Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1998 Jul;149(3):1451–1464. doi: 10.1093/genetics/149.3.1451

Chromosome rearrangements induce both variegated and reduced, uniform expression of heterochromatic genes in a development-specific manner.

K S Weiler 1, B T Wakimoto 1
PMCID: PMC1460224  PMID: 9649533

Abstract

In Drosophila melanogaster, chromosome rearrangements that juxtapose euchromatin and heterochromatin can result in position effect variegation (PEV), the variable expression of heterochromatic and euchromatic genes in the vicinity of the novel breakpoint. We examined PEV of the heterochromatic light (lt) and concertina (cta) genes in order to investigate potential tissue or developmental differences in chromosome structure that might be informative for comparing the mechanisms of PEV of heterochromatic and euchromatic genes. We employed tissue pigmentation and in situ hybridization to RNA to assess expression of lt in individual cells of multiple tissues during development. Variegation of lt was induced in the adult eye, larval salivary glands and larval Malpighian tubules for each of three different chromosome rearrangements. The relative severity of the effect in these tissues was not tissue-specific but rather was characteristic of each rearrangement. Surprisingly, larval imaginal discs did not exhibit variegated lt expression. Instead, a uniform reduction of the lt transcript was observed, which correlated in magnitude with the degree of variegation. The same results were obtained for cta expression. These two distinct effects of rearrangements on heterochromatic gene expression correlated with the developmental stage of the tissue. These results have implications for models of heterochromatin formation and the nuclear organization of chromosomes during development and differentiation.

Full Text

The Full Text of this article is available as a PDF (655.8 KB).

Selected References

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

  1. Aparicio O. M., Gottschling D. E. Overcoming telomeric silencing: a trans-activator competes to establish gene expression in a cell cycle-dependent way. Genes Dev. 1994 May 15;8(10):1133–1146. doi: 10.1101/gad.8.10.1133. [DOI] [PubMed] [Google Scholar]
  2. Boyd L., O'Toole E., Thummel C. S. Patterns of E74A RNA and protein expression at the onset of metamorphosis in Drosophila. Development. 1991 Aug;112(4):981–995. doi: 10.1242/dev.112.4.981. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Devlin R. H., Bingham B., Wakimoto B. T. The organization and expression of the light gene, a heterochromatic gene of Drosophila melanogaster. Genetics. 1990 May;125(1):129–140. doi: 10.1093/genetics/125.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Eberl D. F., Duyf B. J., Hilliker A. J. The role of heterochromatin in the expression of a heterochromatic gene, the rolled locus of Drosophila melanogaster. Genetics. 1993 May;134(1):277–292. doi: 10.1093/genetics/134.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edgar B. A., O'Farrell P. H. Genetic control of cell division patterns in the Drosophila embryo. Cell. 1989 Apr 7;57(1):177–187. doi: 10.1016/0092-8674(89)90183-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fanti L., Berloco M., Pimpinelli S. Carnitine suppression of position-effect variegation in Drosophila melanogaster. Mol Gen Genet. 1994 Sep 28;244(6):588–595. doi: 10.1007/BF00282748. [DOI] [PubMed] [Google Scholar]
  9. Golic M. M., Golic K. G. A quantitative measure of the mitotic pairing of alleles in Drosophila melanogaster and the influence of structural heterozygosity. Genetics. 1996 May;143(1):385–400. doi: 10.1093/genetics/143.1.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hessler A Y. V-Type Position Effects at the Light Locus in Drosophila Melanogaster. Genetics. 1958 May;43(3):395–403. doi: 10.1093/genetics/43.3.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Howe M., Dimitri P., Berloco M., Wakimoto B. T. Cis-effects of heterochromatin on heterochromatic and euchromatic gene activity in Drosophila melanogaster. Genetics. 1995 Jul;140(3):1033–1045. doi: 10.1093/genetics/140.3.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Janning W. Bestimmung des Heterochromatisierungsstadiums beim white-Positionseffekt mittels röntgeninduzierter mitotischer Rekombination in der Augenanlage von Drosophila melanogaster. Mol Gen Genet. 1970;107(2):128–149. doi: 10.1007/BF00333629. [DOI] [PubMed] [Google Scholar]
  13. Kim N., Kim J., Park D., Rosen C., Dorsett D., Yim J. Structure and expression of wild-type and suppressible alleles of the Drosophila purple gene. Genetics. 1996 Apr;142(4):1157–1168. doi: 10.1093/genetics/142.4.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. LEWIS E. B. The phenomenon of position effect. Adv Genet. 1950;3:73–115. doi: 10.1016/s0065-2660(08)60083-8. [DOI] [PubMed] [Google Scholar]
  15. Lu B. Y., Bishop C. P., Eissenberg J. C. Developmental timing and tissue specificity of heterochromatin-mediated silencing. EMBO J. 1996 Mar 15;15(6):1323–1332. [PMC free article] [PubMed] [Google Scholar]
  16. Martin D. I., Whitelaw E. The vagaries of variegating transgenes. Bioessays. 1996 Nov;18(11):919–923. doi: 10.1002/bies.950181111. [DOI] [PubMed] [Google Scholar]
  17. Martínez-Balbás M. A., Dey A., Rabindran S. K., Ozato K., Wu C. Displacement of sequence-specific transcription factors from mitotic chromatin. Cell. 1995 Oct 6;83(1):29–38. doi: 10.1016/0092-8674(95)90231-7. [DOI] [PubMed] [Google Scholar]
  18. Milot E., Strouboulis J., Trimborn T., Wijgerde M., de Boer E., Langeveld A., Tan-Un K., Vergeer W., Yannoutsos N., Grosveld F. Heterochromatin effects on the frequency and duration of LCR-mediated gene transcription. Cell. 1996 Oct 4;87(1):105–114. doi: 10.1016/s0092-8674(00)81327-6. [DOI] [PubMed] [Google Scholar]
  19. Milán M., Campuzano S., García-Bellido A. Cell cycling and patterned cell proliferation in the wing primordium of Drosophila. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):640–645. doi: 10.1073/pnas.93.2.640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Moore G. D., Sinclair D. A., Grigliatti T. A. Histone Gene Multiplicity and Position Effect Variegation in DROSOPHILA MELANOGASTER. Genetics. 1983 Oct;105(2):327–344. doi: 10.1093/genetics/105.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mottus R., Reeves R., Grigliatti T. A. Butyrate suppression of position-effect variegation in Drosophila melanogaster. Mol Gen Genet. 1980;178(2):465–469. doi: 10.1007/BF00270501. [DOI] [PubMed] [Google Scholar]
  22. O'Farrell P. H., Edgar B. A., Lakich D., Lehner C. F. Directing cell division during development. Science. 1989 Nov 3;246(4930):635–640. doi: 10.1126/science.2683080. [DOI] [PubMed] [Google Scholar]
  23. Parks S., Wieschaus E. The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell. 1991 Jan 25;64(2):447–458. doi: 10.1016/0092-8674(91)90652-f. [DOI] [PubMed] [Google Scholar]
  24. Reuter G., Dorn R., Hoffmann H. J. Butyrate sensitive suppressor of position-effect variegation mutations in Drosophila melanogaster. Mol Gen Genet. 1982;188(3):480–485. doi: 10.1007/BF00330052. [DOI] [PubMed] [Google Scholar]
  25. Reuter G., Spierer P. Position effect variegation and chromatin proteins. Bioessays. 1992 Sep;14(9):605–612. doi: 10.1002/bies.950140907. [DOI] [PubMed] [Google Scholar]
  26. Tobler J. E., Yim J. J., Grell E. H., Jacobson K. B. Developmental changes of sepiapterin synthase activity associated with a variegated purple gene in Drosophila melanogaster. Biochem Genet. 1979 Feb;17(1-2):197–206. doi: 10.1007/BF00484485. [DOI] [PubMed] [Google Scholar]
  27. Weiler K. S., Wakimoto B. T. Heterochromatin and gene expression in Drosophila. Annu Rev Genet. 1995;29:577–605. doi: 10.1146/annurev.ge.29.120195.003045. [DOI] [PubMed] [Google Scholar]
  28. Wines D. R., Talbert P. B., Clark D. V., Henikoff S. Introduction of a DNA methyltransferase into Drosophila to probe chromatin structure in vivo. Chromosoma. 1996;104(5):332–340. doi: 10.1007/BF00337221. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES