Transvection at the vestigial locus of Drosophila melanogaster

Abstract

Transvection is a phenomenon wherein gene expression is effected by the interaction of alleles in trans and often results in partial complementation between mutant alleles. Transvection is dependent upon somatic pairing between homologous chromosome regions and is a form of interallelic complementation that does not occur at the polypeptide level. In this study we demonstrated that transvection could occur at the vestigial (vg) locus by revealing that partial complementation between two vg mutant alleles could be disrupted by changing the genomic location of the alleles through chromosome rearrangement. If chromosome rearrangements affect transvection by disrupting somatic pairing, then combining chromosome rearrangements that restore somatic pairing should restore transvection. We were able to restore partial complementation in numerous rearrangement trans-heterozygotes, thus providing substantial evidence that the observed complementation at vg results from a transvection effect. Cytological analyses revealed this transvection effect to have a large proximal critical region, a feature common to other transvection effects. In the Drosophila interphase nucleus, paired chromosome arms are separated into distinct, nonoverlapping domains. We propose that if the relative position of each arm in the nucleus is determined by the centromere as a relic of chromosome positions after the last mitotic division, then a locus will be displaced to a different territory of the interphase nucleus relative to its nonrearranged homolog by any rearrangement that links that locus to a different centromere. This physical displacement in the nucleus hinders transvection by disrupting the somatic pairing of homologous chromosomes and gives rise to proximal critical regions.

Figure 1.—

Mutagenesis screens used to create complementation-disrupting derivatives. (A) The screen to recover noncomplementing derivatives of vg^83b27. (B) The screen to recover noncomplementing derivatives of vg¹. The screen to recover derivatives of vg^1-7b is identical to the one used for vg¹ except vg^1-7b males were irradiated in cross 1. In both screens * indicates an irradiated chromosome.

Figure 2.—

Partial complementation between vg^83b27 and vg¹. (A) A homozygous vg^83b27 female lacking wings and halteres (a wing score of 1). (B) A homozygous vg¹ female lacking halteres but having small, stumpy wings (a wing score of 2). (C) A typical vg^83b27/vg¹ trans-heterozygous female having halteres and long, blistered wings (a wing score of 3). The arrow points to a haltere.

Figure 3.—

Diagrams of haploid chromosome arrangements of wild-type chromosomes (top arrangement) and eight complementation-disrupting chromosome rearrangements. Chromosomes are labeled on the left. Ellipses represent centromeres, and hatched boxes represent centromeric heterochromatin. Hatches ascend to the right for second chromosome heterochromatin and ascend to the left for third chromosome heterochromatin. Chromosome arms are labeled on the wild-type chromosomes but they can also be distinguished as follows: 2L, thickly striped blue; 2R, solid blue; 3L, open with no color; 3R, thinly striped red. Chromosomes are drawn to scale. There is some uncertainty about the exact location of heterochromatic breakpoints.

Figure 4.—

Proposed somatic pairing for trans-heterozygote combinations of vg^83b27 derivatives and vg^1-7b derivatives that restore complementation. Chromosomes are labeled on the left. Solid horizontal lines separate the complementing pairs on the basis of the level of complementation restoration. Chromosomes are drawn in the Rabl orientation in instances where vg alleles are located on different chromosome arms. Chromosome arms can be distinguished by the description in the Figure 3 legend.

Figure 5.—

Representation of a reciprocal translocation (right) and wild-type chromosomes (left) showing how chromosome organization in the Drosophila interphase nucleus might contribute to proximal critical regions. If the relative position of each chromosome arm in the nucleus is determined by the centromere as a relic of chromosome positions after the last mitotic division, then locus A on the rearranged chromosome will be displaced to a different territory of the interphase nucleus relative to locus A on the nonrearranged homolog. This will affect the ability of the alleles of locus A to interact. Locus B will be unaffected by the rearrangement because the breakpoint occurred distal to the locus.