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Import of Polypeptides into Chloroplasts

Bio/Technology volume 3, pages 803–808 (1985)Cite this article

Abstract

The majority of the protein components of chloroplasts are synthesized outside the organelle and are subsequently imported. These imported polypeptides are produced as precursors containing an amino-terminal extension. Recent experiments have demonstrated that foreign polypeptides can be imported into chloroplasts when fused to these amino-terminal extensions. This ability provides exciting opportunities for improvement of economically important plants through genetic manipulation.

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References

  1. Ellis, R.J. 1981. Chloroplast proteins: synthesis, transport and assembly. Annu. Rev. Plant Physiol. 32: 111–137.

    Article  CAS  Google Scholar 

  2. Cashmore, A.R. 1976. Protein synthesis in plant leaf tissue: The sites of synthesis of the major proteins. J. Biol. Chem. 251: 2848–2853.

    CAS  PubMed  Google Scholar 

  3. Van den Broeck, G., Timko, M.P., Kausch, A.P., Cashmore, A.R., Van Montagu, M. 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-bisphosphate carboxylase. Nature 313: 358–363.

    Article  CAS  Google Scholar 

  4. Schreier, P.H., Seftor, E.A., Schell, J. and Bohnert, H.J. 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.

    Article  CAS  Google Scholar 

  5. 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.

    Article  CAS  Google Scholar 

  6. Cashmore, A.R., Broadhurst, M.K. and Gray, R.E. 1978. Cell-free synthesis of leaf protein. Identification of an apparent precursor of the small subunit of ribulose-1,5-bisphosphate carboxylase. Proc. Natl. Acad. Sci. USA 75: 655–659.

    Article  CAS  Google Scholar 

  7. Highfield, P.E. and Ellis, R.J. 1978. Synthesis and transport of the small subunit of ribulose bisphosphate carboxylase. Nature 27: 420–424.

    Article  Google Scholar 

  8. Chua, N.-H. and Schmidt, G.W. 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.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Apel, K. and Kloppstech, K. 1978. Light-induced appearance of mRNA coding for the apoprotein of the light-harvesting chlorophyll a/b protein. Eur. J. Biochem. 85: 581–588.

    Article  CAS  Google Scholar 

  11. Schmidt, G.W., Bartlett, S.G., Grossman, A.R., Cashmore, A.R. and Chua, N.-H. 1981. Biosynthetic pathways of two polypeptide subunits of the light-harvesting chlorophyll a/b protein complex. J. Cell Biol. 91: 468–478.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Grossman, A.R., Bartlett, S., Schmidt, G.W., Mullet, J.E. and Chua, N.-H. 1982. Optimal conditions for post-translational uptake of proteins by isolated chloroplasts. J. Biol. Chem. 257: 1558–1563.

    CAS  PubMed  Google Scholar 

  14. Westhoff, P., Jansson, C., Klein-Hitpass, L., Berzborn, R., Larsson, C. and Bartlett, S. 1985. Intracellular coding sites of polypeptides associated with photosynthetic oxygen evolution of photosystem II. Plant Mol. Biol. 4: 137–146.

    Article  CAS  Google Scholar 

  15. Hauska, G.A., McCarty, R.E., Berzborn, R.J. and Racker, E. 1971. The function of plastocyanin and its interaction with a specific antibody. J. Biol. Chem. 246: 3524–3531.

    CAS  PubMed  Google Scholar 

  16. Cline, K., Werner-Washburne, M., Lubben, T.H. 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.

    CAS  PubMed  Google Scholar 

  17. Nelson, N. and Schatz, G. 1979. Energy-dependent processing of cytoplasmically made precursors to mitochondrial proteins. Proc. Natl. Acad. Sci. USA 76: 4365–4369.

    Article  CAS  Google Scholar 

  18. Schleyer, M., Schmidt, B. and Neupert, W. 1982. Requirement of a membrane potential for the post-translational transfer of proteins into mitochondria. Eur. J. Biochem. 125: 109–116.

    Article  CAS  Google Scholar 

  19. Kolansky, D.M., Conboy, J.G., Fenton, W.A. and Rosenberg, L.E. 1982. Energy-dependent translocation of the precursor of ornithine transcarbamylase by isolated rat liver mitochondria. J. Biol. Chem. 257: 8467–8471.

    CAS  PubMed  Google Scholar 

  20. Gasser, S.M., Daum, G. and Schatz, G. 1982. Import of proteins into mitochondria. Energy-dependent uptake of precursors by isolated mitochondria. J. Biol. Chem. 257: 13034–13041.

    CAS  PubMed  Google Scholar 

  21. Date, T., Zwizinski, C., Ludmerer, S. and Wickner, W. 1980. Mechanisms of membrane assembly: Effects of energy poisons on the conversion of soluble M13 coliphage procoate to membrane-bound coat protein. Proc. Natl. Acad. Sci. USA 77: 827–831.

    Article  CAS  Google Scholar 

  22. 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.

    Article  CAS  Google Scholar 

  23. Miura, S., Mori, M. and Tatibana, M. 1983. Transport of ornithine carbamoyltransferase precursor into mitochondria. Stimulation by potassium ion, magnesium ion, and a reticulocyte cytosolic protein(s). J. Biol. Chem. 258: 6671–6674.

    CAS  PubMed  Google Scholar 

  24. Argan, C., Lusty, C.J. and Shore, G.C. 1983. Membrane and cytosolic components affecting transport of the precursor for ornithine carbamyltransferase into mitochondria. J. Biol. Chem. 258: 6667–6670.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  26. Firgaira, F.A., Hendrick, J.P., Kalousek, F., Kraus, J.P. and Rosenberg, L.E. 1984. RNA required for import of precursor proteins into mitochondria. Science 226: 1319–1322.

    Article  CAS  Google Scholar 

  27. Robinson, C. and Ellis, R.J. 1984. 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.

    Article  CAS  Google Scholar 

  28. Robinson, C. and Ellis, R.J. 1984. Transport of proteins into chloroplasts: The precursor of small subunit of ribulose bisphosphate carboxylase is processed to the mature size in two step. Eur. J. Biochem. 142: 343–346.

    Article  CAS  Google Scholar 

  29. Mishkind, M.L., Wessler, S.R. and Schmidt, G.W. 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.

    Article  CAS  Google Scholar 

  30. Gasser, S.M., Ohashi, A., Daum, G., Bohni, P.C., Gibson, J., Reid, G.A., Yonetani, T. and Schatz, G. 1982. Imported mitochondrial proteins cytochrome b2 and cytochrome c1 are processed in two steps. Proc. Natl. Acad. Sci. USA 79: 267–271.

    Article  CAS  Google Scholar 

  31. Ohashi, A., Gibson, J., Gregor, I. and Schatz, G. 1982. Import of proteins into mitochondria. The precursor of cytochrome C1 is processed in two steps, one of them Heme-dependent. J. Biol. Chem. 257: 13042–13047.

    CAS  PubMed  Google Scholar 

  32. Bohni, P., Gasser, S., Leaver, C. and Schatz, G. 1980. A matrix-localized mitochondrial protease processing cytoplasmically-made precursor to mitochondrial proteins, 423–433. In: The Organization and Expression of the Mitochondrial Genome. Kroon, A. M. and Saccone, C. (eds.), Elsevier/North-Holland, Amsterdam.

    Google Scholar 

  33. Bohni, P.C., Daum, G. and Schatz, G. 1983. Import of proteins into mitochondria. Partial purification of a matrix-located protease involved in cleavage of mitochondrial precursor polypeptides. J. Biol. Chem. 258: 4937–4943.

    CAS  PubMed  Google Scholar 

  34. McAda, P.C. and Douglas, M.G. 1982. A neutral metallo endoprotease involved in the processing of an F1-ATPase subunit precursor in mitochondria. J. Biol. Chem. 257: 3177–3182.

    CAS  PubMed  Google Scholar 

  35. Schmidt, G.W., Devillers-Thiery, A., Desruisseaux, H., Blobel, G. and Chua, N.-H. 1979. NH2-terminal amino acid sequences of precursor and mature forms of the ribulose-1,5-bisphosphate carboxylase small subunit from Chlamydomonas reinhardtii. J. Cell Biol. 83: 615–622.

    Article  CAS  Google Scholar 

  36. Coruzzi, G., Broglie, R., Cashmore, A.R. and Chua, N.-H. 1983. Nucleotide sequences of two pea cDNA clones encoding the small subunit of ribulose bisphosphate carboxylase and the major chlorophyll a/b binding thylakoid polypeptide. J. Biol. Chem. 258: 1399–1402.

    CAS  PubMed  Google Scholar 

  37. Cashmore, A.R. 1983. Nuclear genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase, p. 29–38. In: Genetic Engineering of Plants, A. Hollaender, (ed.) Plenum Press.

    Chapter  Google Scholar 

  38. Coruzzi, G., Broglie, R., Edwards, C. and Chua, N.-H. 1984. Tissue-specific and light-regulated expression of a pea nuclear gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase. EMBO J. 4: 1671–l679.

    Article  Google Scholar 

  39. Berry-Lowe, S.L., McKnight, T.D., Shah, D.M. and Meagher, R.B. 1982. The nucleotide sequence, expression, and evolution of one member of a multigene family encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean. J. Mol. Appl. Genet. 1: 483–498.

    CAS  PubMed  Google Scholar 

  40. Broglie, R., Coruzzi, G., Lamppa, G., Keith, B. and Chua, N.-H. 1983. Structural analysis of nuclear genes coding for the precursor to the small subunit of wheat ribulose-1,5-bisphosphate carboxylase. Bio/Technology 1: 55–61.

    Google Scholar 

  41. Stiekema, W.J., Wimpee, C.F. and Tobin, E.M. 1983. Nucleotide sequence encoding the precursor of the small subunit of ribulose-1,5-bisphosphate carboxylase from Lemna gibba L.G-3. Nucl Acids Res. 11: 8051–8061.

    Article  CAS  Google Scholar 

  42. Mazur, V.J. and Chui, C.-F. 1985. Sequence of a genomic DNA clone for the small subunit of ribulose-bis-phosphate carboxylase-oxygenase from tobacco. Nuc. Acids Res. 13: 2373–2386.

    Article  CAS  Google Scholar 

  43. Cashmore, A.R. 1984. Structure and expression of a pea nuclear gene encoding a chlorophyll a/b binding polypeptide. Proc. Natl. Acad. Sci. USA 81: 2960–2964.

    Article  CAS  Google Scholar 

  44. Karlin-Neuman, G.A., Kohorn, B.D., Thornber, J.P. and Tobin, E.M. 1985. A chlorophyll a/b-protein encoded by a gene containing intron with characteristics of a transposable element. J. Mol. Appl. Genet. 3: 45–61.

    Google Scholar 

  45. Lamppa, G.K., Morelli, G. and Chua, N.-H. 1985. Structure and developmental regulation of a wheat gene encoding the major chlorophyll a/b-binding polypeptide. Mol. Cell Biol. 5: 1370–1378.

    Article  CAS  Google Scholar 

  46. Dunsmuir, P. 1985. The petunia chlorophyll a/b binding protein genes: a comparison of Cab genes from different gene families. Nuc. Acids Res. 13: 2503–2518.

    Article  CAS  Google Scholar 

  47. Walter, P., Ibrahimi, I. and Blobel, G. 1981. Translocation of proteins across the endoplasmic reticulum I. Signal recognition protein (SRP) binds to in vitro assembled polysomes synthesizing secretory protein. J. Cell Biol. 91: 545–550.

    Article  CAS  Google Scholar 

  48. von Heijne, G. 1984. Analysis of the distribution of charged residues in the N-terminal region of signal sequences: implications for protein export in prokaryotic and eukaryotic cells. EMBO J. 3: 2315–2318.

    Article  CAS  Google Scholar 

  49. Hurt, E.C., Pesold-Hurt, B. and Schatz, G. 1984. The amino-terminal region of an imported mitochondrial precursor polypeptide can direct cytoplasmic dihydrofolate reductase into the mitochondrial matrix. EMBO J. 3: 3149–3156.

    Article  CAS  Google Scholar 

  50. Hirschberg, J. and McIntosh, L. Molecular basis of herbicide resistance in Amaranthus hybridus. Science 222: 1346–1348.

    Article  CAS  Google Scholar 

  51. Erickson, J.M., Rahire, M., Bennoun, P., Delepelaire, P., Diner, B. and Rochaix, J.-D. 1984. Herbicide resistance in Chlamydomonas reinhardtii results from a mutation in the chloroplast gene for the 32-kilodalton protein of photosystem II. Proc. Natl. Acad. Sci. USA 81: 3617–3621.

    Article  CAS  Google Scholar 

  52. Hallick, R.B. 1984. Chloroplast-coded atrazine resistance in Solanum nigrum: psbA loci from susceptible and resistant biotypes are isogenic except for a single codon change. Nuc. Acids Res. 12: 9489–9496.

    Article  Google Scholar 

  53. Mullet, J.E. and Arntzen, C.J. 1981. Identification of a 32–34-kilodalton polypeptide as a herbicide receptor protein in photosystem II. Biochim. et Biophys. Acta 635: 236–248.

    Article  CAS  Google Scholar 

  54. Pfister, K., Steinback, K.E., Gardner, G. and Arntzen, C.J. 1981. Photoaffinity labeling of an herbicide receptor protein in chloroplast membranes. Proc. Natl. Acad. Sci. USA 78: 981–985.

    Article  CAS  Google Scholar 

  55. Gardner, G. 1981. Azidoatrazine: Photoaffinity label for the site of triazine herbicide action in chloroplasts. Science 211: 937–940.

    Article  CAS  Google Scholar 

  56. Mattoo, A.K., Pick, U., Hoffman-Falk, H. and Edelman, M. 1981. The rapidly metabolized 32,000-dalton polypeptide of the chloroplast is the “proteinaceous shield” regulating photosystem II electron transport and mediating diuron herbicide sensitivity. Proc. Natl. Acad. Sci. USA 78: 1572–1576.

    Article  CAS  Google Scholar 

  57. Steinback, K.E., McIntosh, L., Bogorad, L. and Arntzen, C.J. 1981. Identification of the triazine receptor protein as a chloroplast gene product. Proc. Natl. Acad. Sci. USA 78: 7463–7467.

    Article  CAS  Google Scholar 

  58. Caplan, A., Herrera-Estrella, L., Inze, D., Van Haute, E., Van Montagu, M., Schell, J. and Zambryski, P. 1983. Introduction of genetic material into plant cells. Science 222: 815–821.

    Article  CAS  Google Scholar 

  59. Rao, J.K.M., Hargrave, P.A. and Argos, P. 1983. Will the seven-helix bundle be a common structure for integral membrane proteins? FEBS Lett. 156: 165–169.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Cell Biology, The Rockefeller University, New York, NY, 10021, U.S.A.

    A. Cashmore, L. Szabo, M. Timko & A. Kausch

  2. Laboratorium voor Genetika, Rijsuniversiteit Gent, 9000, Gent, Belgium

    G. Van den Broeck, L. Herrera-Estrella, M. Van Montagu & J. Schell

  3. Max-Planck-Institut fur Zuchtungsforschung, 5000, Koln, 30, FRG

    P. Schreier & J. Schell

  4. Department of Biochemistry, University of Arizona, Tucson, AZ, 85721, U.S.A.

    H. Bohnert

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Cashmore, A., Szabo, L., Timko, M. et al. Import of Polypeptides into Chloroplasts. Nat Biotechnol 3, 803–808 (1985). https://doi.org/10.1038/nbt0985-803

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