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Nucleolus organizer-suppressed position-effect variegation in Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Janice B. Spofford*
Affiliation:
Department of Ecology and Evolution, University of Chicago, 1103 E. 57th St, Chicago, Illinois 60637, USA
Rob DeSalle
Affiliation:
Department of Ecology and Evolution, University of Chicago, 1103 E. 57th St, Chicago, Illinois 60637, USA
*
* Corresponding author.
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The white locus is inactivated in a cell-by-cell variegated pattern when juxtaposed with the proximal or distal parts of the nucleolus organizer region (NO) by X chromosome inversion. Recombinants for two such inversions, wm51b and wm4, were obtained and randomized for genetic background. White locus activity was much higher in the wm4 recombinant duplicated for most of the NO and much lower in the wm51b recombinant deficient for it. Although there may be other molecular differences between the heterochromatic regions of the recombinants, the most obvious is the dosage of NO. Suppression of a NO region-evoked variegated phenotype by additional NO doses is discussed in relation to four different classes of models for position-effect variegation (PEV): chromatin structure, nuclear geometry, incomplete transposition of mobile elements, and heterochromatin promoter-driven transcription. A corollary of the structural model is functional subdivision of heterochromatin, which would enable the use of PEV as a tool for its study.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

References

Appels, R. & Hilliker, A.J. (1982). The cytogenetic boundaries of the rDNA region within heterochromatin of the X chromosome of Drosophila melanogaster and their relation to male meiotic pairing sites. Genetical Research 39, 149156.CrossRefGoogle ScholarPubMed
Baker, W. K. (1968). Position effect variegation. Advances in Genetics 14, 133169.CrossRefGoogle ScholarPubMed
Baker, W. K. & Spofford, J. B. (1959). Heterochromatic control of position effect variegation in Drosophila. University of Texas Publication No. 5914, 135154.Google Scholar
Berleth, T., Burri, M., Thoma, G., Bopp, D., Richstein, S., Frigerio, G., Noll, M. & Nüsslein-Volhard, C. (1988). EMBO Journal 7, 17491756.CrossRefGoogle Scholar
Bingham, P. M. & Zachar, Z. (1985). Evidence that two mutations, wDzL and zl, affecting synapsis-dependent genetic behavior of white, are transcription regulatory mutations. Cell 40, 819825.CrossRefGoogle Scholar
Brutlag, D. L. (1980). Molecular arrangement and evolution of heterochromatic DNA. Annual Review of Genetics 14, 121144.CrossRefGoogle ScholarPubMed
Coen, E. S., Thoday, J. M. & Dover, G. (1982). Rate of turnover of structural variants in the rDNA gene family of Drosophila melanogaster. Nature 295, 564568.CrossRefGoogle ScholarPubMed
Cooper, K. W. (1959). Cytogenetic analysis of major heterochromatic elements (especially Xh and Y) in Drosophila melanogaster, and the theory of ‘heterochromatin’. Chromosoma (Berlin) 10, 535588.CrossRefGoogle ScholarPubMed
deCicco, D. V. & Glover, D. M. (1983). Amplification of rDNA and Type I sequences in Drosophila males deficient in rDNA. Cell 32, 12171225.CrossRefGoogle Scholar
Devlin, R. H., Bingham, B. & Wakimoto, B. T. (1990). The organization and expression of the light gene, a heterochromatic gene of Drosophila melanogaster. Genetics 125, 129140.CrossRefGoogle ScholarPubMed
Dimitri, P. & Pisano, C. (1989). Position effect variegation in Drosophila melanogaster: relationship between suppression effect and the amount of Y chromosome. Genetics 122, 793800.CrossRefGoogle ScholarPubMed
Donnelly, R. J. & Kiefer, B. I. (1986). DNA sequence adjacent to and specific for the 1·672 g/cm3 satellite DNA in the Drosophila genome. Proceedings of the National Academy of Sciences USA 83, 71727176.CrossRefGoogle ScholarPubMed
Eissenberg, J. (1989). Position effect variegation in Drosophila: towards a genetics of chromatin assembly. BioEssays 11, 1417.CrossRefGoogle ScholarPubMed
Endow, S. A. & Glover, D. M. (1979). Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell 17, 597605.CrossRefGoogle ScholarPubMed
Fjose, A., Polito, L. C., Weber, U. K. & Gehring, W. J. (1984). Developmental expression of the white locus of Drosophila melanogaster. EMBO Journal 3, 20872094.CrossRefGoogle ScholarPubMed
Foe, V. E. & Alberts, B. M. (1985). Reversible chromosome condensation induced in Drosophila embryos by anoxia: visualization of interphase nuclear organization. Journal of Cell Biology 100, 16231636.CrossRefGoogle ScholarPubMed
Frankham, R. (1988). Molecular hypotheses for position-effect variegation: anti-sense transcription and promoter occlusion. Journal of Theoretical Biology 135, 85107.CrossRefGoogle ScholarPubMed
Gatti, M., Tanzarella, C. & Olivieri, B. (1974). Analysis of the chromosome aberrations induced by X-rays in somatic cells of Drosophila melanogaster. Genetics 11, 701719.CrossRefGoogle Scholar
Golic, K. G. & Lindquist, S. (1989). The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499509.CrossRefGoogle ScholarPubMed
Goodpasture, C. & Bloom, S. E. (1975). Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma (Berlin) 53, 3750.CrossRefGoogle ScholarPubMed
Grell, R. (1970). The time of initiation of segregational pairing between nonhomologues in Drosophila melanogaster: a re-examination of wm4. Genetics 64, 337365.CrossRefGoogle Scholar
Hannah, A. (1951). Localization and function of heterochromatin in Drosophila melanogaster. Advances in Genetics 4, 87125.CrossRefGoogle ScholarPubMed
Hilliker, A. J. (1976). Genetic analysis of the centromeric heterochromatin of chromosome 2 of Drosophila melanogaster: deficiency mapping of EMS-induced lethal complementation groups. Genetics 83, 765782.CrossRefGoogle ScholarPubMed
Hilliker, A.J. & Appels, R. (1982). Pleiotropic effects associated with the deletion of heterochromatin surrounding rDNA on the X chromosome of Drosophila. Chromosoma (Berlin) 86, 469490.CrossRefGoogle ScholarPubMed
Hilliker, A. J., Appels, R. & Schalet, A. (1980). The genetic analysis of Drosophila melanogaster heterochromatin. Cell 21, 607619.CrossRefGoogle Scholar
Holmquist, G. (1975). Hoechst 33258 fluorescent staining of Drosophila chromosomes. Chromosoma (Berlin) 49, 333356.CrossRefGoogle ScholarPubMed
Hubby, J. L. & Lewontin, R. C. (1966). A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. Genetics 54, 577594.CrossRefGoogle Scholar
Indik, Z. K. & Tartof, K. D. (1980). Long spacers among ribosomal genes of Drosophila melanogaster. Nature 284, 477479.CrossRefGoogle ScholarPubMed
John, B. (1988). The biology of heterochromatin. In Heterochromatin (ed. Verma, R. S.), pp. 1147. Cambridge: Cambridge University Press.Google Scholar
Karpen, G. H. (1987). The relationship between organization and function of ribosomal genes in Drosophila melanogaster. Ph.D. dissertation, University of Washington, Seattle, Washington.Google Scholar
Karpen, G. H., Schaefer, J. E. & Laird, C. D. (1988). A Drosophila rDNA gene located in euchromatin is active in transcription and nucleolus formation. Genes and Development 2, 17451763.CrossRefGoogle ScholarPubMed
Karr, T. L. & Alberts, B. M. (1986). Organization of the cytoskeleton in early Drosophila embryos. Journal of Cell Biology 102, 14941509.CrossRefGoogle ScholarPubMed
Khesin, R. B. & Leibovitch, B. A. (1978). Influence of deficiency of the histone gene-containing 38B1–40 region on X-chromosome template activity and the white gene position effect variegation in Drosophila melanogaster. Molecular and General Genetics 162, 323328.CrossRefGoogle Scholar
Koliantz, G. & Hartmann-Goldstein, I. (1984 a). Modification of gene suppression in Drosophila melanogaster by sex chromosomes. 3. Heterochromatisation associated with the wm4 phenotype. Heredity 53, 215222.CrossRefGoogle Scholar
Koliantz, G. & Hartmann-Golstein, I. (1984 b). Modification of gene suppression in Drosophila melanogaster by sex chromosomes. II. Variegation in eyes of wm4 males. Heredity 52, 203213.CrossRefGoogle Scholar
Lefevre, G. Jr (1976). A photographic representation and interpretation of the polytene chromosomes of Drosophila melanogaster salivary glands. In The Genetics and Biology of Drosophila, vol. 1a (ed. Ashburner, M. and Novitski, E.), pp. 3166. London: Academic Press.Google Scholar
Lewis, E. B. (1950). The phenomenon of position effect. Advances in Genetics 3, 73115.CrossRefGoogle ScholarPubMed
Lifschytz, E. & Hareven, D. (1982). Heterochromatin markers: arrangement of obligatory heterochromatin, histone genes, and multisite gene families in the interphase nucleus of Drosophila melanogaster. Chromosoma (Berlin) 86, 443455.CrossRefGoogle Scholar
Lindsley, D. L. & Grell, E. H. (1968). Genetic variations of Drosophila melanogaster. Carnegie Institute of Washington, Publ. No. 627.Google Scholar
Locke, J., Kotarski, M. A. & Tartof, K. D. (1988). Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect. Genetics 120, 181198.CrossRefGoogle Scholar
Lohe, A. & Roberts, P. (1988). Evolution of satellite DNA sequences in Drosophila. In Heterochromatin (ed. Varma, R. S.), pp. 148186. Cambridge: Cambridge University Press.Google Scholar
MacDonald, P. M. & Struhl, G. (1988). Cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos. Nature 336, 595598.CrossRefGoogle ScholarPubMed
McElwain, M. C. (1986). The absence of somatic effects of P–M hybrid dysgenesis in Drosophila melanogaster. Genetics 113, 897918.CrossRefGoogle ScholarPubMed
Merriam, J. R. (1967). The initiation of nonhomologous chromosome pairing before exchange in female Drosophila melanogaster. Genetics 57, 409425.CrossRefGoogle ScholarPubMed
Miklos, G. L. G, Healy, M. J., Pain, P., Howells, A. J. & Russell, R. J. (1984). Molecular and genetic studies on the euchromatin-heterochromatin transition region of the X chromosome of Drosophila melanogaster. I. A cloned entry point near to the uncoordinated (unc) locus. Chromosoma (Berlin) 89, 218227.CrossRefGoogle Scholar
Miklos, G. L. G., Yamomoto, M.-T., Davies, J. & Pirrotta, V. (1988). Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome 4 and the β-heterochromatin of Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 85, 20512055.CrossRefGoogle ScholarPubMed
Moore, G. D., Procunier, J. D., Cross, D. P. & Grigliatti, T. A. (1983). Histone gene multiplicity and position-effect variegation in Drosophila. Genetics 105, 327344.CrossRefGoogle ScholarPubMed
Mottus, R., Reeves, R. & Grigliatti, T. A. (1980). Butyrate suppression of position-effect variegation in Drosophila melanogaster. Molecular and General Genetics 178, 465469.Google ScholarPubMed
Phillips, J. P. & Forrest, H. S. (1980). Ommochromes and pteridines. In The Genetics and Biology of Drosophila, vol. 2d (ed. Ashburner, M. and Wright, T. R. F.), pp. 541623. London: Academic Press.Google Scholar
Pimpinelli, S., Sullivan, W., Prout, M. & Sandler, L. (1985). On biological functions mapping to the heterochromatin of Drosophila melanogaster. Genetics 109, 701724.CrossRefGoogle Scholar
Prakash, S., Lewontin, R. C. & Hubby, J. L. (1969). A molecular approach to the study of genic heterozygosity in natural populations. IV. Patterns of genie variation in central, marginal and isolated populations of Drosophila pseudoobscura. Genetics 61, 841858.CrossRefGoogle Scholar
Procunier, J. D. & Tartof, K. D. (1978). A genetic locus having trans and contiguous cis functions that control the disproportionate replication of ribosomal RNA genes in Drosophila melanogaster. Genetics 88, 6779.CrossRefGoogle ScholarPubMed
Ready, D. F., Hanson, T. E. & Benzer, S. (1976). Development of the Drosophila retina, a neuro-crystalline lattice. Developmental Biology 53, 217240.CrossRefGoogle ScholarPubMed
Reuter, G., Hoffman, H.-J. & Wolff, I. (1983). Genetic study of position-effect variegation in Drosophila melanogaster: In(1)wm4 as a standard rearrangement for the isolation and characterization of suppressor and enhancer mutants. Biologisches Zentralblatt 102, 281298.Google Scholar
Schalet, A. & Lefevre, G. Jr (1976). The proximal region of the X chromosome. In The Genetics and Biology of Drosophila, vol. 1b (ed. Ashburner, M. and Novitski, E.), pp. 847902. London: Academic Press.Google Scholar
Shapiro, J. A. (1979). Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements. Proceedings of the National Academy of Sciences, USA 76, 19331937.CrossRefGoogle ScholarPubMed
Sharp, Z. D., Gandhi, V. V. & Procunier, J. D. (1983). X chromosome nucleus organizer mutants which alter major Type I repeat multiplicity in Drosophila melanogaster. Molecular and General Genetics 190, 438443.CrossRefGoogle ScholarPubMed
Sinclair, D. A. R., Mottus, R. C. & Grigliatti, T. A. (1983). Genes which suppress position effect variegation in Drosophila melanogaster are clustered. Molecular and General Genetics 191, 326333.CrossRefGoogle Scholar
Snedecor, G. W. & Cochran, W. G. (1967). Statistical Methods, 6th edn.Ames, Iowa: Iowa State University Press.Google Scholar
Spofford, J. B. (1967). Single-locus modification of position effect variegation in Drosophila melanogaster. I. White variegation. Genetics 57, 751766.CrossRefGoogle ScholarPubMed
Spofford, J. B. (1969). Single-locus modification of position effect variegation in Drosophila melanogaster. II. Region 3C loci. Genetics 62, 555571.CrossRefGoogle ScholarPubMed
Spofford, J. B. (1976). Position-effect variegation in Drosophila. In The Genetics and Biology of Drosophila, vol. 1c (ed. Ashburner, M. and Novitski, E.), pp. 9551018. London: Academic Press.Google Scholar
Spofford, J. B. (1982). Allopurinol inhibits variegation. Drosophila Information Service 58, 141.Google Scholar
Spofford, J. B. & DeSalle, E. (1978). In(1)wm4 is deficient for heterochromatin distal to NOR. Drosophila Information Service 53, 204.Google Scholar
Stellar, H. & Pirrotta, V. (1985). Expression of the Drosophila white gene under the control of the hsp70 heat shock promoter. EMBO Journal 4, 37653772.CrossRefGoogle Scholar
Szauter, P. (1984). An analysis of regional constraints on exchange in Drosophila melanogaster using recombination-defective meiotic mutants. Genetics 106, 4571.CrossRefGoogle ScholarPubMed
Tartof, K. D., Hobbs, C. & Jones, M. (1984). A structural basis for variegating position effects. Cell 371, 869878.CrossRefGoogle Scholar
Wellauer, P. K., Dawid, I. B. & Tartof, K. D. (1978). X and Y chromosomal ribosomal DNA of Drosophila: comparison of spacers and insertions. Cell 14, 269278.CrossRefGoogle ScholarPubMed
Williams, S. M., Robbins, L. G., Cluster, P. D., Allard, R. W. & Strobeck, C. (1990). Superstructure of the Drosophila ribosomal gene family. Proceedings of the National Academy of Sciences, USA (in the press).Google ScholarPubMed
Yamamoto, M. & Miklos, G. L. G. (1978). Genetic studies on heterochromatin in Drosophila melanogaster and their implications for the functions of satellite DNA. Chromosoma (Berlin) 66, 7198.CrossRefGoogle ScholarPubMed
Yoon, J. S., Richardson, R. H. & Wheeler, M. R. (1973). A technique for improving salivary preparations. Experientia 29, 639641.CrossRefGoogle ScholarPubMed