Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Golgi biogenesis in Toxoplasma gondii

Nature volume 418, pages 548–552 (2002)Cite this article

Abstract

Two models have been put forward to explain the growth of new Golgi during the cell cycle. The first suggests that a new Golgi grows out of the endoplasmic reticulum by de novo synthesis1. The second suggests that a pre-existing Golgi is needed for the growth of a new one, that is, the Golgi is an autonomously replicating organelle2. To resolve this issue, we have exploited the simplicity of the apicomplexan parasite Toxoplasma gondii3, which has only a single Golgi stack4. Here we show, by using video fluorescence microscopy and three-dimensional reconstructions of serial thin sections, that the Golgi grows by a process of lateral extension followed by medial fission. Further fission leads to the inheritance by each daughter of a pair of Golgi structures, which then coalesce to re-form a single Golgi. Our results indicate that new Golgi grow by autonomous duplication and raise the possibility that the Golgi is a paired structure that is analogous to centrioles5.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Stages of Golgi growth and division.
Figure 2: Stable expression of mammalian Golgi proteins.
Figure 3: Immunoelectron microscopy of transgenic parasites.
Figure 4: Biogenesis of the Golgi apparatus in living parasites.

Similar content being viewed by others

References

  1. Lippincott-Schwartz, J. & Zaal, K. J. Cell cycle maintenance and biogenesis of the Golgi complex. Histochem. Cell. Biol. 114, 93–103 (2000)

    CAS  PubMed  Google Scholar 

  2. Bracker, C. E., Morre, D. J. & Grove, S. N. Structure, differentiation, and multiplication of Golgi-apparatus in fungal hyphae. Protoplasma 194, 250–274 (1996)

    Article  Google Scholar 

  3. Joiner, K. A. & Roos, D. S. Secretory traffic in the eukaryotic parasite Toxoplasma gondii: less is more. J. Cell Biol. 157, 557–563 (2002)

    Article  CAS  Google Scholar 

  4. Roos, D. S. et al. Transport and trafficking: Toxoplasma as a model for Plasmodium. Novartis Found. Symp. 226, 176–195 (1999)

    CAS  PubMed  Google Scholar 

  5. Marshall, W. Centrioles take center stage. Curr. Biol. 11, R487–R496 (2001)

    Article  CAS  Google Scholar 

  6. Kelly, T. J. & Brown, G. W. Regulation of chromosome replication. Annu. Rev. Biochem. 69, 829–880 (2000)

    Article  CAS  Google Scholar 

  7. Warren, G. Membrane partitioning during cell division. Annu. Rev. Biochem. 62, 323–348 (1993)

    Article  CAS  Google Scholar 

  8. Whaley, W. G. The Golgi Apparatus (Springer, New York, 1975)

    Book  Google Scholar 

  9. Preuss, D., Mulholland, J., Franzusoff, A., Segev, N. & Botstein, D. Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy. Mol. Biol. Cell 3, 789–803 (1992)

    Article  CAS  Google Scholar 

  10. Zaal, K. J. et al. Golgi membranes are absorbed into and reemerge from the ER during mitosis. Cell 99, 589–601 (1999)

    Article  CAS  Google Scholar 

  11. Presley, J. F. et al. Golgi membrane dynamics. Mol. Biol. Cell 9, 1617–1626 (1998)

    Article  CAS  Google Scholar 

  12. Pelletier, L., Jokitalo, E. & Warren, G. The effect of Golgi depletion on exocytic transport. Nature Cell Biol. 2, 840–846 (2000)

    Article  CAS  Google Scholar 

  13. Shima, D. T., Haldar, K., Pepperkok, R., Watson, R. & Warren, G. Partitioning of the Golgi apparatus during mitosis in living HeLa cells. J. Cell Biol. 137, 1211–1228 (1997)

    Article  CAS  Google Scholar 

  14. Cole, N. B., Sciaky, N., Marotta, A., Song, J. & Lippincott-Schwartz, J. Golgi dispersal during microtubule disruption—regeneration of Golgi stacks at peripheral endoplasmic-reticulum exit sites. Mol. Biol. Cell 7, 631–650 (1996)

    Article  CAS  Google Scholar 

  15. Wooding, S. & Pelham, H. R. The dynamics of Golgi protein traffic visualized in living yeast cells. Mol. Biol. Cell 9, 2667–2680 (1998)

    Article  CAS  Google Scholar 

  16. Rossanese, O. W. et al. Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J. Cell Biol. 145, 69–81 (1999)

    Article  CAS  Google Scholar 

  17. Dubremetz, J. F., Garcia-Reguet, N., Conseil, V. & Fourmaux, M. N. Apical organelles and host-cell invasion by Apicomplexa. Int. J. Parasitol. 28, 1007–1013 (1998)

    Article  CAS  Google Scholar 

  18. Hager, K. M., Striepen, B., Tilney, L. G. & Roos, D. S. The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J. Cell Sci. 112, 2631–2638 (1999)

    CAS  PubMed  Google Scholar 

  19. Sheffield, H. G. & Melton, M. L. The fine structure and reproduction of Toxoplasma gondii. J. Parasitol. 54, 209–226 (1968)

    Article  CAS  Google Scholar 

  20. Radke, J. R. et al. Defining the cell cycle for the tachyzoite stage of Toxoplasma gondii. Mol. Biochem. Parasitol. 115, 165–175 (2001)

    Article  CAS  Google Scholar 

  21. Hu, K. et al. Daughter cell assembly in the protozoan parasite Toxoplasma gondii. Mol. Biol. Cell 13, 593–606 (2002)

    Article  CAS  Google Scholar 

  22. Seemann, J., Jokitalo, E., Pypaert, M. & Warren, G. Matrix proteins can generate the higher order architecture of the Golgi apparatus. Nature 407, 1022–1026 (2000)

    Article  ADS  CAS  Google Scholar 

  23. Ward, T. H., Polishchuk, R. S., Caplan, S., Hirschberg, K. & Lippincott-Schwartz, J. Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155, 557–570 (2001)

    Article  CAS  Google Scholar 

  24. Wiggins, C. A. R. & Munro, S. Activity of the yeast mnn1 α-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc. Natl Acad. Sci. USA 95, 7945–7950 (1998)

    Article  ADS  CAS  Google Scholar 

  25. Odenthal-Schnittler, M., Tomavo, S., Becker, D., Dubremetz, J. F. & Schwarz, R. T. Evidence for N-linked glycosylation in Toxoplasma gondii. Biochem. J. 291, 713–721 (1993)

    Article  CAS  Google Scholar 

  26. Lujan, H. D. et al. Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J. Biol. Chem. 270, 4612–4618 (1995)

    Article  CAS  Google Scholar 

  27. Field, H., Sherwin, T., Smith, A. C., Gull, K. & Field, M. C. Cell-cycle and developmental regulation of TbRAB31 localisation, a GTP- locked Rab protein from Trypanosoma brucei. Mol. Biochem. Parasitol. 106, 21–35 (2000); erratum 107, 329–330 (2000)

    Article  CAS  Google Scholar 

  28. Piel, M., Nordberg, J., Euteneuer, U. & Bornens, M. Centrosome-dependent exit of cytokinesis in animal cells. Science 291, 1550–1553 (2001)

    Article  ADS  CAS  Google Scholar 

  29. Roos, D. S., Donald, R. G. K., Morrissette, N. S. & Moulton, A. L. C. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol. 45, 27–63 (1994)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank F. Barr and T. Nilsson for the GRASP55 and NAGTI plasmids; S. Trombetta for recombinant GFP; the Joiner and Roos labs—mainly F. Quittnat, T. Stedman and O. Harb—for advice and discussion; N. Andrews for the use of her cell-culture room; C. Roy and J. Kagan for help with confocal microscopy; K. Zichichi, C. Horensavitz and C. Deloyer-Pypaert for help with electron microscopy; Olympus for providing some of the microscopes; J. Shorter and E. Procyk for critically reading the manuscript; and the Warren and Mellman labs for discussions. This work was supported by National Institutes of Health grants (to G.W., I.M., K.A.J. and D.S.R.) and the Ludwig Institute for Cancer Research.

Author information

Authors and Affiliations

  1. Department of Cell Biology, Ludwig Institute for Cancer Research, Yale University School of Medicine, Connecticut, 06520, New Haven, USA

    Laurence Pelletier, Marc Pypaert, David Sheff, Nitin Roper, Cynthia Y. He, Derek Toomre & Graham Warren

  2. Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School and The Dana-Farber Cancer Institute, Boston, Massachusetts, 02115, USA

    Charlene A. Stern

  3. Section of Infectious Diseases, Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut, 06520, USA

    Huân M. Ngô, Isabelle Coppens & Keith A. Joiner

  4. Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, 19104, USA

    Ke Hu & David S. Roos

Authors
  1. Laurence Pelletier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charlene A. Stern
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marc Pypaert
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David Sheff
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Huân M. Ngô
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nitin Roper
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cynthia Y. He
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ke Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Derek Toomre
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Isabelle Coppens
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. David S. Roos
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Keith A. Joiner
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Graham Warren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Graham Warren.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pelletier, L., Stern, C., Pypaert, M. et al. Golgi biogenesis in Toxoplasma gondii. Nature 418, 548–552 (2002). https://doi.org/10.1038/nature00946

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature00946

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing