Direct correlation between a chromosome puff and the synthesis of a larval saliva protein in Drosophila melanogaster

142

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...

Section: Resultsmentioning

confidence: 99%

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

Jack

Judd

1979

142

“…In addition to being endoreplicated, homologues are aligned and paired in exact register. While the physiological significance of somatic chromosome synapsis remains unclear, a few instances of synapsisdependent phenotypes have been reported in Drosophila melanogaster (1)(2)(3)(4). "Transvection" is the term coined by Lewis (1) to describe the phenomenon of synapsis-dependent allelic complementation at the bithorax locus.…”

mentioning

confidence: 99%

Synapsis-dependent allelic complementation at the decapentaplegic gene complex in Drosophila melanogaster.

Gelbart¹

1982

Allelic complementation at the decapentaplegic gene complex (dpp: 2-4.0, cytogenetic location: polytene chromosome bands 22F1-3) of Drosophila melanogaster frequently occurs between site mutations. Two specific instances of allelic complementation are shown to be dependent upon normal somatic chromosome synapsis of homologous dpp genes. Numerous strains have been identified that bear lesions that disrupt allelic complementation when heterozygous with structurally normal chromosomes; each ofthese 57 strains contains a gross chromosomal rearrangement with a break on chromosome 2. The properties of the rearrangements carried by 50 of these strains are consonant with the idea that their effects are due to a disruption of somatic chromosome synapsis in the dpp region of chromosome arm 2L. In double heterozygotes of simple two-break rearrangements, allelic complementation is restored (presumably through the restoration of structural homozygosity). The types of rearrangements that disrupt complementation have properties very similar to those of rearrangements that disrupt the transvection effect at bithorax [Lewis, E. B. (1954) Am. Nat 88, 225-239]. The existence of synapsis-dependent allelic complementation is a demonstration of the physiological importance ofnuclear organization in gene expression.Somatic chromosome synapsis between homologues is well known in dipteran insects. The most obvious examples of this phenomenon are the polytene chromosomes found in the nuclei of a variety of specialized cell types. In addition to being endoreplicated, homologues are aligned and paired in exact register. While the physiological significance of somatic chromosome synapsis remains unclear, a few instances of synapsisdependent phenotypes have been reported in Drosophila melanogaster (1-4). "Transvection" is the term coined by Lewis (1) to describe the phenomenon of synapsis-dependent allelic complementation at the bithorax locus. Allelic complementation occurs in genotypes in which somatic chromosome pairing ofthe bithorax alleles is unhindered, whereas complementation is not found in genotypes in which chromosomal rearrangement heterozygosity interferes with such pairing. Synapsis-dependent gene expression also has been demonstrated in the zeste-white system (2), but it appears not to involve allelic complementation.During investigation of the decapentaplegic gene complex in D. melanogaster, allelic complementation between site mutations was noted. In this report, allelic complementation at decapentaplegic is demonstrated to be a transvection effect. As in the bithorax system, structural heterozygosity disrupts complementation. The cytogenetic properties of rearrangements disrupting complementation at decapentaplegic and at bithorax are very similar. A molecular model oftransvection is considered. MATERIALS AND METHODSMutations. With the exception ofthe decapentaplegic alleles described in the text, all mutations and balancer chromosomes are described in Lindsley and Grell (5).Culture Conditions. Flies were culture...

“…This dependence on the ability of chromosomes to pair in order to produce a phenotype is known as transvection and has been observed for other loci (31,(34)(35)(36)(37). The results presented here show that there is no change in the size and no large change (if any) in the abundance of the white transcript we have identified when wild-type flies was also analyzed (rightmost four lanes) as a control for the proportionality of autoradiographic signal to RNA concentration.…”

Section: Results and Discussion Structure Of The Wild-type White Locumentioning

confidence: 81%

Transcription of the white locus in Drosophila melanogaster

O’Hare

Levis

Rubin

1983

Genetic studies of the white locus have shown that it has a distal region where structural mutations occur and a proximal region where regulatory mutations occur. To better understand the molecular basis of this genetic organization we have analyzed white locus transcription. A 2.7-kilobase transcript comprising 0.0005% of poly(A)-RNA was detected in RNA prepared from pupae or adults. The structure of this transcript helps clarify some unusual genetic properties of the locus. There is a small 5' exon separated from the majority of the sequences found in the mature RNA by an intron of "2.8 kilobases. This 5' exon is from the proximal region of the locus, whereas the main body of the RNA maps to the distal region. The mutationally silent region between the proximal and distal regions corresponds to the large intron. We have identified the family and determined the exact location of a number of transposable element insertions within the locus. These results show that transposable element insertions within introns can be without phenotypic effect. We have also investigated the effect on the white transcript of the zeste mutation, which represses white locus expression as judged by eye color phenotype. The RNA was unchanged in size or abundance in poly(A)-RNA from adult flies. This demonstrates that the zeste-white interaction does not occur by simply repressing transcription of the white locus in all tissues.The white locus of Drosophila melanogaster has long been the subject of intensive genetic studies (for a review see ref. 1). Mutations in white affect the degree of pigmentation of the adult eye, ocelli, and testis sheath and of the larval Malpighian tubules (2). The brick-red eye color of wild-type flies is due to the accumulation of both ommochrome (brown) and pteridine (red and yellow) pigments. Some white mutations, including deletions for the entire locus, result in the lack of all pigmentation, whereas other mutations reduce the amounts of one or both classes of pigment.A number of different sites where mutations occur within the white locus have been separated by recombination and ordered on a genetic map of the locus (3, 4). These sites have been divided into distal and proximal regions with respect to the centromere, where the distal region is defined as including the site of the white-apricot (wa) mutation and those mutations mapping distal to it (3). The DNA sequences for the wild-type locus (5, 6) and a number of mutants associated with insertions (6-11) have been isolated and characterized. The physical map constructed from these studies correlates well with the genetic map and shows in addition that the genetically defined distal and proximal regions are physically separated by some 3 kilobases (kb) in which no mutations map.Genetic studies have led to the suggestion that the distal region contains structural sequences, whereas the proximal domain contains regulatory sequences (11-14). Most null mutations (3, 15, 16) and apparent point mutations (11) map to the distal region. A series of m...