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. 1993 Oct 1;123(1):191–208. doi: 10.1083/jcb.123.1.191

The relationship between cell size and cell fate in Volvox carteri

PMCID: PMC2119814  PMID: 8408198

Abstract

In Volvox carteri development, visibly asymmetric cleavage divisions set apart large embryonic cells that will become asexual reproductive cells (gonidia) from smaller cells that will produce terminally differentiated somatic cells. Three mechanisms have been proposed to explain how asymmetric division leads to cell specification in Volvox: (a) by a direct effect of cell size (or a property derived from it) on cell specification, (b) by segregation of a cytoplasmic factor resembling germ plasm into large cells, and (c) by a combined effect of differences in cytoplasmic quality and cytoplasmic quantity. In this study a variety of V. carteri embryos with genetically and experimentally altered patterns of development were examined in an attempt to distinguish among these hypotheses. No evidence was found for regionally specialized cytoplasm that is essential for gonidial specification. In all cases studied, cells with a diameter > approximately 8 microns at the end of cleavage--no matter where or how these cells had been produced in the embryo--developed as gonidia. Instructive observations in this regard were obtained by three different experimental interventions. (a) When heat shock was used to interrupt cleavage prematurely, so that presumptive somatic cells were left much larger than they normally would be at the end of cleavage, most cells differentiated as gonidia. This result was obtained both with wild-type embryos that had already divided asymmetrically (and should have segregated any cytoplasmic determinants involved in cell specification) and with embryos of a mutant that normally produces only somatic cells. (b) When individual wild-type blastomeres were isolated at the 16-cell stage, both the anterior blastomeres that normally produce two gonidia each and the posterior blastomeres that normally produce no gonidia underwent modified cleavage patterns and each produced an average of one large cell that developed as a gonidium. (c) When large cells were created microsurgically in a region of the embryo that normally makes only somatic cells, these large cells became gonidia. These data argue strongly for a central role of cell size in germ/soma specification in Volvox carteri, but leave open the question of how differences in cell size are actually transduced into differences in gene expression.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Cossins A. R. Cell physiology. A sense of cell size. Nature. 1991 Aug 22;352(6337):667–668. doi: 10.1038/352667a0. [DOI] [PubMed] [Google Scholar]
  2. Edgar B. A., Kiehle C. P., Schubiger G. Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell. 1986 Jan 31;44(2):365–372. doi: 10.1016/0092-8674(86)90771-3. [DOI] [PubMed] [Google Scholar]
  3. Green K. J., Kirk D. L. A revision of the cell lineages recently reported for Volvox carteri embryos. J Cell Biol. 1982 Sep;94(3):741–742. doi: 10.1083/jcb.94.3.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Green K. J., Kirk D. L. Cleavage patterns, cell lineages, and development of a cytoplasmic bridge system in Volvox embryos. J Cell Biol. 1981 Dec;91(3 Pt 1):743–755. doi: 10.1083/jcb.91.3.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Harper J. F., Huson K. S., Kirk D. L. Use of repetitive sequences to identify DNA polymorphisms linked to regA, a developmentally important locus in Volvox. Genes Dev. 1987 Aug;1(6):573–584. doi: 10.1101/gad.1.6.573. [DOI] [PubMed] [Google Scholar]
  6. Hayles J., Nurse P. Cell cycle regulation in yeast. J Cell Sci Suppl. 1986;4:155–170. doi: 10.1242/jcs.1986.supplement_4.10. [DOI] [PubMed] [Google Scholar]
  7. Henery C. C., Bard J. B., Kaufman M. H. Tetraploidy in mice, embryonic cell number, and the grain of the developmental map. Dev Biol. 1992 Aug;152(2):233–241. doi: 10.1016/0012-1606(92)90131-y. [DOI] [PubMed] [Google Scholar]
  8. Horvitz H. R., Herskowitz I. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell. 1992 Jan 24;68(2):237–255. doi: 10.1016/0092-8674(92)90468-r. [DOI] [PubMed] [Google Scholar]
  9. Huskey R. J., Griffin B. E. Genetic control of somatic cell differentiation in Volvox analysis of somatic regenerator mutants. Dev Biol. 1979 Oct;72(2):226–235. doi: 10.1016/0012-1606(79)90113-1. [DOI] [PubMed] [Google Scholar]
  10. Illmensee K., Mahowald A. P. Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1016–1020. doi: 10.1073/pnas.71.4.1016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Johnston G. C., Pringle J. R., Hartwell L. H. Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp Cell Res. 1977 Mar 1;105(1):79–98. doi: 10.1016/0014-4827(77)90154-9. [DOI] [PubMed] [Google Scholar]
  12. Kirk D. L., Harper J. F. Genetic, biochemical, and molecular approaches to Volvox development and evolution. Int Rev Cytol. 1986;99:217–293. doi: 10.1016/s0074-7696(08)61428-x. [DOI] [PubMed] [Google Scholar]
  13. Kirk D. L., Kaufman M. R., Keeling R. M., Stamer K. A. Genetic and cytological control of the asymmetric divisions that pattern the Volvox embryo. Dev Suppl. 1991;1:67–82. [PubMed] [Google Scholar]
  14. Kirk D. L., Kirk M. M. Heat shock elicits production of sexual inducer in Volvox. Science. 1986 Jan 3;231(4733):51–54. doi: 10.1126/science.3941891. [DOI] [PubMed] [Google Scholar]
  15. Kirk D. L., Kirk M. M. Protein synthetic patterns during the asexual life cycle of Volvox carteri. Dev Biol. 1983 Apr;96(2):493–506. doi: 10.1016/0012-1606(83)90186-0. [DOI] [PubMed] [Google Scholar]
  16. Kirk D. L. The ontogeny and phylogeny of cellular differentiation in Volvox. Trends Genet. 1988 Feb;4(2):32–36. doi: 10.1016/0168-9525(88)90063-7. [DOI] [PubMed] [Google Scholar]
  17. Kirk M. M., Kirk D. L. Translational regulation of protein synthesis, in response to light, at a critical stage of Volvox development. Cell. 1985 Jun;41(2):419–428. doi: 10.1016/s0092-8674(85)80015-5. [DOI] [PubMed] [Google Scholar]
  18. Kochert G. Developmental mechanisms in Volvox reproduction. Symp Soc Dev Biol. 1975;(33):55–90. doi: 10.1016/b978-0-12-612979-3.50010-8. [DOI] [PubMed] [Google Scholar]
  19. Kochert G., Yates I. A UV-labile morphogenetic substance in Volvox carteri. Dev Biol. 1970 Sep;23(1):128–135. doi: 10.1016/s0012-1606(70)80010-0. [DOI] [PubMed] [Google Scholar]
  20. Kunkel B. Compartmentalized gene expression during sporulation in Bacillus subtilis. Trends Genet. 1991 May;7(5):167–172. doi: 10.1016/0168-9525(91)90381-y. [DOI] [PubMed] [Google Scholar]
  21. Larson A., Kirk M. M., Kirk D. L. Molecular phylogeny of the volvocine flagellates. Mol Biol Evol. 1992 Jan;9(1):85–105. doi: 10.1093/oxfordjournals.molbev.a040710. [DOI] [PubMed] [Google Scholar]
  22. Margolis P., Driks A., Losick R. Establishment of cell type by compartmentalized activation of a transcription factor. Science. 1991 Oct 25;254(5031):562–565. doi: 10.1126/science.1948031. [DOI] [PubMed] [Google Scholar]
  23. Nasmyth K., Shore D. Transcriptional regulation in the yeast life cycle. Science. 1987 Sep 4;237(4819):1162–1170. doi: 10.1126/science.3306917. [DOI] [PubMed] [Google Scholar]
  24. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell. 1982 Oct;30(3):687–696. doi: 10.1016/0092-8674(82)90273-2. [DOI] [PubMed] [Google Scholar]
  25. PRESCOTT D. M. Relation between cell growth and cell division. III. Changes in nuclear volume and growth rate and prevention of cell division in Amoeba proteus resulting from cytoplasmic amputations. Exp Cell Res. 1956 Aug;11(1):94–98. doi: 10.1016/0014-4827(56)90193-8. [DOI] [PubMed] [Google Scholar]
  26. Ransick A. Reproductive cell specification during Volvox obversus development. Dev Biol. 1991 Jan;143(1):185–198. doi: 10.1016/0012-1606(91)90065-b. [DOI] [PubMed] [Google Scholar]
  27. Schmitt R., Fabry S., Kirk D. L. In search of molecular origins of cellular differentiation in Volvox and its relatives. Int Rev Cytol. 1992;139:189–265. doi: 10.1016/s0074-7696(08)61413-8. [DOI] [PubMed] [Google Scholar]
  28. Smith L. D. The role of a "germinal plasm" in the formation of primordial germ cells in Rana pipiens. Dev Biol. 1966 Oct;14(2):330–347. doi: 10.1016/0012-1606(66)90019-4. [DOI] [PubMed] [Google Scholar]
  29. Starr R. C. Control of differentiation in Volvox. Symp Soc Dev Biol. 1970;29:59–100. doi: 10.1016/b978-0-12-395534-0.50009-1. [DOI] [PubMed] [Google Scholar]
  30. Stragier P. Dances with sigmas. EMBO J. 1991 Dec;10(12):3559–3566. doi: 10.1002/j.1460-2075.1991.tb04922.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Strome S. Generation of cell diversity during early embryogenesis in the nematode Caenorhabditis elegans. Int Rev Cytol. 1989;114:81–123. doi: 10.1016/s0074-7696(08)60859-1. [DOI] [PubMed] [Google Scholar]
  32. 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 U S A. 1982 Mar;79(5):1558–1562. doi: 10.1073/pnas.79.5.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tam L. W., Kirk D. L. The program for cellular differentiation in Volvox carteri as revealed by molecular analysis of development in a gonidialess/somatic regenerator mutant. Development. 1991 Jun;112(2):571–580. doi: 10.1242/dev.112.2.571. [DOI] [PubMed] [Google Scholar]

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