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. 1986 Jan 1;102(1):112–123. doi: 10.1083/jcb.102.1.112

Spatial organization of chromosomes in the salivary gland nuclei of Drosophila melanogaster

PMCID: PMC2114037  PMID: 3079766

Abstract

Using a computer-based system for model building and analysis, three- dimensional models of 24 Drosophila melanogaster salivary gland nuclei have been constructed from optically or physically sectioned glands, allowing several generalizations about chromosome folding and packaging in these nuclei. First and most surprising, the prominent coiling of the chromosomes is strongly chiral, with right-handed gyres predominating. Second, high frequency appositions between certain loci and the nuclear envelope appear almost exclusively at positions of intercalary heterochromatin; in addition, the chromocenter is always apposed to the envelope. Third, chromosomes are invariably separated into mutually exclusive spatial domains while usually extending across the nucleus in a polarized (Rabl) orientation. Fourth, the arms of each autosome are almost always juxtaposed, but no other relative arm positions are strongly favored. Finally, despite these nonrandom structural features, each chromosome is found to fold into a wide variety of different configurations. In addition, a set of nuclei has been analyzed in which the normally aggregrated centromeric regions of the chromosomes are located far apart from one another. These nuclei have the same architectural motifs seen in normal nuclei. This implies that such characteristics as separate chromosome domains and specific chromosome-nuclear envelope contacts are largely independent of the relative placement of the different chromosomes within the nucleus.

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Selected References

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  1. Agard D. A., Sedat J. W. Three-dimensional architecture of a polytene nucleus. Nature. 1983 Apr 21;302(5910):676–681. doi: 10.1038/302676a0. [DOI] [PubMed] [Google Scholar]
  2. Appels R., Steffensen D. M., Craig S. A new method for mapping the three-dimensional distribution of DNA sequences in nuclei. Exp Cell Res. 1979 Dec;124(2):436–441. doi: 10.1016/0014-4827(79)90220-9. [DOI] [PubMed] [Google Scholar]
  3. Ashburner M. Puffing patterns in Drosophila melanogaster and related species. Results Probl Cell Differ. 1972;4:101–151. doi: 10.1007/978-3-540-37164-9_5. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Barr H. J., Ellison J. R. Ectopic pairing of chromosome regions containing chemically similar DNA. Chromosoma. 1972;39(1):53–61. doi: 10.1007/BF00320590. [DOI] [PubMed] [Google Scholar]
  6. Becker H. J. The influence of heterochromatin, inversion-heterozygosity and somatic pairing on x-ray induced mitotic recombination in Drosophila melanogaster. Mol Gen Genet. 1969;105(3):203–218. doi: 10.1007/BF00337472. [DOI] [PubMed] [Google Scholar]
  7. Braun W. Representation of short and long-range handedness in protein structures by signed distance maps. J Mol Biol. 1983 Feb 5;163(4):613–621. doi: 10.1016/0022-2836(83)90114-6. [DOI] [PubMed] [Google Scholar]
  8. Burgoyne L. A., Wagar M. A., Atkinson M. R. Calcium-dependent priming of DNA synthesis in isolated rat liver nuclei. Biochem Biophys Res Commun. 1970 Apr 24;39(2):254–259. doi: 10.1016/0006-291x(70)90786-2. [DOI] [PubMed] [Google Scholar]
  9. Comings D. E. Arrangement of chromatin in the nucleus. Hum Genet. 1980 Feb;53(2):131–143. doi: 10.1007/BF00273484. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. GAY H. Nucleocytoplasmic relations in Drosophila. Cold Spring Harb Symp Quant Biol. 1956;21:257–269. doi: 10.1101/sqb.1956.021.01.021. [DOI] [PubMed] [Google Scholar]
  13. Gruenbaum Y., Hochstrasser M., Mathog D., Saumweber H., Agard D. A., Sedat J. W. Spatial organization of the Drosophila nucleus: a three-dimensional cytogenetic study. J Cell Sci Suppl. 1984;1:223–234. doi: 10.1242/jcs.1984.supplement_1.14. [DOI] [PubMed] [Google Scholar]
  14. Hammond M. P., Laird C. D. Control of DNA replication and spatial distribution of defined DNA sequences in salivary gland cells of Drosophila melanogaster. Chromosoma. 1985;91(3-4):279–286. doi: 10.1007/BF00328223. [DOI] [PubMed] [Google Scholar]
  15. Hancock R., Boulikas T. Functional organization in the nucleus. Int Rev Cytol. 1982;79:165–214. doi: 10.1016/s0074-7696(08)61674-5. [DOI] [PubMed] [Google Scholar]
  16. Herreros B., Giannelli F. Spatial distribution of old and new chromatid sub-units and frequency of chromatid exchanges in induced human lymphocyte endoreduplications. Nature. 1967 Oct 21;216(5112):286–288. doi: 10.1038/216286a0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  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. Mathog D., Hochstrasser M., Sedat J. W. Light microscope based analysis of three-dimensional structure: applications to the study of Drosophila salivary gland nuclei. I. Data collection and analysis. J Microsc. 1985 Mar;137(Pt 3):241–252. doi: 10.1111/j.1365-2818.1985.tb02582.x. [DOI] [PubMed] [Google Scholar]
  20. Ohnuki Y. Structure of chromosomes. I. Morphological studies of the spiral structure of human somatic chromosomes. Chromosoma. 1968;25(4):402–428. doi: 10.1007/BF02327721. [DOI] [PubMed] [Google Scholar]
  21. Pearson M. J. Polyteny and the functional significance of the polytene cell cycle. J Cell Sci. 1974 Jul;15(2):457–479. doi: 10.1242/jcs.15.2.457. [DOI] [PubMed] [Google Scholar]
  22. Probeck H. D., Rensing L. Cellular patterns of differing circadian rhythms and levels of RNA synthesis in Drosophila salivary glands. Cell Differ. 1974 Mar;2(6):337–345. doi: 10.1016/0045-6039(74)90012-8. [DOI] [PubMed] [Google Scholar]
  23. Rossman M. G., Liljas A. Letter: Recognition of structural domains in globular proteins. J Mol Biol. 1974 May 5;85(1):177–181. doi: 10.1016/0022-2836(74)90136-3. [DOI] [PubMed] [Google Scholar]
  24. Shields G., Sang J. H. Characteristics of five cell types appearing during in vitro culture of embryonic material from Drosophila melanogaster. J Embryol Exp Morphol. 1970 Feb;23(1):53–69. [PubMed] [Google Scholar]
  25. Sperling K., Lüdtke E. K. Arrangement of prematurely condensed chromosomes in cultured cells and lymphocytes of the Indian muntjac. Chromosoma. 1981;83(4):541–553. doi: 10.1007/BF00328278. [DOI] [PubMed] [Google Scholar]
  26. Sved J. A. Hybrid dysgenesis in Drosophila melanogaster: a possible explanation in terms of spatial organization of chromosomes. Aust J Biol Sci. 1976 Oct;29(4):375–388. doi: 10.1071/bi9760375. [DOI] [PubMed] [Google Scholar]
  27. Zorn C., Cremer C., Cremer T., Zimmer J. Unscheduled DNA synthesis after partial UV irradiation of the cell nucleus. Distribution in interphase and metaphase. Exp Cell Res. 1979 Nov;124(1):111–119. doi: 10.1016/0014-4827(79)90261-1. [DOI] [PubMed] [Google Scholar]

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