Skip to main content

The Chloroplast Protein Import Machinery: A Review

  • Protocol
  • First Online:
Protein Secretion

Part of the book series: Methods in Molecular Biology ((MIMB,volume 619))

Abstract

Plastids are a heterogeneous family of organelles found ubiquitously in plants and algal cells. Most prominent are the chloroplasts, which carry out such essential processes as photosynthesis and the biosynthesis of fatty acids as well as of amino acids. As mitochondria, chloroplasts are derived from a single endosymbiotic event. They are believed to have evolved from an ancient cyanobacterium, which was engulfed by an early eukaryotic ancestor. During evolution the plastid genome has been greatly reduced and most of the genes have been transferred to the host nucleus. Consequently, more than 98% of all plastid proteins are translated on cytosolic ribosomes. They have to be posttranslationally targeted to and imported into the organelle. Targeting is assisted by cytosolic proteins which interact with proteins destined for plastids and thereby keep them in an import competent state. After reaching the target organelle, many proteins have to conquer the barrier of the chloroplast outer and inner envelope. This process is mediated by complex molecular machines in the outer (Toc complex) and inner (Tic complex) envelope of chloroplasts, respectively. Most proteins destined for the compartments inside the chloroplast contain a cleavable N-terminal transit peptide, whereas most of the outer envelope components insert into the membrane without such a targeting peptide.

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

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and 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 109.99
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

Institutional subscriptions

References

  1. Bölter, B., Soll, J., Hill, K., Hemmler, R., and Wagner, R. (1999) A rectifying ATP-regulated solute channel in the chloroplastic outer envelope from pea. EMBO J 18, 5505–5516.

    Article  PubMed  Google Scholar 

  2. Li, H. M. and Chen, L. J. (1996) Protein targeting and integration signal for the chloroplastic outer envelope membrane. Plant Cell 8, 2117–2126.

    Article  CAS  PubMed  Google Scholar 

  3. Pohlmeyer, K., Soll, J., Steinkamp, T., Hinnah, S., and Wagner, R. (1997) Isolation and characterization of an amino acid-selective channel protein present in the chloroplastic outer envelope membrane. PNAS 94, 9504–9509.

    Article  CAS  PubMed  Google Scholar 

  4. Pohlmeyer, K., Soll, J., Grimm, R., Hill, K., and Wagner, R. (1998) A high-conductance solute channel in the chloroplastic outer envelope from Pea. Plant Cell 10, 1207–1216.

    Article  CAS  PubMed  Google Scholar 

  5. Salomon, M., Fischer, K., Flugge, U. I., and Soll, J. (1990) Sequence analysis and protein import studies of an outer chloroplast envelope polypeptide. PNAS 87, 5778–5782.

    Article  CAS  PubMed  Google Scholar 

  6. Seedorf, M., Waegemann, K., and Soll, J. (1995) A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J 7, 401–411.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  8. Cline, K. (2000) Gateway to the chloroplast. Nature 403, 148–149.

    Article  CAS  PubMed  Google Scholar 

  9. Waegemann, K. and Soll, J. (1996) Phosphorylation of the transit sequence of chloroplast precursor proteins. J Biol Chem 271, 6545–6554.

    Article  CAS  PubMed  Google Scholar 

  10. Fulgosi, H., Soll, J., de Faria, M. S., Korthout, H. A., Wang, M., and Testerink, C. (2002) 14-3-3 proteins and plant development. Plant Mol Biol 50, 1019–1029.

    Article  CAS  PubMed  Google Scholar 

  11. Oreb, M., Hofle, A., Mirus, O., and Schleiff, E. (2008) Phosphorylation regulates the assembly of chloroplast import machinery. J Exp Bot 59, 2309–2316.

    Article  CAS  PubMed  Google Scholar 

  12. vonHeijne, G. (1989) Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature 341, 456–458.

    Article  CAS  Google Scholar 

  13. Pfanner, N., Craig, E. A., and Honlinger, A. (1997) Mitochondrial preprotein translocase. Annu Rev Cell Dev Biol 13, 25–51.

    Article  CAS  PubMed  Google Scholar 

  14. Waegemann, K., Paulsen, H., and Soll, J. (1990) Translocation of proteins into chloroplasts requires cytosolic factors to obtain import competence. FEBS Lett 261, 89–92.

    Article  CAS  Google Scholar 

  15. Pilon, M., de Boer, A. D., Knols, S. L., Koppelman, M. H., van der Graaf, R. M., de Kruijff, B., and Weisbeek, P. J. (1990) Expression in Escherichia coli and purification of a translocation-competent precursor of the chloroplast protein ferredoxin. J Biol Chem 265, 3358–3361.

    CAS  PubMed  Google Scholar 

  16. Pilon, M., Rietveld, A. G., Weisbeek, P. J., and de Kruijff, B. (1992) Secondary structure and folding of a functional chloroplast precursor protein. J Biol Chem 267, 19907–19913.

    CAS  PubMed  Google Scholar 

  17. May, T. and Soll, J. (2000) 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12, 53–64.

    Article  CAS  PubMed  Google Scholar 

  18. Rial, D. V., Ottado, J., and Ceccarelli, E. A. (2003) Precursors with altered affinity for Hsp70 in their transit peptides are efficiently imported into chloroplasts. J Biol Chem 278, 46473–46481.

    Article  CAS  PubMed  Google Scholar 

  19. Schleiff, E., Soll, J., Sveshnikova, N., Tien, R., Wright, S., Dabney-Smith, C., Subramanian, C., and Bruce, B. D. (2002) Structural and guanosine triphosphate/diphosphate requirements for transit peptide recognition by the cytosolic domain of the chloroplast outer envelope receptor, Toc34. Biochemistry 41, 1934–1946.

    Article  CAS  PubMed  Google Scholar 

  20. Schleiff, E., Jelic, M., and Soll, J. (2003) A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proc Natl Acad Sci U S A 100, 4604–4609.

    Article  CAS  PubMed  Google Scholar 

  21. Sohrt, K. and Soll, J. (2000) Toc64, a new component of the protein translocon of chloroplasts. J Cell Biol 148, 1213–1221.

    Article  CAS  PubMed  Google Scholar 

  22. Lamb, J. R., Tugendreich, S., and Hieter, P. (1995) Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem Sci 20, 257–259.

    Article  CAS  PubMed  Google Scholar 

  23. Frydman, J. and Hohfeld, J. (1997) Chaperones get in touch: the Hip-Hop connection. Trends Biochem Sci 22, 87–92.

    Article  CAS  PubMed  Google Scholar 

  24. Qbadou, S., Becker, T., Mirus, O., Tews, I., Soll, J., and Schleiff, E. (2006) The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO J 25, 1836–1847.

    Article  CAS  PubMed  Google Scholar 

  25. Schleiff, E., Soll, J., Kuchler, M., Kuhlbrandt, W., and Harrer, R. (2003) Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol 160, 541–551.

    Article  CAS  PubMed  Google Scholar 

  26. Hinnah, S. C., Wagner, R., Sveshnikova, N., Harrer, R., and Soll, J. (2002) The chloroplast protein import channel Toc75: pore properties and interaction with transit peptides. Biophys J 83, 899–911.

    Article  CAS  PubMed  Google Scholar 

  27. Tranel, P. J., Froehlich, J., Goyal, A., and Keegstra, K. (1995) A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway. EMBO J 14, 2436–2446.

    CAS  PubMed  Google Scholar 

  28. Waegemann, K. and Soll, J. (1996) Phosphorylation of the transit sequence of chloroplast precursor proteins. J Biol Chem 271, 6545–6554.

    Article  CAS  PubMed  Google Scholar 

  29. Eckart, K., Eichacker, L., Sohrt, K., Schleiff, E., Heins, L., and Soll, J. (2002) A Toc75-like protein import channel is abundant in chloroplasts. EMBO Rep 3, 557–562.

    Article  CAS  PubMed  Google Scholar 

  30. Jackson-Constan, D. and Keegstra, K. (2001) Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol 125, 1567–1576.

    Article  CAS  PubMed  Google Scholar 

  31. Baldwin, A., Wardle, A., Patel, R., Dudley, P., Park, S. K., Twell, D., Inoue, K., and Jarvis, P. (2005) A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiol 138, 715–733.

    Article  CAS  PubMed  Google Scholar 

  32. Constan, D., Patel, R., Keegstra, K., and Jarvis, P. (2004) An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J 38, 93–106.

    Article  CAS  PubMed  Google Scholar 

  33. Hust, B. and Gutensohn, M. (2006) Deletion of core components of the plastid protein import machinery causes differential arrest of embryo development in Arabidopsis thaliana. Plant Biol 18–30.

    Google Scholar 

  34. Schleiff, E. and Soll, J. (2005) Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep 6, 1023–1027.

    Article  CAS  PubMed  Google Scholar 

  35. Reumann, S. and Keegstra, K. (1999) The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci 4, 302–307.

    Article  PubMed  Google Scholar 

  36. Patel, R., Hsu, S. C., Bedard, J., Inoue, K., and Jarvis, P. (2008) The omp85-related chloroplast outer envelope protein OEP80 is essential for viability in Arabidopsis. Plant Physiol 148, 235–245.

    Article  CAS  PubMed  Google Scholar 

  37. Hiltbrunner, A., Bauer, J., Alvarez-Huerta, M., and Kessler, F. (2001) Protein translocon at the Arabidopsis outer chloroplast membrane. Biochem Cell Biol 79, 629–635.

    Article  CAS  PubMed  Google Scholar 

  38. Kubis, S., Patel, R., Combe, J., Bedard, J., Kovacheva, S., Lilley, K., Biehl, A., Leister, D., Rios, G., Koncz, C., and Jarvis, P. (2004) Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. The Plant Cell 16, 2059–2077.

    Article  CAS  PubMed  Google Scholar 

  39. Kessler, F., Blobel, G., Patel, H. A., and Schnell, D. J. (1994) Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 266, 1035–1039.

    Article  CAS  PubMed  Google Scholar 

  40. Sveshnikova, N., Soll, J., and Schleiff, E. (2000) Toc34 is a preprotein receptor regulated by GTP and phosphorylation. PNAS 97, 4973–4978.

    Article  CAS  PubMed  Google Scholar 

  41. Hirsch, S., Muckel, E., Heemeyer, F., von Heijne, G., and Soll, J. (1994) A receptor component of the chloroplast protein translocation machinery. Science 266, 1989–1992.

    Article  CAS  PubMed  Google Scholar 

  42. Sun, Y. J., Forouhar, F., Li Hm, H. M., Tu, S. L., Yeh, Y. H., Kao, S., Shr, H. L., Chou, C. C., Chen, C., and Hsiao, C. D. (2002) Crystal structure of pea Toc34, a novel GTPase of the chloroplast protein translocon. Nat Struct Biol 9, 95–100.

    Article  PubMed  Google Scholar 

  43. Jelic, M., Sveshnikova, N., Motzkus, M., Hörth, P., Soll, J., and Schleiff, E. (2002) The chloroplast import receptor Toc34 functions as preprotein regulated GTPase. J Biol Chem 12, 1875–1883

    Google Scholar 

  44. Jarvis, P., Chen, L. J., Li, H., Peto, C. A., Fankhauser, C., and Chory, J. (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282, 100–103.

    Article  CAS  PubMed  Google Scholar 

  45. Gutensohn, M., Schulz, B., Nicolay, P., and Flugge, U. I. (2000) Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. Plant J 23, 771–783.

    Article  CAS  PubMed  Google Scholar 

  46. Dahlin, C. and Cline, K. (1991) Developmental regulation of the plastid protein import apparatus. Plant Cell 3, 1131–1140.

    Article  CAS  PubMed  Google Scholar 

  47. Becker, T., Hritz, J., Vogel, M., Caliebe, A., Bukau, B., Soll, J., and Schleiff, E. (2004) Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts. Mol Biol Cell 15, 5130–5144.

    Article  CAS  PubMed  Google Scholar 

  48. Jackson-Constan, D. and Keegstra, K. (2001) Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol 125, 1567–1576.

    Article  CAS  PubMed  Google Scholar 

  49. Aronsson, H., Boij, P., Patel, R., Wardle, A., Töpel, M., and Jarvis, P. (2007) Toc64/OEP64 is not essential for the efficient import of proteins into chloroplasts in Arabidopsis thaliana. Plant J 52, 53–68.

    Article  CAS  PubMed  Google Scholar 

  50. Chew, O. and Whelan, J. (2004) Just read the message: a model for sorting of proteins between mitochondria and chloroplasts. Trends Plant Sci 9, 318–319.

    Article  CAS  PubMed  Google Scholar 

  51. Qbadou, S., Becker, T., Bionda, T., Reger, K., Ruprecht, M., Soll, J., and Schleiff, E. (2007) Toc64 - A Preprotein-receptor at the outer membrane with bipartide function. J Mol Biol 367, 1330–1346.

    Article  CAS  PubMed  Google Scholar 

  52. Akita, M., Nielsen, E., and Keegstra, K. (1997) Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J Cell Biol 136, 983–994.

    Article  CAS  PubMed  Google Scholar 

  53. Nielsen, E., Akita, M., Davila-Aponte, J., and Keegstra, K. (1997) Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J 16, 935–946.

    Article  CAS  PubMed  Google Scholar 

  54. Teng, Y. S., Su, Y. s., Chen, L. J., Lee, Y. J., Hwang, I., and Li, H. M. (2006) Tic21 is an essential translocon component for protein translocation across the chloroplast inner envelope membrane. Plant Cell 18, 2247–2257.

    Article  CAS  PubMed  Google Scholar 

  55. Duy, D., Wanner, G., Meda, A. R., von Wiren, N., Soll, J., and Philippar, K. (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19, 986–1006.

    Article  CAS  PubMed  Google Scholar 

  56. Lübeck, J., Soll, J., Akita, M., Nielsen, E., and Keegstra, K. (1996) Topology of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane. EMBO J 15, 4230–4238.

    PubMed  Google Scholar 

  57. Kessler, F. and Blobel, G. (1996) Interaction of the protein import and folding machineries of the chloroplast. PNAS 93, 7684–7689.

    Article  CAS  PubMed  Google Scholar 

  58. Heins, L., Mehrle, A., Hemmler, R., Wagner, R., Küchler, M., Hörmann, F., Sveshnikov, D., and Soll, J. (2002) The preprotein conducting channel at the inner envelope membrane of plastids. EMBO J 21, 2616–2625.

    Article  CAS  PubMed  Google Scholar 

  59. Inaba, T., Alvarez-Huerta, M., Li, M., Bauer, J., Ewers, C., Kessler, F., and Schnell, D. J. (2005) Arabidopsis tic110 is essential for the assembly and function of the protein import machinery of plastids. Plant Cell 17, 1482–1496.

    Article  CAS  PubMed  Google Scholar 

  60. Ko, K., Budd, D., Wu, C., Seibert, F., Kourtz, L., and Ko, Z. W. (1995) Isolation and characterization of a cDNA clone encoding a member of the Com44/Cim44 envelope components of the chloroplast protein import apparatus. J Biol Chem 270, 28601–28608.

    Article  CAS  PubMed  Google Scholar 

  61. Stahl, T., Glockmann, C., Soll, J., and Heins, L. (1999) Tic40, a new "old" subunit of the chloroplast protein import translocon. J Biol Chem 274, 37467–37472.

    Article  CAS  PubMed  Google Scholar 

  62. Chou, M. L., Fitzpatrick, L. M., Tu, S. L., Budziszewski, G., Potter-Lewis, S., Akita, M., Levin, J. Z., Keegstra, K., and Li, H. M. (2003) Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J 22, 2970–2980.

    Article  CAS  PubMed  Google Scholar 

  63. Inaba, T., Li, M., Alvarez-Huerta, M., Kessler, F., and Schnell, D. J. (2003) AtTic110 functions as a scaffold for coordinating the stromal events of protein import into chloroplasts. J Biol Chem 278, 38617–38627.

    Article  CAS  PubMed  Google Scholar 

  64. Kovacheva, S., Bedard, J., Patel, R., Dudley, P., Twell, D., Rios, G., Koncz, C., and Jarvis, P. (2005) In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J 41, 412–428.

    Article  CAS  PubMed  Google Scholar 

  65. Bedard, J., Kubis, S., Bimanadham, S., and Jarvis, P. (2007) Functional similarity between the chloroplast translocon component, Tic40, and the human co-chaperone, Hsp70-interacting protein (Hip). J Bio Chem 282, 21404–21414.

    Article  CAS  Google Scholar 

  66. Chiu, C. C. and Li, H. M. (2008) Tic40 is important for reinsertion of proteins from the chloroplast stroma into the inner membrane. Plant J Epub ahead of print.

    Google Scholar 

  67. Chou, M. L., Chu, C. C., Chen, L. J., Akita, M., and Li, H. M. (2006) Stimulation of transit-peptide release and ATP hydrolysis by a cochaperone during protein import into chloroplasts. J Cell Biol 175, 893–900.

    Article  CAS  PubMed  Google Scholar 

  68. Stengel, A., Benz, J. P., Balsera, M., and Soll, J. A. B. B. (2008) Tic62 – Redox regulated translocon composition and dynamics. J Biol Chem 283, 6656–6667.

    Article  CAS  PubMed  Google Scholar 

  69. Hormann, F., Kuchler, M., Sveshnikov, D., Oppermann, U., Li, Y., and Soll, J. (2004) Tic32, an essential component in chloroplast biogenesis. J Biol Chem 279, 34756–34762.

    Article  PubMed  Google Scholar 

  70. Chigri, F., Soll, J., and Vothknecht, U. C. (2005) Calcium regulation of chloroplast protein import. Plant J 42, 821–831.

    Article  CAS  PubMed  Google Scholar 

  71. Chigri, F., Hormann, F., Stamp, A., Stammers, D. K., Bolter, B., Soll, J., and Vothknecht, U. C. (2006) Calcium regulation of chloroplast protein translocation is mediated by calmodulin binding to Tic32. Proc Natl Acad Sci U S A 103, 16051–16056.

    Article  CAS  PubMed  Google Scholar 

  72. Caliebe, A., Grimm, R., Kaiser, G., Lubeck, J., Soll, J., and Heins, L. (1997) The chloroplastic protein import machinery contains a Rieske-type iron-sulfur cluster and a mononuclear iron-binding protein. EMBO J 16, 7342–7350.

    Article  CAS  PubMed  Google Scholar 

  73. Kuchler, M., Decker, S., Hormann, F., Soll, J., and Heins, L. (2002) Protein import into chloroplasts involves redox-regulated proteins. EMBO J 21, 6136–6145.

    Article  PubMed  Google Scholar 

  74. Ding, H., Hidalgo, E., and Demple, B. (1996) The redox state of the [2Fe-2S] clusters in SoxR protein regulates its activity as a transcription factor. J Biol Chem 271, 33173–33175.

    Article  CAS  PubMed  Google Scholar 

  75. Hidalgo, E., Ding, H., and Demple, B. (1997) Redox signal transduction via iron-sulfur clusters in the SoxR transcription activator. Trends Biochem Sci 22, 207–210.

    Article  CAS  PubMed  Google Scholar 

  76. Bartsch, S., Monnet, J., Selbach, K., Quigley, F., Gray, J., von Wettstein, D., Reinbothe, S., and Reinbothe, C. (2008) Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism. Proc Nat Acad Sci 105, 4933–4938.

    Article  CAS  PubMed  Google Scholar 

  77. Balsera, M., Stengel, A., Soll, J., and Bolter, B. (2007) Tic62: a protein family from metabolism to protein translocation. BMC Evol Biol 7, 43.

    Article  PubMed  Google Scholar 

  78. Kouranov, A., Chen, X., Fuks, B., and Schnell, D. J. (1998) Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane. J Cell Biol 143, 991–1002.

    Article  CAS  PubMed  Google Scholar 

  79. Chen, X., Smith, M. D., Fitzpatrick, L., and Schnell, D. J. (2002) In vivo analysis of the role of atTic20 in protein import into chloroplasts. Plant Cell 14, 641–654.

    Article  CAS  PubMed  Google Scholar 

  80. Rassow, J., Dekker, P. J., van Wilpe, S., Meijer, M., and Soll, J. (1999) The preprotein translocase of the mitochondrial inner membrane: function and evolution. J Mol Biol 286, 105–120.

    Article  CAS  PubMed  Google Scholar 

  81. Koehler, C. M. (2000) Protein translocation pathways of the mitochondrion. FEBS Lett 476, 27–31.

    Article  CAS  PubMed  Google Scholar 

  82. Li, M. and Schnell, D. J. (2006) Reconstitution of protein targeting to the inner envelope membrane of chloroplasts. J Cell Biol 175, 249–259.

    Article  CAS  PubMed  Google Scholar 

  83. Lubeck, J., Heins, L., and Soll, J. (1997) A nuclear-coded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle. J Cell Biol 137, 1279–1286.

    Article  CAS  PubMed  Google Scholar 

  84. Tripp, J., Inoue, K., Keegstra, K., and Froehlich, J. E. (2007) A novel serine/proline-rich domain in combination with a transmembrane domain is required for the insertion of AtTic40 into the inner envelope membrane of chloroplasts. Plant J 52 (5), 824–838.

    Google Scholar 

  85. Vojta, L., Soll, J., and Bolter, B. (2007) Requirements for a conservative protein translocation pathway in chloroplasts. FEBS Lett 581, 2621–2624.

    Article  CAS  PubMed  Google Scholar 

  86. Flügge, U., Fischer, K., Gross, A., Sebald, W., Lottspeich, F., and Eckerskorn, C. (1989) The triose phosphate-3-phosphoglycerate-phosphate translocator from spinach chloroplasts: nucleotide sequence of a full-length cDNA clone and import of the in vitro synthesized precursor protein into chloroplasts. EMBO J 8, 39–46.

    PubMed  Google Scholar 

  87. Firlej-Kwoka, E., Strittmatter, P., Soll, J., and Bölter, B. (2008) Import of preproteins into the chloroplast inner envelope membrane. Plant Mol Biol 68, 505–519.

    Article  CAS  PubMed  Google Scholar 

  88. Miras, S., Salvi, D., Ferro, M., Grunwald, D., Garin, J., Joyard, J., and Rolland, N. (2002) Non-canonical transit peptide for import into the chloroplast. J Biol Chem 277, 47770–47778.

    Article  CAS  PubMed  Google Scholar 

  89. Nada, A. and Soll, J. (2004) Inner envelope protein 32 is imported into chloroplasts by a novel pathway. J Cell Sci 117, 3975–3982.

    Article  CAS  PubMed  Google Scholar 

  90. Keegstra, K. and Cline, K. (1999) Protein import and routing systems of chloroplasts. Plant Cell 11, 557–570.

    Article  CAS  PubMed  Google Scholar 

  91. Nielsen, E., Akita, M., Davila-Aponte, J., and Keegstra, K. (1997) Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J 16, 935–946.

    Article  CAS  PubMed  Google Scholar 

  92. Tsugeki, R. and Nishimura, M. (1993) Interaction of homologues of Hsp70 and Cpn60 with ferredoxin-NADP+ reductase upon its import into chloroplasts. FEBS Lett 320, 198–202.

    Article  CAS  PubMed  Google Scholar 

  93. Richter, S. and Lamppa, G. K. (1998) A chloroplast processing enzyme functions as the general stromal processing peptidase. PNAS 95, 7463–7468.

    Article  CAS  PubMed  Google Scholar 

  94. Di Cola, A., Klostermann, E., Robinson, C. (2005) The complexity of pathways for proteins import into thylakoids: it’s not easy being green. Biochem Soc Trans 33, 1024–1027

    Article  PubMed  Google Scholar 

  95. Gutensohn, M., Fan, E., Frielingsdorf, S., Hanner, P., Hou, B., Hust, B., and Klosgen, R. B. (2006) Toc, Tic, Tat et al.: structure and function of protein transport machineries in chloroplasts. J Plant Physiol 163, 333–347.

    Article  CAS  PubMed  Google Scholar 

  96. Robinson, C., Thompson, S. J., and Woolhead, C. (2001) Multiple pathways used for the targeting of thylakoid proteins in chloroplasts. Traffic 2, 245–251.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Strittmatter, P., Soll, J., Bölter, B. (2010). The Chloroplast Protein Import Machinery: A Review. In: Economou, A. (eds) Protein Secretion. Methods in Molecular Biology, vol 619. Humana Press. https://doi.org/10.1007/978-1-60327-412-8_18

Download citation

  • DOI: https://doi.org/10.1007/978-1-60327-412-8_18

  • Published:

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-60327-167-7

  • Online ISBN: 978-1-60327-412-8

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics