Site specificity of mutations arising in dysgenic hybrids of Drosophila melanogaster.

Abstract

Mutations arising in dysgenic hybrids of Drosophila melanogaster were collected in the zeste-white region of the X chromosome. A preponderance of the mutations affected the zwl locus; many of these were associated with structural abnormalities including inversions, deficiencies, and insertions in the 3A3-4 region of the polytene chromosome map. The extreme sensitivity of the zwl locus to the mutator activity of dysgenic hybrids contrasted with the apparent insensitivity of the zw2 locus. Other loci in the zeste-white region were weakly sensitive to the mutator activity. Insertions of two and six bands were seen between bands 3A4 and 3A6 in the chromosomes of one of the zwl mutant stocks examined. Another insertion was detected at position 2F4-5 in a different stock. Many of the mutant chromosomes were evidently unstable, as judged by secondary breakage in other parts of the X chromosome. The cytogenetic data are consistent with the idea that mutations arising in dysgenic hybrids are caused by transposable elements which insert preferentially at certain sites on the chromosomes.Hybrid dysgenesis (HD) is a condition noted in the offspring of certain Drosophila strains (1-4). Its appearance is nonreciprocal, meaning that dysgenic hybrids are produced when males of a paternally contributing (P) strain are mated with females of a maternally contributing (M) strain but usually not when the reciprocal cross is performed. Dysgenic hybrids are characterized by high sterility, male recombination, segregation distortion, enhanced mutability, and chromosome breakage.We have studied the last two phenomena by analyzing a small region of the Drosophila X chromosome in which mutations from dysgenic hybrids (HD mutations) were collected. The region selected consists of 17 genes, demarcated by the gt (giant) locus on the left and the w (white) locus on the right. It is known as the zw (zeste-white) region, having been named for two of its loci which produce conspicuous eye color mutations (5). Each of the 17 genes in this region appears to correspond to a single band in the polytene chromosomes of the salivary gland cells (refs. 5-7 Cytogenetic Analysis. Preliminary complementation tests were performed with each zw mutation shortly after it was identified. A series of tester stocks, including partial deficiencies for the zw region, were available for this purpose. The definitive complementation analysis of each zw mutation was performed later, in conjunction with the detailed cytological analysis of each zw mutant chromosome. The procedure was to mate a single zw-l/Bsw +y+ Y(or zw-visible/Y) male from each mutant line to y59bz w'ct6ffemales and also to DB/FM6, 1(1 )69aAbbreviation: HD, hybrid dysgenesis. 6042The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact.

The fitness consequences ofPelement insertion inDrosophila melanogaster

“…However, a second, and probably more important, mutational phenomenon occurs when P elements already in place undergo rearrangement and local deletion, usually with drastic fitness consequences. These events are known to occur at enormously elevated rates in dysgenic crosses (Engels, 1979;Berg, Engels & Kreber, 1980;Simmons & Lim, 1980;Simmons et al 1984 a, b). Existing elements become the foci of localized mutational lesions generating site (or locus) specific effects.…”

“…Each X chromosome was derived from a different dysgenic male in the first generation. This avoids the repeated sampling of identical insertions recovered as premeiotic germ line events (Simmons & Lim, 1980;Engels & Preston, 1984), and thereby ensures independence of observations.…”

Genetic factors that affect rates of spontaneous mutation and chromosome aberrations in <i>Drosophila melanogaster</i>

“…The genetic changes induced by hybrid dysgenesis do not occur at random on the chromosome. There is a degree of site pre ference both for gene mutations (G reen, 1978) and for chromosome breakage (Bi ro et al, 1980;Simmons and L im , 1980). In addition, many of the gene mutations are unstable (G olubovsky et al, 1977;G reen, 1977;Engels, 1979a;G olubow sky, 1980), and the instability is under chromosomalcytoplasmic control (E ngels, 19796).…”

Restriction of P-element insertions at the Notch locus of Drosophila melanogaster.

“…As mentioned earlier, P-element insertion mutations occur with quite different frequencies at different genetic loci (4,5,7,18), so there may be two levels of insertion specificity: (i) choice of a target gene and (ii) choice of a position within an affected gene. In trying to imagine how these specificities are achieved at Notch, rudimentary, and RpII215, it may be important to consider when the transposon and its targets are active during development.…”