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. 1995 Sep;141(1):245–253. doi: 10.1093/genetics/141.1.245

Mutations of Zeste That Mediate Transvection Are Recessive Enhancers of Position-Effect Variegation in Drosophila Melanogaster

B H Judd 1
PMCID: PMC1206722  PMID: 8536972

Abstract

Evidence is presented demonstrating that mutations of zeste, particularly the null state, are strong recessive enhancers of position-effect variegation (PEV) for the white, roughest and Notch loci. The zeste locus encodes a DNA-binding protein that acts as a transcription factor and mediates transvection phenomena at several loci. Its involvement with these seemingly diverse phenomena suggests that the normal zeste product functions in the decondensation of chromatin. A model is presented proposing that zeste is important for opening and stabilizing domains of chromatin, a step in gene determination and the establishment of cell memory. It postulates that chromatin domains that have been structurally modified by chromosomal rearrangement or by insertion of transposable elements are particularly sensitive to the absence or modification of the zeste protein. Such a view unifies the role of zeste in transcription, transvection and PEV.

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Selected References

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  1. Adler P. N., Charlton J., Brunk B. Genetic interactions of the suppressor 2 of zeste region genes. Dev Genet. 1989;10(3):249–260. doi: 10.1002/dvg.1020100314. [DOI] [PubMed] [Google Scholar]
  2. Ashburner M. Gene activity dependent on chromosome synapsis in the polytene chromosomes of Drosophila melanogaster. Nature. 1967 Jun 10;214(5093):1159–1160. doi: 10.1038/2141159b0. [DOI] [PubMed] [Google Scholar]
  3. Babu P., Bhat S. Effect of zeste on white complementation. Basic Life Sci. 1980;16:35–40. doi: 10.1007/978-1-4684-7968-3_4. [DOI] [PubMed] [Google Scholar]
  4. Biggin M. D., Bickel S., Benson M., Pirrotta V., Tjian R. Zeste encodes a sequence-specific transcription factor that activates the Ultrabithorax promoter in vitro. Cell. 1988 Jun 3;53(5):713–722. doi: 10.1016/0092-8674(88)90089-x. [DOI] [PubMed] [Google Scholar]
  5. Biggin M. D., Tjian R. Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts. Cell. 1988 Jun 3;53(5):699–711. doi: 10.1016/0092-8674(88)90088-8. [DOI] [PubMed] [Google Scholar]
  6. Dorn R., Krauss V., Reuter G., Saumweber H. The enhancer of position-effect variegation of Drosophila, E(var)3-93D, codes for a chromatin protein containing a conserved domain common to several transcriptional regulators. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11376–11380. doi: 10.1073/pnas.90.23.11376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eissenberg J. C., James T. C., Foster-Hartnett D. M., Hartnett T., Ngan V., Elgin S. C. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9923–9927. doi: 10.1073/pnas.87.24.9923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eissenberg J. C. Position effect variegation in Drosophila: towards a genetics of chromatin assembly. Bioessays. 1989 Jul;11(1):14–17. doi: 10.1002/bies.950110105. [DOI] [PubMed] [Google Scholar]
  9. Fauvarque M. O., Dura J. M. polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila. Genes Dev. 1993 Aug;7(8):1508–1520. doi: 10.1101/gad.7.8.1508. [DOI] [PubMed] [Google Scholar]
  10. Garzino V., Pereira A., Laurenti P., Graba Y., Levis R. W., Le Parco Y., Pradel J. Cell lineage-specific expression of modulo, a dose-dependent modifier of variegation in Drosophila. EMBO J. 1992 Dec;11(12):4471–4479. doi: 10.1002/j.1460-2075.1992.tb05548.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Gelbart W. M., Wu C. T. Interactions of zeste mutations with loci exhibiting transvection effects in Drosophila melanogaster. Genetics. 1982 Oct;102(2):179–189. doi: 10.1093/genetics/102.2.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grigliatti T. Position-effect variegation--an assay for nonhistone chromosomal proteins and chromatin assembly and modifying factors. Methods Cell Biol. 1991;35:587–627. [PubMed] [Google Scholar]
  14. Hayashi S., Ruddell A., Sinclair D., Grigliatti T. Chromosomal structure is altered by mutations that suppress or enhance position effect variegation. Chromosoma. 1990 Oct;99(6):391–400. doi: 10.1007/BF01726690. [DOI] [PubMed] [Google Scholar]
  15. Hazelrigg T., Petersen S. An unusual genomic position effect on Drosophila white gene expression: pairing dependence, interactions with zeste, and molecular analysis of revertants. Genetics. 1992 Jan;130(1):125–138. doi: 10.1093/genetics/130.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Henikoff S. Position-effect variegation after 60 years. Trends Genet. 1990 Dec;6(12):422–426. doi: 10.1016/0168-9525(90)90304-o. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. James T. C., Elgin S. C. Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol. 1986 Nov;6(11):3862–3872. doi: 10.1128/mcb.6.11.3862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jones R. S., Gelbart W. M. Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics. 1990 Sep;126(1):185–199. doi: 10.1093/genetics/126.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Judd B. H. Transvection: allelic cross talk. Cell. 1988 Jun 17;53(6):841–843. doi: 10.1016/s0092-8674(88)90209-7. [DOI] [PubMed] [Google Scholar]
  22. Kassis J. A. Unusual properties of regulatory DNA from the Drosophila engrailed gene: three "pairing-sensitive" sites within a 1.6-kb region. Genetics. 1994 Mar;136(3):1025–1038. doi: 10.1093/genetics/136.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kassis J. A., VanSickle E. P., Sensabaugh S. M. A fragment of engrailed regulatory DNA can mediate transvection of the white gene in Drosophila. Genetics. 1991 Aug;128(4):751–761. doi: 10.1093/genetics/128.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kornher J. S., Kauffman S. A. Variegated expression of the Sgs-4 locus in Drosophila melanogaster. Chromosoma. 1986;94(3):205–216. doi: 10.1007/BF00288495. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Lefevre G., Jr, Green M. M. Genetic duplication in the white-split interval of the X chromosome in Drosophila melanogaster. Chromosoma. 1972;36(4):391–412. doi: 10.1007/BF00336795. [DOI] [PubMed] [Google Scholar]
  27. Leiserson W. M., Bonini N. M., Benzer S. Transvection at the eyes absent gene of Drosophila. Genetics. 1994 Dec;138(4):1171–1179. doi: 10.1093/genetics/138.4.1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mansukhani A., Crickmore A., Sherwood P. W., Goldberg M. L. DNA-binding properties of the Drosophila melanogaster zeste gene product. Mol Cell Biol. 1988 Feb;8(2):615–623. doi: 10.1128/mcb.8.2.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Miklos G. L., Yamamoto M. T., Davies J., Pirrotta V. Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome 4 and the beta-heterochromatin of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2051–2055. doi: 10.1073/pnas.85.7.2051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Paro R., Hogness D. S. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):263–267. doi: 10.1073/pnas.88.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pelegri F., Lehmann R. A role of polycomb group genes in the regulation of gap gene expression in Drosophila. Genetics. 1994 Apr;136(4):1341–1353. doi: 10.1093/genetics/136.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Peterson K. M., Davis P. S., Judd B. H. The determined state of white expression in the Drosophila eye is modified by zeste1 in the wzm family of mutants. Mol Gen Genet. 1994 Mar;242(6):717–726. doi: 10.1007/BF00283427. [DOI] [PubMed] [Google Scholar]
  33. Pirrotta V., Manet E., Hardon E., Bickel S. E., Benson M. Structure and sequence of the Drosophila zeste gene. EMBO J. 1987 Mar;6(3):791–799. doi: 10.1002/j.1460-2075.1987.tb04821.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pirrotta V., Rastelli L. White gene expression, repressive chromatin domains and homeotic gene regulation in Drosophila. Bioessays. 1994 Aug;16(8):549–556. doi: 10.1002/bies.950160808. [DOI] [PubMed] [Google Scholar]
  35. Pirrotta V. The genetics and molecular biology of zeste in Drosophila melanogaster. Adv Genet. 1991;29:301–348. doi: 10.1016/s0065-2660(08)60110-8. [DOI] [PubMed] [Google Scholar]
  36. Qian S., Varjavand B., Pirrotta V. Molecular analysis of the zeste-white interaction reveals a promoter-proximal element essential for distant enhancer-promoter communication. Genetics. 1992 May;131(1):79–90. doi: 10.1093/genetics/131.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Reuter G., Gausz J., Gyurkovics H., Friede B., Bang R., Spierer A., Hall L. M., Spierer P. Modifiers of position-effect variegation in the region from 86C to 88B of the Drosophila melanogaster third chromosome. Mol Gen Genet. 1987 Dec;210(3):429–436. doi: 10.1007/BF00327193. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Reuter G., Wolff I. Isolation of dominant suppressor mutations for position-effect variegation in Drosophila melanogaster. Mol Gen Genet. 1981;182(3):516–519. doi: 10.1007/BF00293947. [DOI] [PubMed] [Google Scholar]
  40. Rushlow C. A., Bender W., Chovnick A. Studies on the mechanism of heterochromatic position effect at the rosy locus of Drosophila melanogaster. Genetics. 1984 Nov;108(3):603–615. doi: 10.1093/genetics/108.3.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sinclair D. A., Ruddell A. A., Brock J. K., Clegg N. J., Lloyd V. K., Grigliatti T. A. A cytogenetic and genetic characterization of a group of closely linked second chromosome mutations that suppress position-effect variegation in Drosophila melanogaster. Genetics. 1992 Feb;130(2):333–344. doi: 10.1093/genetics/130.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Tartof K. D., Hobbs C., Jones M. A structural basis for variegating position effects. Cell. 1984 Jul;37(3):869–878. doi: 10.1016/0092-8674(84)90422-7. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Wu C. T., Jones R. S., Lasko P. F., Gelbart W. M. Homeosis and the interaction of zeste and white in Drosophila. Mol Gen Genet. 1989 Sep;218(3):559–564. doi: 10.1007/BF00332424. [DOI] [PubMed] [Google Scholar]
  46. Wustmann G., Szidonya J., Taubert H., Reuter G. The genetics of position-effect variegation modifying loci in Drosophila melanogaster. Mol Gen Genet. 1989 Jun;217(2-3):520–527. doi: 10.1007/BF02464926. [DOI] [PubMed] [Google Scholar]

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