Abstract
Many proteins found in the chloroplast are synthesized in the cytoplasm as precursor molecules containing transit peptides. Proteins targeted to the stroma must pass through the two envelope membranes to reach their destination. Proteins located in the chloroplast lumen also have to be transferred across the thylakoid membrane. That is, lumen proteins must cross three biological membranes in order to reach their final location. Recent evidence shows that the routing of plastocyanin towards the lumen involves two post-translational transport processes mediated by two different regions of the transit peptide and two different processing proteases. It is postulated that the genetic information for the plastocyanin precursor, which already contained a signal peptide, was transferred from the endosymbiont to the nucleus. Then a chloroplast-specific targeting-peptide was added.
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References
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
Cline K, Werner-Washburne M, Lubben T and 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
Cline K (1986) Import of proteins in chloroplasts. Membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J Biol Chem 261: 14804–14810
Ellis JR (1981) Chloroplast proteins: synthesis, transport and assembly. Ann Rev Plant Physiol 32: 111–137
Hageman J, Robinson C, Smeekens S and Weisbeek P (1986) A thylakoid-located processing protease is required for complete maturation of the lumen protein plastocyanin. Nature 324: 567–569
Hartl F-U, Schmidt B, Wachter E, Weiss H and Neupert W (1987) Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase. Cell: 939–950
Jansen T, Rother C, Steppuhn J, Reinke H, Beyreuther K, Jansson C, Andersson B and Herrmann R (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
Kaput J, Goltz S and Blobel G (1982) Nucleotide sequence of the yeast nuclear gene for cytochrome c peroxidase precursor. J Biol Chem 257: 15054–15058
Kaiser C, Preuss D, Grisafi P and Botstein D. (1986) Science 235: 312–317
Karlin-Neumann GA and Tobin EM (1986) Transit peptides of nuclear encoded chloroplast proteins share a common amino acid framework. EMBO J 5: 9–13
Mayfield S, Rahire M, Frank G, Zuber H and Rochaix J-D (1987) Cloning of the OEE2 gene from Chlamydomonas. Proc Natl Acad Sci USA 84: 749–753
Merchant S and Bogorad L (1987) The Cu(II)-repressible plastidic cytochrome c. Cloning and sequence of a cDNA for Pre-apoprotein. J Biol chem 262: 9062–9067
Mueckler M and Lodish HF (1986) The human glucose transporter can insert posttranslationally into microsomes. Cell 44: 629–637
Oliver D (1985) Protein secretion in Escherichia coli. Ann Rev Microbiol 39: 615–648
Perara E, Rothman RE and Lingappa VR (1986) Uncoupling of translocation from translation: implications for transport of proteins across membranes. Science 232: 348–352
Rothblatt JA and Meyer DI (1986) Secretion in yeast: translocation and glycolysation of prepro-alpha-factor in vitro can occur via an ATP-dependent post-translational mechanism. EMBO J 5: 1031–1036
Rother C, Jansen T, Tyagi A, Tittgen J and Herrmann R (1986) Plastocyanin is encoded by an uninterrupted nuclear gene in spinach. Curr Genet 11: 171–176
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 Sciences 82: 7955–7959
Sadler I, Suda K, Schatz G, Kaudewitz F and Haid A (1984) Sequencing of the nuclear gene for the cytochrome cl precursor reveals and unusually complex amino-terminal presequence. EMBO J 3: 2137–2143
Schmidt GW and Mishkind M (1986) The transport of proteins into chloroplasts. Ann Rev Biochem 55: 879–912
Schreier PH, Seftor EA, Schell J and 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
Smeekens S, vanSteeg 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
Smeekens S, VanBinsbergen J and Weisbeek P (1985a) The plant ferredoxin precursor: nucleotide sequence of a full length cDNA clone. Nucl Acids Res 13: 3179–3194
Smeekens S, DeGroot M, VanBinsbergen J and Weisbeek P (1985b) Sequence of the precursor of the chloroplast lumen protein plastocyanin. Nature 317: 456–458
Smeekens S, Bauerle C, Hageman J, Keegstra K and Weisbeek P (1986) The role of the transit peptide in the routing of precursors towards different chloroplast compartments. Cell 46: 365–375
Tyagi A, Hermans J, Steppuhn J, Jansson C, Vater F and Herrmann R (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
Van denBroeck G, Timko MP, Kausch AP, Cashmore AR, Montagu Mvan and Herrera-Estrella L (1985) Targeting of foreign protein to chloroplasts by fusion to the transit peptide from the small subunit of ribulose-1,5-biphosphate carboxylase. Nature 313: 358–363
VanLoon A, Brandli A and Schatz G (1986) The presequence of two imported mitochondrial proteins contain information for intracellular and intramitochondrial sorting. Cell 44: 8012–812
VonHeyne G (1982) Signal sequences are not uniformly hydrophobic. J Mol Biol 159: 537–541
Vorst O, Oosterhoff-Teertstra R, Van Kan P, Smeekens S and Weisbeek P (1988) Plastocyanin of Arabidopsis thaliana; isolation and characterization of the gene and chloroplast import of the precursor protein. Gene (in press)
Willey DL, Auffret AD and Gray JC (1984) Structure and topology of cytochrome f in pea chloroplast membranes. Cell 36: 555–562.
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Smeekens, S., Weisbeek, P. Protein transport towards the thylakoid lumen: post-translational translocation in tandem. Photosynth Res 16, 177–186 (1988). https://doi.org/10.1007/BF00039492
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DOI: https://doi.org/10.1007/BF00039492