Skip to main content
SpringerLink
Log in
Book cover

Protein Trafficking in Plant Cells pp 209–221Cite as

Multiple pathways for the targeting of thylakoid proteins in chloroplasts

  • Chapter

Abstract

The assembly of the photosynthetic apparatus requires the import of numerous cytosolically synthesised proteins and their correct targeting into or across the thylakoid membrane. Biochemical and genetic studies have revealed the operation of several targeting pathways for these proteins, some of which are used for thylakoid lumen proteins whereas others are utilised by membrane proteins. Some pathways can be traced back to the prokarytoic ancestors of chloroplasts but at least one pathway appears to have arisen in response to the transfer of genes from the organelle to the nucleus. In this article we review recent findings in this field that point to the operation of a mechanistically unique protein translocase in both plastids and bacteria, and we discuss emerging data that reconcile the remarkable variety of targeting pathways with the natures of the substrate precursor proteins.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

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

    Article  CAS  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).

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  4. Berks BC: A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22: 393–404 (1996).

    Article  PubMed  CAS  Google Scholar 

  5. Bogsch E, Brink S, Robinson C: Pathway specificity for a ApH-dependent precursor thylakoid lumen protein is governed by a’ Sec-avoidance’ motif in the transfer peptide and a’ Sec-incompatible’ mature protein. EMBO J 16: 3851–3858 (1997).

    Article  PubMed  CAS  Google Scholar 

  6. Brink S, Bogsch E, Mant A, Robinson C: Unusual characteristics of aminoterminal and hydrophobic domains in nuclear-encoded thylakoid signal peptides. Eur J Biochem 245:340–348 (1997).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  8. 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).

    Article  CAS  Google Scholar 

  9. Chaal B, Howe CJ: Characterisation of a cDNA encoding the thylakoidal processing peptidase from Arabidopsis thaliana. J Biol Chem 273: 689–692 (1998).

    Article  PubMed  CAS  Google Scholar 

  10. Chaddock AM, Mant A, Karnauchov I, Brink S, Herrmann RG, Klösgen RB, Robinson C: A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the ΔpH-dependent thylakoidal protein translocase. EMBO J 14: 2715–2722 (1995).

    PubMed  CAS  Google Scholar 

  11. Clausmeyer S, Klösgen RB, Herrmann RG: Protein import into chloroplasts. The hydrophilic lumenal proteins exhibit unexpected import and sorting specificities in spite of structurally conserved transit peptides. J Biol Chem 268: 13869–13876 (1989).

    Google Scholar 

  12. 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).

    Article  CAS  Google Scholar 

  13. Clark SA, Theg SM: A folded protein can be transported across the chloroplast envelope and thylakoid membranes. Mol Biol Cell 8: 923–934 (1997).

    PubMed  CAS  Google Scholar 

  14. 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).

    PubMed  CAS  Google Scholar 

  15. 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).

    PubMed  CAS  Google Scholar 

  16. 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 

  17. de Gier J-WL, Valent QA, ovn Heijne G, Luirink J: The E. coli SRP: preferences of a targeting factor. FEBS Letts 408: 1–4 (1997).

    Article  Google Scholar 

  18. de Gier J-WL, Mansournia P, Valent QA, Phillips GJ, Luirink J, von Heijne G: Assembly of a cytoplasmic membrane protein in Escherichia coliis dependent on the signal recognition particle. FEBS Lett 399: 307–309 (1997).

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  20. 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).

    PubMed  CAS  Google Scholar 

  21. 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).

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. 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).

    PubMed  CAS  Google Scholar 

  24. 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).

    PubMed  CAS  Google Scholar 

  25. 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).

    PubMed  CAS  Google Scholar 

  26. 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).

    Article  CAS  Google Scholar 

  27. Henry R, Kapazoglou A, McCaffery M, Cline K: Differences between lumen targeting domains of chloroplast transit peptides determine pathway specificity for thylakoid transport. J Biol Chem 269: 10189–10192 (1994).

    PubMed  CAS  Google Scholar 

  28. Henry R, Carrigan M, McCaffrey M, MaX, Cline K: Targeting determinants and proposed evolutionary basis for the Sec and the delta pH protein transport systems in chloroplast thylakoid membranes. J Cell Biol 136: 823–832 (1997).

    Article  PubMed  CAS  Google Scholar 

  29. 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).

    Article  PubMed  CAS  Google Scholar 

  30. High S, Henry R, Mould RM, Valent QA, Meacock S, Cline K, Gray JC, Luirink J: Chloroplast SRP54 interacts with a specific subset of thylakoid precursor proteins. J Biol Chem 272: 11622–11628 (1997)

    Article  PubMed  CAS  Google Scholar 

  31. Hoffman NE, Franklin AE: Evidence for a stromal GTP requirement for the integration of a chlorophyll a/b binding polypeptide into thylakoid membranes. Plant Physiol 105: 295–304 (1994).

    Article  PubMed  CAS  Google Scholar 

  32. 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).

    Article  PubMed  CAS  Google Scholar 

  33. 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).

    Article  PubMed  CAS  Google Scholar 

  34. 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).

    PubMed  CAS  Google Scholar 

  35. 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).

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  37. Karnauchov I, Cai D, Schmidt I, Herrmann RG, Klösgen RB: The thylakoid translocation of subunit 3 of photosystem I, the psaF gene product, depends on a bipartite transit peptide and proceeds along an azide-sensitive pathway. J Biol Chem 269: 32871–32878 (1994).

    PubMed  CAS  Google Scholar 

  38. Kiefer D, Xintong H, Dalbey R, Kuhn A: Negatively-charged amino acid residues play an active role in orienting the Secindependent Pf3 coat protein in the Escherichia coliinner membrane. EMBO J 16: 2197–2204 (1997).

    Article  PubMed  CAS  Google Scholar 

  39. Kim SJ, Robinson D, Robinson C: An Arabidopsis thalianacDNA encoding PSII-X, a 4.1 kDa component of photosystem II: a bipartite presequence mediates SecA/ΔpH-independent targeting into thylakoids. FEBS Lett 390: 175–178 (1996).

    Article  PubMed  CAS  Google Scholar 

  40. Kim SJ, Robinson C, Mant A: Sec/SRP-independent insertion of two thylakoid membrane proteins bearing cleavable signal peptides. FEBS Lett 424: 105–108 (1998).

    Article  PubMed  CAS  Google Scholar 

  41. Kirwin PM, Elderfield PD, Williams RS, Robinson C: Transport of proteins into chloroplasts. Organization, orientation, and lateral distribution of the plastocyanin processing peptidase in the thylakoid network. J Biol Chem 263: 18128–18132 (1988).

    PubMed  CAS  Google Scholar 

  42. 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).

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  45. 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).

    CAS  Google Scholar 

  46. Kuhn, A: Major coat proteins of bacteriophage Pf3 and M13 as model systems for Sec-independent protein transport. FEMS Micro Rev 17: 185–190 (1995).

    Article  CAS  Google Scholar 

  47. 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).

    Article  PubMed  CAS  Google Scholar 

  48. Laidler V, Chaddock AM, Knott TG, Walker D, Robinson C: A SecY homolog in Arabidopsis thaliana. Sequence of a full-length cDNA clone and import of the precursor protein into chloroplasts. J Biol Chem 270: 17664–17667 (1995).

    Article  PubMed  CAS  Google Scholar 

  49. 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).

    PubMed  CAS  Google Scholar 

  50. Li X, Henry R, Yuan J, Cline K, Hoffman NE: A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the post-translational integration of a protein into thylakoid membranes. Proc Natl Acad Sci USA 92:3789–3793 (1995).

    Article  PubMed  CAS  Google Scholar 

  51. Lorkovic ZJ, Schroder WP, Pakrasi HB, Irrgang K-D, Herrmann RG, Oelmüller R: Molecular characterisation of PSII-W, the only nuclear-encoded component of the photosystem II reaction centre. Proc Natl Acad Sci USA 92: 8930–8934 (1995).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  53. Madueño F, Bradshaw SA, Gray JC: The thylakoid-targeting domain of the chloroplast Rieske iron-sulphur protein is located in the N-terminal hydrophobic region of the mature protein. J Biol Chem 269: 17458–17463 (1994).

    PubMed  Google Scholar 

  54. Mant A, Nielsen VS, Knott TG, Møller BL, Robinson C: Multiple mechanisms for the targeting of photosystem I subunits F, H, K, L, and N into and across the thylakoid membrane. J Biol Chem 269: 27303–27309 (1994).

    PubMed  CAS  Google Scholar 

  55. Mant A, Schmidt I, Herrmann RG, Robinson C, Klösgen RB: Sec-dependent thylakoid protein translocation. ΔpH requirement is dictated by passenger protein and ATP concentration. J Biol Chem 270: 23275–23281 (1995).

    Article  PubMed  CAS  Google Scholar 

  56. Mant A, Robinson C: An Arabidopsis cDNA encodes an apparent polyprotein of two non-identical thylakoid membrane proteins that are associated with photosystem II and homologous to algal ycf32 open reading frames. FEBS Lett 423: 183–188 (1998).

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  58. 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).

    PubMed  CAS  Google Scholar 

  59. Mould RM, Knight JS, Bogsch E, Gray JC: Azide-sensitive thylakoid membrane insertion of chimeric cytochrome f constructs imported by isolated pea chloroplasts. Plant J 11: 1051–1058 (1997).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  61. Nakai M, Goto A, Nohara T, Sugita D, Endo T: Identification of the SecA protein homolog in pea chloroplasts and its possible involvement in thylakoidal protein transport. J Biol Chem 269:31338–31341 (1994).

    PubMed  CAS  Google Scholar 

  62. 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).

    PubMed  CAS  Google Scholar 

  63. Nohara T, Asai T, Nakai M, Sugiura M, Endo T: Cytochrome f encoded by the chloroplast genome is imported into thylakoids via the SecA-dependent pathway. Biochem Biophys Res Comm 224: 474–478 (1996).

    Article  PubMed  CAS  Google Scholar 

  64. Oliver DB, Cabelli RJ, Dolan KM, Jarosuk GP: Azide-resistant 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).

    Article  PubMed  CAS  Google Scholar 

  65. Pay an 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).

    Article  CAS  Google Scholar 

  66. 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).

    PubMed  CAS  Google Scholar 

  67. Robinson D, Karnauchov I, Herrmann RG, Klösgen RB, Robinson C: Protease-sensitive thylakoidal import machinery for the Sec-, ΔpH-and signal recognition particle-dependent protein targeting pathways, but not for CF0 II integration. Plant J 10: 149–155 (1996).

    Article  CAS  Google Scholar 

  68. Roffey RA, Theg SM: Analysis of the import of carboxy-terminal truncations of the 23-kilodalton subunit of the oxygen-evolving complex suggests that its structure is an important determinant for thylakoid transport. Plant Physiol 111: 1329–1338 (1996).

    PubMed  CAS  Google Scholar 

  69. Santini C-L, Ize B, Chanal A, Müller M, Giordano G, Wu L-F: A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli EMBO J 17: 101–112 (1998)

    Article  PubMed  CAS  Google Scholar 

  70. 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).

    Article  PubMed  CAS  Google Scholar 

  71. 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).

    PubMed  CAS  Google Scholar 

  72. Settles MA, Yonetani A, Baron A, Bush DR, Cline K, Martienssen R: Sec-independent protein translocation by the maize Hcf 106 protein. Science 278: 1467–1470 (1997).

    Article  PubMed  CAS  Google Scholar 

  73. 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).

    Article  PubMed  CAS  Google Scholar 

  74. Sommer A, Ne’eman E, Steffens JC, Mayer AM, Harel E: Import, targeting, and processing of a plant polyphenol oxidase. Plant Physiology 105: 1301–1311 (1994).

    Article  PubMed  CAS  Google Scholar 

  75. Ulbrandt ND, Newitt JA, Bernstein HD: The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88: 187–196 (1997).

    Article  PubMed  CAS  Google Scholar 

  76. 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).

    Article  PubMed  CAS  Google Scholar 

  77. van der Vere PS, Bennett TM, Oblong JE, Lamppa GK: A chloroplast processing enzyme involved in precursor maturation shares a zinc-binding motif with a recently recognized family of metalloendopeptidases. Proc Natl Acad Sci USA 92: 7177–7181 (1995).

    Article  Google Scholar 

  78. 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).

    PubMed  CAS  Google Scholar 

  79. Voelker R, Barkan A: Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. EMBO J 14: 3905–3914 (1995).

    PubMed  CAS  Google Scholar 

  80. Voelker R, Mendel-Hartvig J, Barkan A: Transposon-Disruption of a maize nuclear gene, tha l, encoding a chloroplast SecA homologue: in vivo role of cp-SecA in thylakoid protein targeting. Genetics 145: 467–478 (1997).

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  82. von Heijne G: Membrane proteins: from sequence to structure. Annu Rev Biophys Biomol Struct 23: 167–192 (1994).

    Article  Google Scholar 

  83. 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).

    Article  CAS  Google Scholar 

  84. Yuan J, Henry R, McCaffery M, Cline K: SecA homolog in protein transport within chloroplasts: evidence for endosymbiont-derived sorting. Science 266: 796–798 (1994).

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Warwick, Coventry, CV4 7AL, UK

    Colin Robinson, Peter J. Hynds, David Robinson & Alexandra Mant

Authors
  1. Colin Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter J. Hynds
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexandra Mant
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Jürgen Soll

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Robinson, C., Hynds, P.J., Robinson, D., Mant, A. (1998). Multiple pathways for the targeting of thylakoid proteins in chloroplasts. In: Soll, J. (eds) Protein Trafficking in Plant Cells. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5298-3_11

Download citation

  • DOI: https://doi.org/10.1007/978-94-011-5298-3_11

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-6229-9

  • Online ISBN: 978-94-011-5298-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation