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Localization and segregation of lineage-specific cleavage potential in embryos of Caenorhabditis elegans

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Summary

Early embryogenesis of the nematode Caenorhabditis elegans is characterized by the continuous visibility of a germline and the stepwise separation of all somatic cells from it. Germline and somatic cells exhibit different cleavage patterns. Typical for the germline is a series of stemcell-like, unequal cleavages generating blastomeres, which differ in size, cell cycle periods, and fate. Typical for members of somatic cell lineages during early development are their equal and synchronous cleavages generating cells of similar appearance. Using a laser microbeam various experiments have been carried out to investigate the conditions that lead to the two different types of cleavage. Development of partial embryos demonstrates that the potential for germline-like cleavage is localized in the posterior region of the fertilized egg prior to both the formation of pronuclei and the posterior aggregation of germline-specific granules. Experimental alteration of the cleavage plane can result in a switch from unequal to equal cleavage, with an apparent correlation between the orientation of the mitotic spindle and the type of cleavage. Nuclear transfer experiments indicate that nuclei and centrioles are not involved in the decision as to which type of cleavage will be executed. Cytoplasmic transfer from soma-like to germline-like cleaving cells and vice versa does not alter the cleavage type in the recipient cell. But if separation of germline from soma is delayed after the removal of a centrosome, germline-like cleavage may be completely suppressed, all cells thereafter dividing soma-like.

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References

  • Albertson DG (1984) Formation of first cleavage spindle in nematode embryos. Dev Biol 101:61–72

    Google Scholar 

  • Alexandre H, Petrocellis B de, Brachet J (1982) Studies on differentiation without cleavage in Chaetopterus. Requirement for a definite number of DNA replication cycles shown by aphidicolin pulses. Differentiation 22:132–135

    Google Scholar 

  • Boveri T (1892) Über die Entstehung des Gegensatzes zwischen den Geschlechtszellen und den somatischen Zellen bei Ascaris megalocephala. Sitzber Ges Morphol Physiol 8:114–125

    Google Scholar 

  • Boveri T (1899) Die Entwicklung von Ascaris megalocephala mit besonderer Rücksicht auf die Kernverhältnisse. Festschrift für C v Kupffer, Fischer, Jena, pp 383–430

    Google Scholar 

  • Boveri T (1910) Die Potenzen der Ascaris Blastomeren bei abgeänderter Furchung. Festschrift für R Hertwig, Fischer, Jena, pp 133–214

    Google Scholar 

  • Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94

    Google Scholar 

  • Cole TS, Schierenberg E (1986) Laser microbeam-induced fixation for electronmicroscopy: Visualization of transient developmental features in nematode embryos. Experientia 42:1046–1048

    Google Scholar 

  • Dan K, Ikeda M (1971) On the system controlling the time of micromere formation in the sea urchin embryo. Dev Growth Differ 13:285–301

    Google Scholar 

  • Deppe U, Schierenberg E, Cole T, Krieg C, Schmitt D, Yoder B, Ehrenstein G von (1978) Cell lineages of the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 75:376–380

    Google Scholar 

  • Edgar EG, McGhee JD (1988) DNA synthesis and the control of embryonic gene expression in C. elegans. Cell 53:589–599

    Google Scholar 

  • Hartwell L, Culotti J, Pringle J, Reid B (1974) Genetic control of the cell division cycle in yeast: a model. Science 183:46–51

    Google Scholar 

  • Hill DP, Strome S (1988) The role of microfilaments in the establishment and maintainance of asymmetry in Caenorhabditis elegans zygotes. Dev Biol 125:75–84

    Google Scholar 

  • Illmensee K, Mahowald AP (1974) Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc Natl Acad Sci USA 71:1016–1020

    Google Scholar 

  • Kemphues KJ, Priess JR, Morton DG, Cheng N (1988) Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52:311–320

    Google Scholar 

  • King RL, Beams HW (1938) An experimental study of chromatin diminution in Ascaris. J Exp Zool 77:425–443

    Google Scholar 

  • Laufer JS, Ehrenstein G von (1981) Nematode development after removal of egg cytoplasm: Absence of localized unbound determinants. Science 211:402–405

    Google Scholar 

  • Laufer JS, Bazzicalupo P, Wood WB (1980) Segregation of developmental potential in early embryos of Caenorhabditis elegans. Cell 19:569–577

    Google Scholar 

  • Nigon V, Guerrier P, Monin H (1960) L'architecture polaire de l'oeuf et les movements des constituants cellulaire au cours des premières étappes du développement chez quelques nématodes. Bull Biol Fr Belg 94:131–202

    Google Scholar 

  • Priess JR, Thomson JN (1987) Cellular interactions in early C. elegans embryos. Cell 48:241–250

    Google Scholar 

  • Satoh N, Ikegami S (1981) A definite number of aphidicolin-sensitive cell-cyclic events are required for acetylcholinesterase development in the presumptive muscle cells of the ascidian embryos. J Embryol Exp Morphol 61:1–13

    Google Scholar 

  • Schierenberg E (1984a) Altered cell division rates after laser-induced cell fusion in nematode embryos. Dev Biol 101:240–245

    Google Scholar 

  • Schierenberg E (1984b) Embryonic development of the nematode Caenorhabditis elegans. Film D1542 by IWF, Göttingen, FRG. Available in USA from “C. elegans Genetics Center”, Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211

    Google Scholar 

  • Schierenberg E (1985) Cell determination during early development of the nematode Caenorhabditis elegans. Cold Spring Harbor Symp Quant Biol 50:59–68

    Google Scholar 

  • Schierenberg E (1986) Developmental strategies during early embryogenesis of Caenorhabditis elegans. J Embryol Exp Morphol 97 (suppl): 31–44

    Google Scholar 

  • Schierenberg E (1987) Reversal of cellular polarity and early cell-cell interaction in the embryo of Caenorhabditis elegans. Dev Biol 122:452–463

    Google Scholar 

  • Schierenberg E, Wood WB (1985) Control of cell cycle timing in early embryos of Caenorhabditis elegans. Dev Biol 107:337–354

    Google Scholar 

  • Strome S (1986a) Fluorescence visualization of the distribution of microfilaments in gonads and early embryos of the nematode Caenorhabditis elegans. J Cell Biol 103:2241–2252

    Google Scholar 

  • Strome S (1986b) Establishment of asymmetry in early Caenorhabditis elegans embryos: Visualization with antibodies to germ cell components. In: Gall JC (ed) Gametogenesis and the early embryo. Liss, New York, pp 77–95

    Google Scholar 

  • Strome S (1988) Generation of cell diversity during early embryogenesis in the nematode Caenorhabditis elegans. Int Rev Cytol (in press)

  • Strome S, Wood WB (1983) Generation of asymmetry and segregation of germline granules in early C. elegans embryos. Cell 35:15–25

    Google Scholar 

  • Sulston JE, Brenner S (1974) The DNA of Caenorhabditis elegans. Genetics 77:95–104

    Google Scholar 

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

    Google Scholar 

  • Tobler H (1986) The differentiation of germ and somatic cell lines in nematodes. In: Hennig W (ed) Germline-soma differentiation. Springer, Berlin Heidelberg New York Tokyo, pp 1–69

    Google Scholar 

  • Yamaguchi Y, Murakami K, Furusawa M, Miwa J (1983) Germ line-specific antigens identified by monoclonal antibodies in the nematode Caenorhabditis elegans. Dev Growth Differ 25:121–131

    Google Scholar 

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Dedicated to Professor A. Egelhaaf on the occasion of his retirement

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Schierenberg, E. Localization and segregation of lineage-specific cleavage potential in embryos of Caenorhabditis elegans . Roux's Arch Dev Biol 197, 282–293 (1988). https://doi.org/10.1007/BF00380022

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  • DOI: https://doi.org/10.1007/BF00380022

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