Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1985 May 1;100(5):1623–1636. doi: 10.1083/jcb.100.5.1623

Reversible chromosome condensation induced in Drosophila embryos by anoxia: visualization of interphase nuclear organization

PMCID: PMC2113892  PMID: 3921555

Abstract

We have studied the morphology of nuclei in Drosophila embryos during the syncytial blastoderm stages. Nuclei in living embryos were viewed with differential interference-contrast optics; in addition, both isolated nuclei and fixed preparations of whole embryos were examined after staining with a DNA-specific fluorescent dye. We find that: (a) The nuclear volumes increase dramatically during interphase and then decrease during prophase of each nuclear cycle, with the magnitude of the nuclear volume increase being greatest for those cycles with the shortest interphase. (b) Oxygen deprivation of embryos produces a rapid developmental arrest that is reversible upon reaeration. During this arrest, interphase chromosomes condense against the nuclear envelope and the nuclear volumes increase dramatically. In these nuclei, individual chromosomes are clearly visible, and each condensed chromosome can be seen to adhere along its entire length to the inner surface of the swollen nuclear envelope, leaving the lumen of the nucleus devoid of DNA. (c) In each interphase nucleus the chromosomes are oriented in the "telophase configuration," with all centromeres and all telomeres at opposite poles of the nucleus; all nuclei at the embryo periphery (with the exception of the pole cell nuclei) are oriented with their centromeric poles pointing to the embryo exterior.

Full Text

The Full Text of this article is available as a PDF (3.3 MB).

Selected References

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

  1. Appels R., Bell P. B., Ringertz N. R. The first division of HeLa times chick erythrocyte heterokaryons. Transfer of chick nuclei to daughter cells. Exp Cell Res. 1975 Apr;92(1):79–86. doi: 10.1016/0014-4827(75)90639-4. [DOI] [PubMed] [Google Scholar]
  2. Comings D. E. The rationale for an ordered arrangement of chromatin in the interphase nucleus. Am J Hum Genet. 1968 Sep;20(5):440–460. [PMC free article] [PubMed] [Google Scholar]
  3. Ellison J. R., Barr H. J. Quinacrine fluorescence of specific chromosome regions. Late replication and high A: T content in Samoaia leonensis. Chromosoma. 1972;36(4):375–390. doi: 10.1007/BF00336794. [DOI] [PubMed] [Google Scholar]
  4. Ellison J. R., Howard G. C. Non-random position of the A-T rich DNA sequences in early embryos of Drosophila virilis. Chromosoma. 1981;83(4):555–561. doi: 10.1007/BF00328279. [DOI] [PubMed] [Google Scholar]
  5. Foe V. E., Alberts B. M. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci. 1983 May;61:31–70. doi: 10.1242/jcs.61.1.31. [DOI] [PubMed] [Google Scholar]
  6. Fullilove S. L., Jacobson A. G. Nuclear elongation and cytokinesis in Drosophila montana. Dev Biol. 1971 Dec;26(4):560–577. doi: 10.1016/0012-1606(71)90141-2. [DOI] [PubMed] [Google Scholar]
  7. Gerace L., Blobel G. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell. 1980 Jan;19(1):277–287. doi: 10.1016/0092-8674(80)90409-2. [DOI] [PubMed] [Google Scholar]
  8. Gerace L., Blum A., Blobel G. Immunocytochemical localization of the major polypeptides of the nuclear pore complex-lamina fraction. Interphase and mitotic distribution. J Cell Biol. 1978 Nov;79(2 Pt 1):546–566. doi: 10.1083/jcb.79.2.546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gurdon J. B. Changes in somatic cell nuclei inserted into growing and maturing amphibian oocytes. J Embryol Exp Morphol. 1968 Nov;20(3):401–414. [PubMed] [Google Scholar]
  10. Harris H. The reactivation of the red cell nucleus. J Cell Sci. 1967 Mar;2(1):23–32. doi: 10.1242/jcs.2.1.23. [DOI] [PubMed] [Google Scholar]
  11. Horowitz S. B., Paine P. L. Cytoplasmic exclusion as a basis for asymmetric nucleocytoplasmic solute distributions. Nature. 1976 Mar 11;260(5547):151–153. doi: 10.1038/260151a0. [DOI] [PubMed] [Google Scholar]
  12. Johnson R. T., Rao P. N. Mammalian cell fusion: induction of premature chromosome condensation in interphase nuclei. Nature. 1970 May 23;226(5247):717–722. doi: 10.1038/226717a0. [DOI] [PubMed] [Google Scholar]
  13. Lamb M. M., Laird C. D. Increase in nuclear poly(A)-containing RNA at syncytial blastoderm in Drosophila melanogaster embryos. Dev Biol. 1976 Aug;52(1):31–42. doi: 10.1016/0012-1606(76)90004-x. [DOI] [PubMed] [Google Scholar]
  14. Lewis M., Helmsing P. J., Ashburner M. Parallel changes in puffing activity and patterns of protein synthesis in salivary glands of Drosophila. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3604–3608. doi: 10.1073/pnas.72.9.3604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lewis M., Helmsing P. J., Ashburner M. Parallel changes in puffing activity and patterns of protein synthesis in salivary glands of Drosophila. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3604–3608. doi: 10.1073/pnas.72.9.3604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lifschytz E., Hareven D. Heterochromatin markers: arrangement of obligatory heterochromatin, histone genes and multisite gene families in the interphase nucleus of D. melanogaster. Chromosoma. 1982;86(4):443–455. doi: 10.1007/BF00330120. [DOI] [PubMed] [Google Scholar]
  17. MAHOWALD A. P. ULTRASTRUCTURAL DIFFERENTIATIONS DURING FORMATION OF THE BLASTODERM IN THE DROSOPHILA MELANOGASTER EMBRYO. Dev Biol. 1963 Oct;8:186–204. doi: 10.1016/0012-1606(63)90041-1. [DOI] [PubMed] [Google Scholar]
  18. Mathog D., Hochstrasser M., Gruenbaum Y., Saumweber H., Sedat J. Characteristic folding pattern of polytene chromosomes in Drosophila salivary gland nuclei. 1984 Mar 29-Apr 4Nature. 308(5958):414–421. doi: 10.1038/308414a0. [DOI] [PubMed] [Google Scholar]
  19. Maul G. G. The nuclear and the cytoplasmic pore complex: structure, dynamics, distribution, and evolution. Int Rev Cytol Suppl. 1977;(6):75–186. [PubMed] [Google Scholar]
  20. McLaughlin A. C., Takeda H., Chance B. Rapid ATP assays in perfused mouse liver by 31P NMR. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5445–5449. doi: 10.1073/pnas.76.11.5445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mitchison T. J., Sedat J. Localization of antigenic determinants in whole Drosophila embryos. Dev Biol. 1983 Sep;99(1):261–264. doi: 10.1016/0012-1606(83)90275-0. [DOI] [PubMed] [Google Scholar]
  22. Newman S. M., Jr, Schubiger G. A morphological and developmental study of Drosophila embryos ligated during nuclear multiplication. Dev Biol. 1980 Sep;79(1):128–138. doi: 10.1016/0012-1606(80)90078-0. [DOI] [PubMed] [Google Scholar]
  23. Röhme D. Evidence suggesting chromosome continuity during the S phase of Indian muntjac cells. Hereditas. 1975;80(1):145–149. doi: 10.1111/j.1601-5223.1975.tb01510.x. [DOI] [PubMed] [Google Scholar]
  24. Velazquez J. M., Lindquist S. hsp70: nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell. 1984 Mar;36(3):655–662. doi: 10.1016/0092-8674(84)90345-3. [DOI] [PubMed] [Google Scholar]
  25. Zalokar M. Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev Biol. 1976 Apr;49(2):425–437. doi: 10.1016/0012-1606(76)90185-8. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES