P element transposition in Drosophila melanogaster: an analysis of sister-chromatid pairs and the formation of intragenic secondary insertions during meiosis

Abstract

The gap-repair model proposes that P elements move via a conservative, "cut-and-paste" mechanism followed by double-strand gap repair, using either the sister chromatid or homolog as the repair template. We have tested this model by examining meiotic perturbations of an X-linked ry+ transposon during the meiotic cycle of males, employing the mei-S332 mutation, which induces high frequency equational nondisjunction. This system permits the capture of both sister-X chromatids in a single patroclinous daughter. In the presence of P-transposase, transpositions within the immediate proximity of the original site are quite frequent. These are readily detectable among the patroclinous daughters, thereby allowing the combined analysis of the transposed element, the donor site and the putative sister-strand template. Molecular analysis of 22 meiotic transposition events provide results that support the gap-repair model of P element transposition. Prior to this investigation, it was not known whether transposition events were exclusively or predominantly premeiotic. The results of our genetic analysis revealed that P elements mobilize at relatively high frequencies during meiosis. We estimated that approximately 4% of the dysgenic male gametes have transposon perturbations of meiotic origin; the proportion of gametes containing lesions of premeiotic origin was estimated at 32%.