Skip to main content
Log in

Targeting of proteins into and across the thylakoid membrane — a multitude of mechanisms

Plant Molecular Biology Aims and scope Submit manuscript

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

References

  1. Alt J, Herrmann RG: Nucleotide sequence of the gene for pre-apocytochrome f in the spinach plastid genome. Curr Genet 8: 551–557 (1984).

    Google Scholar 

  2. Barbrook A, Packer JC, Howe CJ: Components of the protein translocation machinery in the thermophilic cyanobacterium Phormidium laminosum. Biochem Biophys Res Comm 197: 874–877 (1993).

    Google Scholar 

  3. Bartling D, Clausmeyer S, Oelmüller R, Herrmann RG: Towards epitope models for chloroplast transit sequences. Bot Mag Tokyo 2: 119–144 (1990).

    Google Scholar 

  4. Bassham DC, Bartling D, Mould RM, Dunbar B, Weisbeek P, Herrmann RG, Robinson C: Transport of proteins into chloroplasts: delineation of envelope transit and thylakoid transfer signals within the presequences of three imported thylakoid lumen proteins. J Biol Chem 266: 23606–23610 (1991).

    Google Scholar 

  5. Blobel G, Dobberstein B: 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 (1975).

    Google Scholar 

  6. Briggs LM, Pecoraro VL, McIntosh L: Copper-induced expression, cloning and regulatory studies of the plastocyanin gene from the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 15: 633–642 (1990).

    Google Scholar 

  7. Cai D, Herrmann RG, Klösgen RB: The 20 kDa apoprotein of the CP24 complex of photosystem II: an alternative model to study import and intra-organellar routing of nuclear-encoded thylakoid proteins. Plant J 3: 383–392 (1993).

    Google Scholar 

  8. Chitnis PR, Nechushtai R, Thornber JP: Insertion of the precursor of the light-harvesting chlorophyll a/b protein into the thylakoids requires the presence of a developmentally regulated stromal factor. Plant Mol Biol 10: 3–11 (1987).

    Google Scholar 

  9. Chua N-H, Schmidt GW: 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 (1978).

    Google Scholar 

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

    Google Scholar 

  11. Cline K, Ettinger WF, Theg SM: Protein-specific energy requirements for protein transport across or into thylakoid membranes. Two lumenal proteins are transported in the absence of ATP. J Biol Chem 267: 2688–2696 (1992).

    Google Scholar 

  12. Cline K, Henry R, Li C, Yuan J: Multiple pathways for protein transport into or across the thylakoid membrane. EMBO J 12: 1405–4114 (1993).

    Google Scholar 

  13. Cozens AL, Walker JE: The organisation and sequence of the genes for ATP synthase subunits in the cyanobacterium Synechococcus 6301. J Mol Biol 194: 359–383 (1987).

    Google Scholar 

  14. de Boer D, Cremers F, Teerstra R, Smits J, Hille J, Smeekens S, Weisbeek P: In vivo import of plastocyanin and a fusion protein into developmentally different plastids of transgenic plants. EMBO J 7: 2631–2635 (1988).

    Google Scholar 

  15. Flachmann R, Michalowski CB, Löffelhardt W, Bohnert HJ: Sec Y, an integral subunit of the bacterial preprotein translocase, is encoded by a plastid genome. J Biol Chem 268: 7514–7519 (1993).

    Google Scholar 

  16. Franklin AE, Hoffman NE: Chloroplasts contain a homolog of the 54 kD subunit of the signal recognition particle. J Biol Chem 268: 22175–22180 (1993).

    Google Scholar 

  17. Haehnel W, Jansen T, Gause K, Klösgen RB, Stahl B, Michl D, Huvermann B, Karas M, Herrmann RG: Electron transfer from plastocyanin to photosystem I. EMBO J 13: 1028–1038 (1994).

    Google Scholar 

  18. Hageman J, Baecke C, Ebskamp M, Pilon R, Smeekens S, Weisbeek P: Protein import into and sorting inside the chloroplast are independent processes. Plant Cell 2: 479–494 (1990).

    Google Scholar 

  19. Hageman J, Robinson C, Smeekens S, Weisbeek P: A thylakoid processing protease is required for complete maturation of the lumen protein plastocyanin. Nature 324: 567–569 (1986).

    Google Scholar 

  20. Halpin C, Elderfield PD, James HE, Zimmermann R, Dunbar B, Robinson C: The reaction specificities of the thylakoidal processing peptidase and Escherichia coli leader peptidase are identical. EMBO J 8: 3917–3921 (1989).

    Google Scholar 

  21. Hand JM, Szabo LJ, Vasconcelos AC, Cashmore AR: The transit peptide of a chloroplast thylakoid membrane protein is functionally equivalent to a stromal-targeting sequence. EMBO J 8: 3195–3206 (1989).

    Google Scholar 

  22. Hennig J, Herrmann RG: Chloroplast ATP synthase of spinach contains nine nonidentical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement. Mol Gen Genet 203: 117–128 (1986).

    Google Scholar 

  23. Herrmann RG, Steppuhn J, Herrmann GS, Nelson N: The nuclear-encoded polypeptide CFoII from spinach is a real, ninth subunit of chloroplast ATP synthase. FEBS Lett 326: 192–198 (1993).

    Google Scholar 

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

    Google Scholar 

  25. Howe G, Merchant S: Maturation of thylakoid lumen proteins proceeds post-translationally through an intermediate in vivo. Proc Natl Acad Sci USA 90: 1862–1866 (1993).

    Google Scholar 

  26. Huang L, Adam Z, Hoffman NE: Deletion mutants of chlorophyll a/b binding proteins are efficiently imported into chloroplasts but do not integrate into thylakoid membranes. Plant Physiol 99: 247–255 (1992).

    Google Scholar 

  27. Hulford A, Hazell L, Mould RM, Robinson C: Two distinct mechanisms for the translocation of proteins across the thylakoid membrane, one requiring the presence of a stromal protein factor and nucleotide triphosphates. J Biol Chem 269: 3251–3256 (1994).

    Google Scholar 

  28. James HE, Bartling D, Musgrove JE, Kirwin PM, Herrmann RG, Robinson C: Transport of proteins into chloroplasts: import and maturation of precursors to the 33-, 23-, and 16-kDa proteins of the photosynthetic oxygen-evolving complex. J Biol Chem 264: 19573–19576 (1989).

    Google Scholar 

  29. Johnson K, Murphy CK, Beckwith J: Protein export in E. coli. Curr Opin Biotechnol 3: 481–485 (1992).

    Google Scholar 

  30. Kang P-J, Ostermann J, Shilling J, Neupert W, Craig EA, Pfanner N: Requirement for hsp70 in the mitochondrial matrix for translocation and folding of proteins. Nature 348: 137–143. (1990).

    Google Scholar 

  31. Kirwin PM, Meadows JW, Shackleton JB, Musgrove JE, Elderfield PD, Mould R, Hay NA, Robinson C: ATP-dependent import of a lumenal protein by isolated thylakoid vesicles. EMBO J 8: 2251–2255 (1989).

    Google Scholar 

  32. Klösgen RB, Brock IW, Herrmann RG, Robinson C: Proton gradient-driven import of the 16kDa oxygen-evolving complex protein as the full precursor protein by isolated thylakoids. Plant Mol Biol 18: 1031–1034 (1992).

    Google Scholar 

  33. Klösgen RB, Saedler H, Weil J-H: The amyloplast-targeting transit peptide of the waxy protein of maize also mediates protein import in vitro into chloroplasts. Mol Gen Genet 217: 155–161 (1989).

    Google Scholar 

  34. Knott TG, Robinson C: The SecA inhibitor, azide, reversibly blocks the translocation of a subset of lumenal proteins across the thylakoid membrane. J Biol Chem 269: 7843–7846 (1994).

    Google Scholar 

  35. Ko K, Cashmore AR: Targeting of proteins to the thylakoid lumen by the bipartite transit peptide of the 33 kDa oxygen-evolving protein. EMBO J 8: 3187–3194 (1989).

    Google Scholar 

  36. Konishi T, Watanabe A: Transport of proteins into the thylakoid lumen: stromal processing and energy requirements for the import of the precursor to the 23 kDa protein of PSII. Plant Cell Physiol 34: 315–319 (1993).

    Google Scholar 

  37. Kuwabara T, Reddy KJ, Sherman LA: Nucleotide sequence of the gene from the cyanobacterium Anacystis nidulans R2 encoding the Mn-stabilising protein involved in photosystem II water oxidation. Proc Natl Acad Sci USA 84: 8230–8234 (1987).

    Google Scholar 

  38. Lamppa GK: The chlorophyll a/b-binding protein inserts into the thylakoids independent of its cognate transit peptide. J Biol Chem 263: 14996–14999 (1988).

    Google Scholar 

  39. Luirink JL, Dobberstein B: Mammalian and Escherichia coli signal recognition particles. Mol Microbiol 11: 9–13 (1994).

    Google Scholar 

  40. Michl D, Robinson C, Shackleton JB, Herrmann RG, Klösgen RB: Targeting of proteins to thylakoids by bipartite presequences: CFoII is imported by a novel, third pathway. EMBO J 13: 1310–1317 (1994).

    Google Scholar 

  41. Mould RM, Robinson C: A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane. J Biol Chem 266: 12189–12193 (1991).

    Google Scholar 

  42. Mould RM, Shackleton JB, Robinson C: Transport of proteins into chloroplasts: requirements for the efficient import of two lumenal oxygen-evolving complex proteins into isolated thylakoids. J Biol Chem 266: 17286–17289 (1991).

    Google Scholar 

  43. Nakai M, Sugita D, Omata T, Endo T: Sec Y protein is localised in both the cytoplasmic and thylakoid membranes in the cyanobacterium Synechococcus PCC7942. Biochem Biophys Res Comm 193: 228–234 (1993).

    Google Scholar 

  44. Nielsen VS, Mant A, Knoetzel J, Møller BL, Robinson C: Import of barley photosystem I subunit N into the thylakoid lumen is mediated by a bipartite presequence lacking an intermediate cleavage site: role of the delta pH in translocation across the thylakoid membrane. J Biol Chem 269: 3762–3766 (1994).

    Google Scholar 

  45. Oliver DB, Cabelli RJ, Dolan KM, Jarosuk GP: Azideresistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc Natl Acad Sci USA 87: 8227–8231 (1990).

    Google Scholar 

  46. Payan LA, Cline K: A stromal protein factor maintains the solubility and insertion competence of an imported thylakoid membrane protein. J Cell Biol 112: 603–613 (1991).

    Google Scholar 

  47. Robinson C, Cai D, Hulford A, Brock IW, Michl D, Hazell L, Schmidt I, Herrmann RG, Klösgen RB: The presequence of a chimeric construct dictates which of two mechanisms is utilised for translocation across the thylakoid membrane: evidence for the existence of two distinct translocation systems. EMBO J 13: 279–285 (1994).

    Google Scholar 

  48. Rothstein SJ, Gatenby AA, Willey DL, Gray JC: 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 (1985).

    Google Scholar 

  49. Scaramuzzi CD, Hiller RG, Stokes HW: Identification of a chloroplast-encoded secA gene homologue in a chromophytic alga: possible role in chloroplast protein translocation. Curr Genet 22: 421–426 (1992).

    Google Scholar 

  50. Seidler A, Michel H: Expression in Escherichia coli of the psbO gene encoding the 33 kd protein of the oxygen-evolving complex from spinach. EMBO J 9: 1743–1748 (1990).

    Google Scholar 

  51. Smeekens S, Bauerle C, Hageman J, Keegstra K, Weisbeek P: The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell 46: 365–375 (1986).

    Google Scholar 

  52. Theg SM, Bauerle C, Olsen LJ, Selman BR, Keegstra K: Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes. J Biol Chem 264: 6730–6736 (1989).

    Google Scholar 

  53. Valentin K: SecA is plastid-encoded in a red alga: implications for the evolution of plastid genomes and the thylakoid protein import apparatus. Mol Gen Genet 236: 245 (1993).

    Google Scholar 

  54. Viitanen PV, Doran ER, Dunsmuir P: What is the role of the transit peptide in thylakoid integration of the light-harvesting chlorophyll a/b protein? J Biol Chem 263: 15000–15007 (1988).

    Google Scholar 

  55. Von Heijne G, Steppuhn J, Herrmann RG: Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180: 535–545 (1989).

    Google Scholar 

  56. Willey DL, Howe CJ, Auffret AD, Bowman CM, Dyer TA, Gray JC: Location and nucleotide sequence of the gene for cytochrome f in wheat chloroplast DNA. Mol Gen Genet 194: 416–422 (1984).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Robinson, C., Klösgen, R.B. Targeting of proteins into and across the thylakoid membrane — a multitude of mechanisms. Plant Mol Biol 26, 15–24 (1994). https://doi.org/10.1007/BF00039516

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00039516

Key words

Navigation