Allelic pairing and gene regulation: A model for the zeste—white interaction in Drosophila melanogaster

Abstract

Data are presented that indicate that the z locus of Drosophila melanogaster represses w locus activity, but the repression is effective only on paired or physically adjacent w loci. Various mutant alleles of z and w were combined in a series of different doses to determine the effect of dosage and physical position in the nucleus on gene expression. In z/z individuals, paired white alleles fail to be expressed, while unpaired alleles are expressed normally. The results are discussed in terms of a model postulating that the z gene product represses the transcription of wr by complexing with an RNA produced by part of the white locus itself. In order to be effective in repression, there must be two w+ genes producing the RNA in a limited volume in the nucleus. Such a model necessarily imposes a specific architecture on the chromatin of interphase nuclei.Examples of regulatory interactions between loci in eukaryotes are rare; communication between two alleles at a single locus is even less well documented. We present evidence that a particular locus of Drosophila melanogaster functions as a repressor of another locus. Repression is generally apparent, however, only if two alleles of the repressed locus are physically adjacent or paired.Gans (1) discovered the mutation zeste (z; 1-1.0) that produces yellow eye color in females but is wild type in males. She showed that the expression of the zeste phenotype in the females is due to the presence of two wild-type alleles of the white locus (w; 1-1.5). Certain duplications of w+ allow zeste phenotype expression in males. On the other hand, females heterozygous for a white locus deletion (z w + /z w -) are wild type in eye color. Some mutant alleles of w act in the same fashion as a deletion of the locus (1). Such white locus alleles were determined by Green (2) to map in the proximal part of the white locus (here designated as wPrX). Those alleles of white located in the distal portion of the locus (wdst) allow expression of zeste just as w + does. In fact, all the mutations that appear to upset regulatory function of the white locus map in WPrx. Pattern mutants that produce mosaics of pigmented and nonpigmented facets are located in WPrX, and all mutants in the region fail to show dosage compensation, which is characteristic of w+. A tandem duplication of only the wPorx portion of the locus behaves with respect to z as two doses of w+ (3). On the basis of these and some other distinguishing properties, Judd (4) has suggested that WPrX is involved in the regulation of the white locus while wdst contains the structural sequence.Historically the zeste-white interaction has been stated in terms of white locus deletions and mutants in wPrx acting as dominant suppressors of zeste. We believe this is not an accurate description of the system, and we will here describe the interaction from the point of view of repression of w+ by z. The reduction in pigmentation in z w + /z w + females results from the continued repression of w+ even when the gene should be active. Th...

Effect of transvection on the expression of the Notch locus in Drosophila melanogaster

“…In the bithorax locus transvection induced an enhancement of the mutant phenotype of alleles in the trans position, and was thought to be due to the prevention of the opposition of homologous alleles (Lewis, 1954;Gelbart, 1982). In addition to the effect at the bithorax complex (BX-C; map location 3-58.8) transvection has been observed in the decapentaplegic complex (DPP-C; 2-4.0) (Gelbart, 1982) and at the white locus (w; 1-1.5) (Green, 1967;Gelbart, 1971Gelbart, , 1982Jack and Judd, 1979;Gelbart and Wu, 1982;Zachar et a!., 1985;Smolik-Utlaut and Gelbart, 1987). Synapsis-dependent trans regulation of gene activity has also been suggested for the salivary gland glue protein 4 (Sgs-4) gene by Korge (1981).…”

Molecular Genetic Analysis of Suppressor 2 of zeste Identifies Key Functional Domains

“…This allele was isolated as a gain-of-function (g-o-f) dominant suppressor of an allele of the X-linked zeste gene, called z 1 , which represses expression from the white 1 (w 1 ) eye-color gene in a manner that is sensitive to whether the w 1 gene is paired with another w 1 gene ( Jack and Judd 1979; reviewed by Wu and Goldberg 1989;Pirrotta 1991;Kassis 2002). For example, the eye color of z 1 w 1 / z 1 w 1 females is yellow instead of wild-type red because the somatic homolog pairing that occurs in Drosophila (Stevens 1907(Stevens , 1908Metz 1916;Lewis 1954 (Wu 1984;Adler et al 1989;Wu and Howe 1995).…”

Effects of Chromosomal Rearrangements on Transvection at theyellowGene ofDrosophila melanogaster

“…For example, studies of transvection at Ubx (Lewis 1954), dpp (Gelbart 1982), eya (Leiserson et al 1994), and Abd-B (Sipos et al 1998) showed that 0.2-0.8% and possibly more of chromosomes that had been exposed to 4000-4500 rad of X rays carried a transvection-disrupting rearrangement. In contrast, transvection at white (w) ( Jack and Judd 1979;Smolik-Utlaut and Gelbart 1987;Gubb et al 1997) and a second example of transvection at Abd-B (Hendrickson and Sakonju 1995;Hopmann et al 1995) are associated with small critical regions; only chromosomal rearrangements that break very close to white or Abd-B are able to disrupt transvection.…”

“…org), or those that disrupt transvection at both loci. Transvection at white can be observed in a zeste 1 (z 1 ) background, which does not affect unpaired white genes but causes paired white genes to be repressed, producing flies with eyes that are yellow in color instead of wild-type red ( Jack and Judd 1979;reviewed by Pirrotta 1991). Interestingly, mutations at zeste have also been shown to disrupt transvection-associated phenotypes at dpp (Gelbart and Wu 1982), eya (Leiserson et al 1994), and Ubx (Lewis 1954).…”