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The major protein import receptor of plastids is essential for chloroplast biogenesis

Nature volume 403, pages 203–207 (2000)Cite this article

Abstract

Light triggers the developmental programme in plants that leads to the production of photosynthetically active chloroplasts from non-photosynthetic proplastids1. During this chloroplast biogenesis, the photosynthetic apparatus is rapidly assembled, mostly from nuclear-encoded imported proteins2,3,4, which are synthesized in the cytosol as precursors with cleavable amino-terminal targeting sequences called transit sequences. Protein translocon complexes at the outer (Toc complex)5,6,7 and inner (Tic complex)6,8,9 envelope membranes recognize these transit sequences, leading to the precursors being imported. The Toc complex in the pea consists of three major components, Toc75, Toc34 and Toc159 (formerly termed Toc86)6,7,10,11. Toc159, which is an integral membrane GTPase12, functions as a transit-sequence receptor5,6,7,13. Here we show that Arabidopsis thaliana Toc159 (atToc159) is essential for the biogenesis of chloroplasts. In an Arabidopsis mutant (ppi2) that lacks atToc159, photosynthetic proteins that are normally abundant are transcriptionally repressed, and are found in much smaller amounts in the plastids, although ppi2 does not affect either the expression or the import of less abundant non-photosynthetic plastid proteins. These findings indicate that atToc159 is required for the quantitative import of photosynthetic proteins. Two proteins that are related to atToc159 (atToc120 and atToc132) probably help to maintain basal protein import in ppi2, and so constitute components of alternative, atToc159-independent import pathways.

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Figure 1: A family of three Toc159-related genes in Arabidopsis.
Figure 2: Toc159, atToc132 and atToc120 are components of the Toc complex of the plastid protein import machinery.
Figure 3: Characteristics of the ppi2 mutant.
Figure 4: ppi2 plants contain reduced amounts of photosynthetic proteins.
Figure 5: Characterization of the chloroplast biogenetic defect in ppi2 plants.

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References

  1. Kendrick, R. E. & Kronenberg, G. H. M. Photomorphogenesis in Plants (Junk, Dordrecht, 1994).

    Book  Google Scholar 

  2. Chen, X. & Schnell, D. J. Protein import into chloroplasts. Trends Cell Biol. 9, 222– 227 (1999).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  4. Soll, J. & Tien, R. Protein translocation into and across the chloroplastic envelope membranes. Plant Mol. Biol. 38, 191–207 (1998).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  6. Schnell, D. J., Kessler, F. & Blobel, G. Isolation of components of the chloroplast protein import machinery. Science 266, 1007– 1012 (1994).

    Article  ADS  CAS  Google Scholar 

  7. Perry, S. E. & Keegstra, K. Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 6, 93–105 (1994).

    Article  CAS  Google Scholar 

  8. Kessler, F. & Blobel, G. Interaction of the protein important of the protein import and folding machineries in the chloroplast. Proc. Natl Acad. Sci. USA 93, 7684– 7689 (1996).

    Article  ADS  CAS  Google Scholar 

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

    Article  Google Scholar 

  10. Chen, K., Chen, X. & Schnell, D. J. Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts. Plant Phys. (in the press).

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

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  13. Ma, Y., Kouranov, A., LaSala, S. E. & Schnell, D. J. Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and translocation of precursor proteins at the outer envelope. J. Cell Biol. 134, 1–13 (1996).

    Article  Google Scholar 

  14. Jarvis, P. et al. An arabidopsis mutant defective in the plastid general protein import apparatus. Science 282, 100– 103 (1998).

    Article  ADS  CAS  Google Scholar 

  15. McKinney, E. C. et al. Sequence-based identification of T-DNA insertion mutations in Arabidopsis: actin mutants act2-1 and act4-1. Plant J. 8, 613–622 ( 1995).

    Article  CAS  Google Scholar 

  16. Bölter, B., May, T. & Soll, J. A protein import receptor in pea chloroplasts, Toc86, is only a proteolytic fragment of a larger polypeptide. FEBS Lett. 441, 59–62 (1998).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. Feldmann, K. T-DNA insertion mutagenesis in Arabidopsis—mutational spectrum. Plant J. 1, 71–82 (1991).

    Article  CAS  Google Scholar 

  20. Surpin, M. & Chory, J. The co-ordination of nuclear and organellar genome expression in eukaryotic cells. Essays Biochem. 32, 113–125 (1997).

    CAS  PubMed  Google Scholar 

  21. Ang, L.-H. et al. Molecular Interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol. Cell 1, 213–222 ( 1998).

    Article  CAS  Google Scholar 

  22. Li, H.-M., Culligan, K., Dixon, R. A. & Chory, J. CUE1: A mesophyll cell-specific positive regulator of light-controlled gene expression in Arabidopsis. Plant Cell 7, 1599– 1610 (1995).

    Article  CAS  Google Scholar 

  23. Eberhard, J. et al. Cytosolic and plastidic chorismate mutase isozymes from Arabidopsis thaliana: molecular characterization and enzymatic properties. Plant J. 10, 815–821 (1996).

    Article  CAS  Google Scholar 

  24. Lübeck, J., Heins, L. & Soll, J. A nuclear encoded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle. J. Cell Biol. 137, 1279–1286 ( 1997).

    Article  Google Scholar 

  25. Chen, D. & Schnell, D. J. Insertion of the 34 kDA chloroplast protein import component, IAP34, into the chloroplast outer membrane is dependent on its intrinsic GTP-binding capacity. J. Biol. Chem. 272, 6614–6620 ( 1997).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Michel, M., Hillmann, T. & Müller, M. Cryosectioning of plant material frozen at high pressure. J. Microsc. 163, 3–18 (1991).

    Article  Google Scholar 

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Acknowledgements

We thank G. Armstrong, Q. Su and K. Apel for antibodies, cDNA probes and discussion; N. Amrhein, P. Macheroux and A. Schaller for support and discussion; and G. Schatz for encouragement. D.S. was supported by grants from the National Science Foundation and a Charles and Johanna Busch Memorial Fund award. F.K. was supported by grants from the Swiss Federal Institute of Technology and the Swiss National Science Foundation.

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  1. Jörg Bauer, Kunhua Chen, Andreas Hiltbunner and Ernst Wehrli: These authors contributed equally to this work

Authors and Affiliations

  1. Institute of Plant Sciences, Swiss Federal Institute of Technology, Universitätstrasse 2, Zürich, CH-8092, Switzerland

    Jörg Bauer, Andreas Hiltbunner, Monika Eugster & Felix Kessler

  2. Department of Biological Sciences Rutgers, The State University of New Jersey, 101 Warren Street , Newark, 07102, New Jersey, USA

    Kunhua Chen & Danny Schnell

  3. Laboratory for Electronmicroscopy I, Institute of Biochemistry, Swiss Federal Institue of Technology, Schmelzbergstrasse 7, Zürich, CH-8092, Switzerland

    Ernst Wehrli

Authors
  1. Jörg Bauer
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Correspondence to Felix Kessler.

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Bauer, J., Chen, K., Hiltbunner, A. et al. The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403, 203–207 (2000). https://doi.org/10.1038/35003214

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