Skip to main content
Genetics logoLink to Genetics
. 2003 Nov;165(3):1183–1193. doi: 10.1093/genetics/165.3.1183

Heterochromatic self-association, a determinant of nuclear organization, does not require sequence homology in Drosophila.

Brian T Sage 1, Amy K Csink 1
PMCID: PMC1462834  PMID: 14668374

Abstract

Chromosomes of higher eukaryotes contain blocks of heterochromatin that can associate with each other in the interphase nucleus. A well-studied example of heterochromatic interaction is the brown(Dominant) (bwD) chromosome of D. melanogaster, which contains an approximately 1.6-Mbp insertion of AAGAG repeats near the distal tip of chromosome 2. This insertion causes association of the tip with the centric heterochromatin of chromosome 2 (2h), which contains megabases of AAGAG repeats. Here we describe an example, other than bwD, in which distally translocated heterochromatin associates with centric heterochromatin. Additionally, we show that when a translocation places bwD on a different chromosome, bwD tends to associate with the centric heterochromatin of this chromosome, even when the chromosome contains a small fraction of the sequence homology present elsewhere. To further test the importance of sequence homology in these interactions, we used interspecific mating to introgress the bwD allele from D. melanogaster into D. simulans, which lacks the AAGAG on the autosomes. We find that D. simulans bwD associates with 2h, which lacks the AAGAG sequence, while it does not associate with the AAGAG containing X chromosome heterochromatin. Our results show that intranuclear association of separate heterochromatic blocks does not require that they contain the same sequence.

Full Text

The Full Text of this article is available as a PDF (401.8 KB).

Selected References

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

  1. Barbash D. A., Roote J., Ashburner M. The Drosophila melanogaster hybrid male rescue gene causes inviability in male and female species hybrids. Genetics. 2000 Apr;154(4):1747–1771. doi: 10.1093/genetics/154.4.1747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barbash Daniel A., Ashburner Michael. A novel system of fertility rescue in Drosophila hybrids reveals a link between hybrid lethality and female sterility. Genetics. 2003 Jan;163(1):217–226. doi: 10.1093/genetics/163.1.217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown K. E., Guest S. S., Smale S. T., Hahm K., Merkenschlager M., Fisher A. G. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell. 1997 Dec 12;91(6):845–854. doi: 10.1016/s0092-8674(00)80472-9. [DOI] [PubMed] [Google Scholar]
  4. Carmena M., Abad J. P., Villasante A., Gonzalez C. The Drosophila melanogaster dodecasatellite sequence is closely linked to the centromere and can form connections between sister chromatids during mitosis. J Cell Sci. 1993 May;105(Pt 1):41–50. doi: 10.1242/jcs.105.1.41. [DOI] [PubMed] [Google Scholar]
  5. Carmena M., González C. Transposable elements map in a conserved pattern of distribution extending from beta-heterochromatin to centromeres in Drosophila melanogaster. Chromosoma. 1995 Jul;103(10):676–684. doi: 10.1007/BF00344228. [DOI] [PubMed] [Google Scholar]
  6. Cerda M. C., Berríos S., Fernández-Donoso R., Garagna S., Redi C. Organisation of complex nuclear domains in somatic mouse cells. Biol Cell. 1999 Jan;91(1):55–65. [PubMed] [Google Scholar]
  7. Csink A. K., Henikoff S. Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature. 1996 Jun 6;381(6582):529–531. doi: 10.1038/381529a0. [DOI] [PubMed] [Google Scholar]
  8. Csink A. K., Henikoff S. Something from nothing: the evolution and utility of satellite repeats. Trends Genet. 1998 May;14(5):200–204. doi: 10.1016/s0168-9525(98)01444-9. [DOI] [PubMed] [Google Scholar]
  9. Csink Amy K., Bounoutas Alexander, Griffith Michelle L., Sabl Joy F., Sage Brian T. Differential gene silencing by trans-heterochromatin in Drosophila melanogaster. Genetics. 2002 Jan;160(1):257–269. doi: 10.1093/genetics/160.1.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Davis A. W., Roote J., Morley T., Sawamura K., Herrmann S., Ashburner M. Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature. 1996 Mar 14;380(6570):157–159. doi: 10.1038/380157a0. [DOI] [PubMed] [Google Scholar]
  11. Delattre M., Spierer A., Tonka C. H., Spierer P. The genomic silencing of position-effect variegation in Drosophila melanogaster: interaction between the heterochromatin-associated proteins Su(var)3-7 and HP1. J Cell Sci. 2000 Dec;113(Pt 23):4253–4261. doi: 10.1242/jcs.113.23.4253. [DOI] [PubMed] [Google Scholar]
  12. Dernburg A. F., Broman K. W., Fung J. C., Marshall W. F., Philips J., Agard D. A., Sedat J. W. Perturbation of nuclear architecture by long-distance chromosome interactions. Cell. 1996 May 31;85(5):745–759. doi: 10.1016/s0092-8674(00)81240-4. [DOI] [PubMed] [Google Scholar]
  13. Dorer D. R., Henikoff S. Transgene repeat arrays interact with distant heterochromatin and cause silencing in cis and trans. Genetics. 1997 Nov;147(3):1181–1190. doi: 10.1093/genetics/147.3.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Francastel C., Schübeler D., Martin D. I., Groudine M. Nuclear compartmentalization and gene activity. Nat Rev Mol Cell Biol. 2000 Nov;1(2):137–143. doi: 10.1038/35040083. [DOI] [PubMed] [Google Scholar]
  15. Francastel C., Walters M. C., Groudine M., Martin D. I. A functional enhancer suppresses silencing of a transgene and prevents its localization close to centrometric heterochromatin. Cell. 1999 Oct 29;99(3):259–269. doi: 10.1016/s0092-8674(00)81657-8. [DOI] [PubMed] [Google Scholar]
  16. Fung J. C., Marshall W. F., Dernburg A., Agard D. A., Sedat J. W. Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J Cell Biol. 1998 Apr 6;141(1):5–20. doi: 10.1083/jcb.141.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Henikoff S., Jackson J. M., Talbert P. B. Distance and pairing effects on the brownDominant heterochromatic element in Drosophila. Genetics. 1995 Jul;140(3):1007–1017. doi: 10.1093/genetics/140.3.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hiraoka Y., Dernburg A. F., Parmelee S. J., Rykowski M. C., Agard D. A., Sedat J. W. The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J Cell Biol. 1993 Feb;120(3):591–600. doi: 10.1083/jcb.120.3.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lee C., Wevrick R., Fisher R. B., Ferguson-Smith M. A., Lin C. C. Human centromeric DNAs. Hum Genet. 1997 Sep;100(3-4):291–304. doi: 10.1007/s004390050508. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Locke J., Kotarski M. A., Tartof K. D. Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect. Genetics. 1988 Sep;120(1):181–198. doi: 10.1093/genetics/120.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lohe A. R., Brutlag D. L. Identical satellite DNA sequences in sibling species of Drosophila. J Mol Biol. 1987 Mar 20;194(2):161–170. doi: 10.1016/0022-2836(87)90365-2. [DOI] [PubMed] [Google Scholar]
  23. Parada Luis, Misteli Tom. Chromosome positioning in the interphase nucleus. Trends Cell Biol. 2002 Sep;12(9):425–432. doi: 10.1016/s0962-8924(02)02351-6. [DOI] [PubMed] [Google Scholar]
  24. Platero J. S., Csink A. K., Quintanilla A., Henikoff S. Changes in chromosomal localization of heterochromatin-binding proteins during the cell cycle in Drosophila. J Cell Biol. 1998 Mar 23;140(6):1297–1306. doi: 10.1083/jcb.140.6.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Saffery R., Irvine D. V., Griffiths B., Kalitsis P., Wordeman L., Choo K. H. Human centromeres and neocentromeres show identical distribution patterns of >20 functionally important kinetochore-associated proteins. Hum Mol Genet. 2000 Jan 22;9(2):175–185. doi: 10.1093/hmg/9.2.175. [DOI] [PubMed] [Google Scholar]
  26. Smoller D. A., Petrov D., Hartl D. L. Characterization of bacteriophage P1 library containing inserts of Drosophila DNA of 75-100 kilobase pairs. Chromosoma. 1991 Sep;100(8):487–494. doi: 10.1007/BF00352199. [DOI] [PubMed] [Google Scholar]
  27. Talbert P. B., Henikoff S. A reexamination of spreading of position-effect variegation in the white-roughest region of Drosophila melanogaster. Genetics. 2000 Jan;154(1):259–272. doi: 10.1093/genetics/154.1.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Talbert P. B., LeCiel C. D., Henikoff S. Modification of the Drosophila heterochromatic mutation brownDominant by linkage alterations. Genetics. 1994 Feb;136(2):559–571. doi: 10.1093/genetics/136.2.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wu C. I., Lyttle T. W., Wu M. L., Lin G. F. Association between a satellite DNA sequence and the Responder of Segregation Distorter in D. melanogaster. Cell. 1988 Jul 15;54(2):179–189. doi: 10.1016/0092-8674(88)90550-8. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES