Flamenco plasticity tunes somatic piRNAs, rewiring host isoforms and opening a route to heritable transposon spread

Transposons drive genome innovation, yet how they evade somatic piRNA defenses, reach the germline, and rewire host genes with limited cost remains unclear. Using comparative long-read sequencing in Drosophila ovarian somatic cells (OSCs), we show that the LTR transposon Springer rewires gene expression by inserting into promoter-proximal introns at an AT-rich motif. Its 5' LTR initiates transcripts that splice into host exons, expanding isoform diversity without adding coding sequence. We catalog 72 Springer-driven isoforms, indicating broad mutagenic potential. In parallel, the Flamenco (Flam) uni-strand piRNA cluster undergoes structural remodeling that replaces antisense transposon fragments with forward-oriented copies, reshaping piRNA populations and eroding silencing of specific elements, including Springer. This relaxation of somatic repression creates conditions permissive for germ-cell entry, providing a plausible route to heritable genome change. Thus, Flam plasticity, contrasting with the relative stability of dual-strand clusters, mechanistically links transposon activity to genome rewiring and evolutionary innovation.