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:

Polarization of the anterior–posterior axis of C. elegans is a microtubule-directed process

Abstract

In Caenorhabditis elegans, polarity along the anterior–posterior (A/P) axis is established shortly after fertilization and is determined by the sperm, whose position specifies the posterior end of the embryo1. Although many factors required for the establishment of A/P polarity have been described2,3, the nature of the spatial cue provided by the sperm remains unknown. Here we show that a microtubule-organizing centre is necessary and sufficient to establish several aspects of A/P polarity. In wild-type embryos, appearance of the first molecular asymmetries along the A/P axis correlates with and requires nucleation of microtubules by the sperm-derived centrosomes (sperm asters). In mutant embryos arrested in meiosis, sperm asters fail to form, and posterior is defined by the position of the persistent meiotic spindle rather than by the position of the sperm. Together, our data indicate that the primary spatial cue for A/P polarity in C. elegans derives from microtubules emanating from the sperm asters. Our findings support a parallel4,5,6,7 between C. elegans zygotes and other cells, such as Drosophila oocytes, which rely on microtubules to regulate polarity.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Establishment of A/P polarity in C. elegans.
Figure 2: A/P polarity in mat mutant embryos. a, mat-1( ax227) embryo immunostained for PIE-1 (red) and DAPI (blue).
Figure 3: Establishment of A/P polarity in wild type correlates with and requires sperm aster formation.

Similar content being viewed by others

References

  1. Goldstein, B. & Hird, S. N. Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122, 1467–1474 (1996).

    CAS  PubMed  Google Scholar 

  2. Rose, L. S. & Kemphues, K. J. Early patterning of the C. elegans embryo. Annu. Rev. Genet. 32, 521–545 (1998).

    Article  CAS  Google Scholar 

  3. Bowerman, B. Maternal control of pattern formation in early Caenorhabditis elegans embryos. Curr. Top. Dev. Biol. 39, 73– 117 (1998).

    Article  CAS  Google Scholar 

  4. Shulman, J. M., Benton, R. & St Johnston, D. The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 101, 377– 388 (2000).

    Article  CAS  Google Scholar 

  5. Tomancak, P. et al. A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic-axis formation. Nature Cell Biol. 2, 458–460 (2000).

    Article  CAS  Google Scholar 

  6. Kemphues, K. PARsing embryonic polarity. Cell 101, 345 –348 (2000).

    Article  CAS  Google Scholar 

  7. Morris, J., Lehmann, R. & Navarro, C. PARallels in axis formation. Science 288, 1759–1760 (2000).

    Article  CAS  Google Scholar 

  8. Hird, S. N. & White, J. G. Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J. Cell Biol. 121, 1343–1355 ( 1993).

    Article  CAS  Google Scholar 

  9. Hird, S. N., Paulsen, J. E. & Strome, S. Segregation of germ granules in living Caenorhabditis elegans embryos: cell-type-specific mechanisms for cytoplasmic localisation. Development 122, 1303– 1312 (1996).

    CAS  PubMed  Google Scholar 

  10. Sadler, P. L. & Shakes, D. C. Anucleate Caenorhabditis elegans sperm can crawl, fertilize oocytes and direct anterior-posterior polarization of the 1-cell embryo. Development 127, 355 –366 (2000).

    CAS  PubMed  Google Scholar 

  11. Furuta, T. et al. EMB-30: An APC4 homologue required for metaphase-to-anaphase transitions during meiosis and mitosis in Caenorhabditis elegans. Mol. Biol. Cell 11, 1401–1419 (2000).

    Article  CAS  Google Scholar 

  12. Etemad-Moghadam, B., Guo, S. & Kemphues, K. J. Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 83, 743–752 (1995).

    Article  CAS  Google Scholar 

  13. Tenenhaus, C., Schubert, C. & Seydoux, G. Genetic requirements for PIE-1 localization and inhibition of gene expression in the embryonic germ lineage of Caenorhabditis elegans . Dev. Biol. 200, 212– 224 (1998).

    Article  CAS  Google Scholar 

  14. Boxem, M., Srinivasan, D. G. & van den Heuvel, S. The Caenorhabditis elegans gene ncc-1 encodes a cdc2-related kinase required for M phase in meiotic and mitotic cell divisions, but not for S phase. Development 126 , 2227–2239 (1999).

    CAS  PubMed  Google Scholar 

  15. Albertson, D. G. Formation of the first cleavage spindle in nematode embryos. Dev. Biol. 101, 61–72 ( 1984).

    Article  CAS  Google Scholar 

  16. Boyd, L., Guo, S., Levitan, D., Stinchcomb, D. T. & Kemphues, K. J. PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122, 3075– 3084 (1996).

    CAS  PubMed  Google Scholar 

  17. Strome, S. & Wood, W. B. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35, 15–25 ( 1983).

    Article  CAS  Google Scholar 

  18. Schumacher, J. M., Ashcroft, N., Donovan, P. J. & Golden, A. A highly conserved centrosomal kinase, AIR-1, is required for accurate cell cycle progression and segregation of developmental factors in Caenorhabditis elegans embryos. Development 125, 4391 –4402 (1998).

    CAS  PubMed  Google Scholar 

  19. O'Connell, K., Maxwell, K. & White, J. The spd-2 gene is required for polarization of the anteroposterior axis and formation of the sperm asters in the Caenorhabditis elegans zygote. Dev. Biol. 221, 55– 70 (2000).

    Article  Google Scholar 

  20. Hill, D. P. & Strome, S. Brief cytochalasin-induced disruption of microfilaments druing a critical interval in one-cell C. elegans embryos alters the partitioning of developmental instructions to the two-cell embryo. Development 108, 159– 172 (1990).

    CAS  PubMed  Google Scholar 

  21. Shelton, C. A., Carter, J. C., Ellis, G. C. & Bowerman, B. The nonmuscle myosin regulatory light chain gene mlc-4 is required for cytokinesis, anterior-posterior polarity, and body morphology during Caenorhabditis elegans embryogenesis. J. Cell Biol. 146, 439–451 (1999).

    Article  CAS  Google Scholar 

  22. van Eeden, F. & St Johnston, D. The polarisation of the anterior-posterior and dorsal-ventral axes during Drosophila oogenesis. Curr. Opin. Genet. Dev. 9, 396–404 (1999).

    Article  CAS  Google Scholar 

  23. Bohm, H., Brinkmann, V., Drab, M., Henske, A. & Kurzchalia, T. V. Mammalian homologues of C. elegans PAR-1 are asymmetrically localized in epithelial cells and may influence their polarity. Curr. Biol. 7, 603–606 (1997).

    Article  CAS  Google Scholar 

  24. Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E. M. & Mandelkow, E. MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89, 297–308 ( 1997).

    Article  CAS  Google Scholar 

  25. Reese, K. J., Dunn, M. A., Waddle, J. A. & Seydoux, G. Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains. Mol. Cell. 6, 445–455 ( 2000).

    Article  CAS  Google Scholar 

  26. Guo, S. & Kemphues, K. J. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611–620 (1995).

    Article  CAS  Google Scholar 

  27. Strome, S. & Wood, W. B. Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 79, 1558–1562 (1982).

    Article  ADS  CAS  Google Scholar 

  28. Timmons, L. & Fire, A. Specific interference by ingested dsRNA. Nature 395, 854 ( 1998).

    Article  ADS  CAS  Google Scholar 

  29. Edgar, L. G. Blastomere culture and analysis. Methods Cell Biol. 48, 303–321 (1995).

    Article  CAS  Google Scholar 

  30. McCarter, J., Bartlett, B., Dang, T. & Schedl, T. On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 205, 111–128 (1999).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to A. Golden, P. Sadler, J. Schumacher and D. Shakes for their characterization of the mat mutants. We also thank K. O'Connell and J. White for sharing results before publication; K. Kemphues and L. Boyd for antibodies; L. Timmons and A. Fire for RNAi feeding materials; and A. Golden, P. Sadler, D. Shakes, K. Kemphues, K. O'Connell, Y. Zheng and members of the Seydoux lab for comments on the manuscript. Some strains used in this study were provided by the Caenorhabditis Genetics Center (University of Minnesota). M.R.W. was an NSF predoctoral fellow. This work was supported by grants from the Searle and Packard Foundations to G.S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Geraldine Seydoux.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wallenfang, M., Seydoux, G. Polarization of the anterior–posterior axis of C. elegans is a microtubule-directed process. Nature 408, 89–92 (2000). https://doi.org/10.1038/35040562

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35040562

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

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