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:

Binary specification of the embryonic lineage in Caenorhabditis elegans

Abstract

In Caenorhabditis elegans, the early embryo contains five somatic founder cells (known as AB, MS, E, C and D) which give rise to very different lineages. Two simply produce twenty intestinal (E) or muscle (D) cells each, whereas the remainder produce a total of 518 cells which collectively contribute in a complex pattern to a variety of tissues1. A central problem in embryonic development is to understand how the developmental potential of blastomeres is restricted to permit the terminal expression of such complex differentiation patterns. Here we identify a gene, lit-1, that appears to play a central role in controlling the asymmetry of cell division during embryogenesis in C. elegans. Mutants in lit-1 suggest that its product controls up to six consecutive binary switches which cause one of the two equivalent cells produced at each cleavage to assume a posterior fate. Most blastomere identities in C. elegans may therefore stem from a process of stepwise binary diversification.

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

Access options

Buy this article

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

Figure 1: Tissue differentiation in wild-type (a, c, e, g) at the 1.5-fold stage of embryogenesis1 and in two lit-1 (t1512) embryos (one embryo, b, d, f; the second, h).
Figure 2: Lineage analysis of lit-1 embryos with a four-dimensional microscope2.
Figure 3: The temperature-sensitive period of lit-1 (t1512).
Figure 4: Requirement of lit-1 at multiple stages during development.

Similar content being viewed by others

References

  1. Sulston, J. E., Schierenberg, E., White, J. G. & Thomson, J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64–119 (1983).

    Article  CAS  Google Scholar 

  2. Schnabel, R., Hutter, H., Moerman, D. G. & Schnabel, H. Assessing normal embryogenesis in C. elegans using a 4D-microscope: variability of development and regional specification. Dev. Biol. 184, 234–265 (1997).

    Article  CAS  Google Scholar 

  3. Riddle, D. L., Blumenthal, T., Meyer, B. J. & Priess, J. R. Monograph 33(Cold Spring Harbor Laboratory, New York, (1997)).

    Google Scholar 

  4. Schierenberg, E. Reversal of cellular polarity and early cell–cell interactions in the embryo of Caenorhabditis elegans. Dev. Biol. 122, 452–463 (1987).

    Article  CAS  Google Scholar 

  5. Goldstein, B. Cell contacts orient some cell division axes in the Caenorhabditis elegans embryo. J. Cell. Biol. 129, 1071–1080 (1995).

    Article  CAS  Google Scholar 

  6. Draper, B. W., Mello, C. C., Bowerman, B., Hardin, J. & Priess, J. R. MEX-3 is a KH domain protein that regulates blastomere identity in the early C. elegans embryo. Cell 87, 205–216 (1996).

    Article  CAS  Google Scholar 

  7. Hunter, C. P. & Kenyon, C. Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87, 217–226 (1996).

    Article  CAS  Google Scholar 

  8. Drubin, D. G. & Nelson, W. J. Origins of cell polarity. Cell 84, 335–344 (1996).

    Article  CAS  Google Scholar 

  9. Lin, R., Thompson, S. & Priess, J. R. Pop-1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos. Cell 83, 599–609 (1995).

    Article  CAS  Google Scholar 

  10. Guo, S. & Kemphues, K. J. Molecular genetics of asymmetric cleavage in the early Caenorhabditis elegans embryo. Curr. Opin. Genet. Dev. 6, 408–415 (1996).

    Article  CAS  Google Scholar 

  11. Weintraub, H. et al. The myoD gene family: nodal point during the specification of the muscle cell lineage. Science 255, 761–766 (1991).

    Article  ADS  Google Scholar 

  12. Schnabel, R. Pattern formation: regional specification in the C. elegans embryo. BioEssays 18, 591–594 (1996).

    Article  CAS  Google Scholar 

  13. Rivera-Pomar, R. & Jäckle, H. From gradients to stripes in Drosophila embryogenesis: filling in the gaps. Trends Genet. 12, 478–483 (1997).

    Article  Google Scholar 

  14. St Johnston, D. & Nüsslein Volhard, D. The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–220 (1992).

    Article  CAS  Google Scholar 

  15. Lin, H. & Schagat, T. Neuroblasts: a model for the asymmetric division of stem cells. Trends Genet. 13, 33–39 (1997).

    Article  CAS  Google Scholar 

  16. Greenwald, I. S., Sternberg, P. W. & Horvitz, H. R. The lin-12 locus specifies cell fates in C. elegans. Cell 34, 435–444 (1983).

    Article  CAS  Google Scholar 

  17. Hodgkin, J. & Doniach, T. Natural variation and copulatory plug formation in C. elegans. Genetics 146, 149–164 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Wood, W. B. The nematode Caenorhabditis elegans(Cold Spring Harbor Laboratory, New York, (1988)).

    Google Scholar 

  19. Hutter, H. & Schnabel, R. glp-1 and inductions establishing embryonic axes in Caenorhabditis elegans. Development 120, 2051–2064 (1994).

    CAS  PubMed  Google Scholar 

  20. Priess, J. R. & Thomson, J. N. Cellular interactions in early C. elegans embryos. Cell 48, 241–250 (1987).

    Article  CAS  Google Scholar 

  21. Schnabel, R. & Schnabel, H. Early determination in the C. elegans embryo: a gene, cib-1, required to specify a set of stem-cell-like blastomers. Development 108, 107–119 (1990).

    CAS  PubMed  Google Scholar 

  22. Priess, J. R., Schnabel, H. & Schnabel, R. The glp-1 locus and cellular interactions in early C. elegans embryos. Cell 51, 601–611 (1987).

    Article  CAS  Google Scholar 

  23. Kemphues, K. J., Priess, J. R., Morton, D. G. & Cheng, N. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52, 311–320 (1988).

    Article  CAS  Google Scholar 

  24. Hutter, H. & Schnabel, R. Specification of anterior–posterior differences within the AB lineage in the C. elegans embryo: a polarising induction. Development 121, 1559–1568 (1995).

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kaletta, T., Schnabel, H. & Schnabel, R. Binary specification of the embryonic lineage in Caenorhabditis elegans. Nature 390, 294–298 (1997). https://doi.org/10.1038/36869

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/36869

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