Experimentally evolvingDrosophila erectapopulations may fail to establish an effective piRNA-based host defense against invadingP-elements

Abstract

To prevent the spread of transposable elements (TEs) hosts have developed sophisticated defense mechanisms. In mammals and invertebrates, a major defense mechanism operates through PIWI-interacting RNAs (piRNAs). To investigate the establishment of the host defence we introduced theP-element, one of the most widely studied eukaryotic transposons, into naive lines ofDrosophila erecta. We monitored the invasion in 3 replicates for more than 50 generations by sequencing the genomic DNA (using short and long reads), the small RNAs and the transcriptome at regular intervals. A piRNA-based host defense was rapidly established in two replicates (R1, R4) but not in a third (R2), whereP-elementcopy numbers kept increasing for over 50 generations. We found that the ping-pong cycle could not be activated in R2 although the ping-pong cycle is fully-functional against other TEs. Furthermore, R2 had both insertions in piRNA clusters and siRNAs, suggesting that neither of them is sufficient to trigger the host defense. Our work shows that control of an invading TE requires activation of ping-pong cycle and that this activation is a stochastic event that may fail in some populations leading to a proliferation of TEs that ultimately threaten the integrity of the host genome.

Transposon and Transgene Tribulations in Mosquitoes: A Perspective of piRNA Proportions

“…Earlier studies of a transposon from Drosophila virilis called Penelope was transplanted to D. melanogaster to create dysgenic Drosophila crosses, and Penelope also first initiated progeny flies to generate siRNAs, but eventually piRNAs were utilized by recovering fly progeny to complete Penelope silencing [132,194]. More recently, the Kofler lab put mobile P-elements in Drosophila simulans populations to also trigger gonadal dysgenesis, but two populations would then rebound their fertility by first generating siRNAs against the P-element that in later generations become piRNAs that enforce stable transposon silencing [195]. However, a third population in Kofler study at first initiated a strong siRNA response, but then there was still a failure to establish a stable piRNA response, suggesting that siRNA generation is not a guarantee for an eventual piRNA response.…”