Binary specification of the embryonic lineage in Caenorhabditis elegans (original) (raw)

Nature volume 390, pages 294–298 (1997)Cite this article

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.

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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

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  1. Max-Planck-Institut für Biochemie, 82152, Martinsried, Germany
    Titus Kaletta, Heinke Schnabel & Ralf Schnabel

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  1. Titus Kaletta
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  2. Heinke Schnabel
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  3. Ralf Schnabel
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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

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