: 235–246

    Google Scholar 

  • Singer, SJ, Maher, PA and Yaffe, MP (1987) On the translocation of proteins across membranes. Proc Natl Acad Sci USA 84: 1015–1019

    Google Scholar 

  • 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: 456–458

    Google Scholar 

  • 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: 365–375

    Google Scholar 

  • 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: 377–388

    Google Scholar 

  • 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: 799–806

    Google Scholar 

  • 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: 2631–2639

    Google Scholar 

  • Tamm, LK (1986) Incorporation of a synthetic mitochondrial signal peptide into charged and uncharged phospholipid monolayers. Biochemistry 25: 7470

    Google Scholar 

  • 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: 288–293

    Google Scholar 

  • 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: 358–363

    Google Scholar 

  • 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: 2441–2448

    Google Scholar 

  • 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: 3643–3650

    Google Scholar 

  • 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: 411–418

    Google Scholar 

  • 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: 705–711

    Google Scholar 

  • 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: 2449–2456

    Google Scholar 

  • 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 151–179

    Google Scholar 

  • von, Heijne, G (1986a) Why mitochondria need a genome. FEBS Lett 198: 1–4

    Google Scholar 

  • von, Heijne, G (1986b) Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 5: 1335–1342

    Google Scholar 

  • Walter, P and Lingappa, VR (1986) Mechanisms of protein translocation across the endoplasmic reticulum membrane. Ann Rev Cell Biol 2: 499–516

    Google Scholar 

  • Walter, P, Gilmore, R and Blobel, G (1984) Protein translocation across the endoplasmic reticulum. Cell 38: 5–8

    Google Scholar 

  • 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: 446–463

    Google Scholar 

  • 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: 1543–1550

    Google Scholar 

  • Weisbeek, P and Smeekens, S (1988) Protein transport toward the thylakoid lumen: Posttranslational translocation in tandem. Photosyn Res 16: 177–186

    Google Scholar 

  • 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 88–104

    Google Scholar 

  • 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: 569–575

    Google Scholar 

  • Wiedmann, M, Kurzchalia, TV, Hartmann, E and Rapoport, TA (1987) A signal sequence receptor in the endoplasmic reticulum membrane. Nature 328: 831–833

    Google Scholar 

  • Zimmermann, R, Hennig, B and Neupert, W (1981) Different transport pathways of individual precursor proteins in mitochondria. Eur J Biochem 116: 455–460

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry and Microbiology, Cook College, Rutgers University, Lipman Hall, 08903, New Brunswick, New Jersey, USA

    Michael L. Mishkind & Scott E. Scioli

Authors
  1. Michael L. Mishkind
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Scott E. Scioli
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mishkind, M.L., Scioli, S.E. Recent developments in chloroplast protein transport. Photosynth Res 19, 153–184 (1988). https://doi.org/10.1007/BF00114573

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00114573

Key words

Search

Navigation