<i>Har-P</i>, a short <i>P</i>-element variant, weaponizes <i>P</i>-transposase to severely impair <i>Drosophila</i> development.

Abstract

Without transposon-silencing Piwi-interacting RNAs (piRNAs), transposition causes an ovarian atrophy syndrome in <i>Drosophila</i> called gonadal dysgenesis (GD). <i>Harwich</i> (<i>Har</i>) strains with <i>P</i>-elements cause severe GD in F1 daughters when <i>Har</i> fathers mate with mothers lacking <i>P</i>-element-piRNAs (i.e. <i>ISO1</i> strain). To address the mystery of why <i>Har</i> induces severe GD, we bred hybrid <i>Drosophila</i> with <i>Har</i> genomic fragments into the <i>ISO1</i> background to create <i>HISR-D or HISR-N</i> lines that still cause <u>D</u>ysgenesis or are <u>N</u>on-dysgenic, respectively. In these lines, we discovered a highly truncated <i>P</i>-element variant we named '<i>Har-P</i>' as the most frequent de novo insertion. Although <i>HISR-D</i> lines still contain full-length <i>P</i>-elements, <i>HISR-N</i> lines lost functional <i>P</i>-transposase but retained <i>Har-P</i>'s that when crossed back to <i>P</i>-transposase restores GD induction. Finally, we uncovered <i>P</i>-element-piRNA-directed repression on <i>Har-P's</i> transmitted paternally to suppress somatic transposition. The <i>Drosophila</i> short <i>Har-P's</i> and full-length <i>P</i>-elements relationship parallels the MITEs/DNA-transposase in plants and SINEs/LINEs in mammals.