Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1993 Feb 1;120(3):591–600. doi: 10.1083/jcb.120.3.591

The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis

PMCID: PMC2119536  PMID: 8425892

Abstract

We have determined the position within the nucleus of homologous sites of the histone gene cluster in Drosophila melanogaster using in situ hybridization and high-resolution, three-dimensional wide field fluorescence microscopy. A 4.8-kb biotinylated probe for the histone gene repeat, located approximately midway along the short arm of chromosome 2, was hybridized to whole-mount embryos in late syncytial and early cellular blastoderm stages. Our results show that the two homologous histone loci are distinct and separate through all stages of the cell cycle up to nuclear cycle 13. By dramatic contrast, the two homologous clusters were found to colocalize with high frequency during interphase of cycle 14. Concomitant with homolog pairing at cycle 14, both histone loci were also found to move from their position near the midline of the nucleus toward the apical side. This result suggests that coincident with the initiation of zygotic transcription, there is dramatic chromosome and nuclear reorganization between nuclear cycles 13 and 14.

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. Anderson K. V., Lengyel J. A. Rates of synthesis of major classes of RNA in Drosophila embryos. Dev Biol. 1979 May;70(1):217–231. doi: 10.1016/0012-1606(79)90018-6. [DOI] [PubMed] [Google Scholar]
  2. Arnoldus E. P., Peters A. C., Bots G. T., Raap A. K., van der Ploeg M. Somatic pairing of chromosome 1 centromeres in interphase nuclei of human cerebellum. Hum Genet. 1989 Oct;83(3):231–234. doi: 10.1007/BF00285162. [DOI] [PubMed] [Google Scholar]
  3. Avivi L., Feldman M. Arrangement of chromosomes in the interphase nucleus of plants. Hum Genet. 1980;55(3):281–295. doi: 10.1007/BF00290206. [DOI] [PubMed] [Google Scholar]
  4. Belmont A. S., Braunfeld M. B., Sedat J. W., Agard D. A. Large-scale chromatin structural domains within mitotic and interphase chromosomes in vivo and in vitro. Chromosoma. 1989 Aug;98(2):129–143. doi: 10.1007/BF00291049. [DOI] [PubMed] [Google Scholar]
  5. Billia F., de Boni U. Localization of centromeric satellite and telomeric DNA sequences in dorsal root ganglion neurons, in vitro. J Cell Sci. 1991 Sep;100(Pt 1):219–226. doi: 10.1242/jcs.100.1.219. [DOI] [PubMed] [Google Scholar]
  6. Coen E. S., Carpenter R. A semi-dominant allele, niv-525, acts in trans to inhibit expression of its wild-type homologue in Antirrhinum majus. EMBO J. 1988 Apr;7(4):877–883. doi: 10.1002/j.1460-2075.1988.tb02891.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dancis B. M., Holmquist G. P. Telomere replication and fusion in eukaryotes. J Theor Biol. 1979 May 21;78(2):211–224. doi: 10.1016/0022-5193(79)90265-0. [DOI] [PubMed] [Google Scholar]
  8. Edgar B. A., Schubiger G. Parameters controlling transcriptional activation during early Drosophila development. Cell. 1986 Mar 28;44(6):871–877. doi: 10.1016/0092-8674(86)90009-7. [DOI] [PubMed] [Google Scholar]
  9. Foe V. E., Alberts B. M. Reversible chromosome condensation induced in Drosophila embryos by anoxia: visualization of interphase nuclear organization. J Cell Biol. 1985 May;100(5):1623–1636. doi: 10.1083/jcb.100.5.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Foe V. E. Mitotic domains reveal early commitment of cells in Drosophila embryos. Development. 1989 Sep;107(1):1–22. [PubMed] [Google Scholar]
  12. Gelbart W. M. Synapsis-dependent allelic complementation at the decapentaplegic gene complex in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2636–2640. doi: 10.1073/pnas.79.8.2636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. HANNAH A. Localization and function of heterochromatin in Drosophila melanogaster. Adv Genet. 1951;4:87–125. doi: 10.1016/s0065-2660(08)60232-1. [DOI] [PubMed] [Google Scholar]
  14. Hawley R. S. Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. I. Evidence for and mapping of the sites. Genetics. 1980 Mar;94(3):625–646. doi: 10.1093/genetics/94.3.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hawley R. S. Genetic and molecular analysis of a simple disjunctional system in Drosophila melanogaster. Prog Clin Biol Res. 1989;311:277–302. [PubMed] [Google Scholar]
  16. Henikoff S., Dreesen T. D. Trans-inactivation of the Drosophila brown gene: evidence for transcriptional repression and somatic pairing dependence. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6704–6708. doi: 10.1073/pnas.86.17.6704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hilliker A. J., Appels R. The arrangement of interphase chromosomes: structural and functional aspects. Exp Cell Res. 1989 Dec;185(2):267–318. doi: 10.1016/0014-4827(89)90301-7. [DOI] [PubMed] [Google Scholar]
  18. Hiraoka Y., Agard D. A., Sedat J. W. Temporal and spatial coordination of chromosome movement, spindle formation, and nuclear envelope breakdown during prometaphase in Drosophila melanogaster embryos. J Cell Biol. 1990 Dec;111(6 Pt 2):2815–2828. doi: 10.1083/jcb.111.6.2815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hiraoka Y., Swedlow J. R., Paddy M. R., Agard D. A., Sedat J. W. Three-dimensional multiple-wavelength fluorescence microscopy for the structural analysis of biological phenomena. Semin Cell Biol. 1991 Jun;2(3):153–165. [PubMed] [Google Scholar]
  20. Jack J. W., Judd B. H. Allelic pairing and gene regulation: A model for the zeste-white interaction in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1368–1372. doi: 10.1073/pnas.76.3.1368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Korge G. Direct correlation between a chromosome puff and the synthesis of a larval saliva protein in Drosophila melanogaster. Chromosoma. 1977 Jul 5;62(2):155–174. doi: 10.1007/BF00292637. [DOI] [PubMed] [Google Scholar]
  22. Lawrence J. B., Singer R. H., Marselle L. M. Highly localized tracks of specific transcripts within interphase nuclei visualized by in situ hybridization. Cell. 1989 May 5;57(3):493–502. doi: 10.1016/0092-8674(89)90924-0. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Lifton R. P., Goldberg M. L., Karp R. W., Hogness D. S. The organization of the histone genes in Drosophila melanogaster: functional and evolutionary implications. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1047–1051. doi: 10.1101/sqb.1978.042.01.105. [DOI] [PubMed] [Google Scholar]
  25. Maguire M. P. The mechanism of meiotic homologue pairing. J Theor Biol. 1984 Feb 21;106(4):605–615. doi: 10.1016/0022-5193(84)90010-9. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Pardue M. L., Hennig W. Heterochromatin: junk or collectors item? Chromosoma. 1990 Dec;100(1):3–7. doi: 10.1007/BF00337597. [DOI] [PubMed] [Google Scholar]
  28. Pirrotta V. Transvection and long-distance gene regulation. Bioessays. 1990 Sep;12(9):409–414. doi: 10.1002/bies.950120903. [DOI] [PubMed] [Google Scholar]
  29. Shaw P. J., Agard D. A., Hiraoka Y., Sedat J. W. Tilted view reconstruction in optical microscopy. Three-dimensional reconstruction of Drosophila melanogaster embryo nuclei. Biophys J. 1989 Jan;55(1):101–110. doi: 10.1016/S0006-3495(89)82783-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shermoen A. W., O'Farrell P. H. Progression of the cell cycle through mitosis leads to abortion of nascent transcripts. Cell. 1991 Oct 18;67(2):303–310. doi: 10.1016/0092-8674(91)90182-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Smith A. V., Orr-Weaver T. L. The regulation of the cell cycle during Drosophila embryogenesis: the transition to polyteny. Development. 1991 Aug;112(4):997–1008. doi: 10.1242/dev.112.4.997. [DOI] [PubMed] [Google Scholar]
  32. Smolik-Utlaut S. M., Gelbart W. M. The effects of chromosomal rearrangements on the zeste-white interaction in Drosophila melanogaster. Genetics. 1987 Jun;116(2):285–298. doi: 10.1093/genetics/116.2.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tartof K. D., Henikoff S. Trans-sensing effects from Drosophila to humans. Cell. 1991 Apr 19;65(2):201–203. doi: 10.1016/0092-8674(91)90153-p. [DOI] [PubMed] [Google Scholar]
  34. Wakimoto B. T., Hearn M. G. The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster. Genetics. 1990 May;125(1):141–154. doi: 10.1093/genetics/125.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wu C. T., Goldberg M. L. The Drosophila zeste gene and transvection. Trends Genet. 1989 Jun;5(6):189–194. doi: 10.1016/0168-9525(89)90074-7. [DOI] [PubMed] [Google Scholar]
  36. Young B. S., Pession A., Traverse K. L., French C., Pardue M. L. Telomere regions in Drosophila share complex DNA sequences with pericentric heterochromatin. Cell. 1983 Aug;34(1):85–94. doi: 10.1016/0092-8674(83)90138-1. [DOI] [PubMed] [Google Scholar]

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

RESOURCES