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 defense, we introduced the P-element, one of the most widely studied eukaryotic transposons, into naive lines of Drosophila erecta. We monitored the invasion in three 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), in which P-element copy 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 the 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.

中文翻译：

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实验进化的直立果蝇种群可能无法建立有效的基于 piRNA 的宿主防御系统来抵御 P 元素的入侵

为了防止转座因子（TE）的传播，宿主已经开发出复杂的防御机制。在哺乳动物和无脊椎动物中，主要的防御机制是通过 PIWI 相互作用 RNA (piRNA) 发挥作用。为了研究宿主防御的建立，我们将P元件（研究最广泛的真核转座子之一）引入直立果蝇的幼稚系中。我们通过定期对基因组 DNA（使用短读长和长读长）、小 RNA 和转录组进行测序，监测了 50 多代的三个重复的入侵。基于 piRNA 的宿主防御在两次重复（R1、R4）中迅速建立，但在第三次重复（R2）中却没有建立，其中P元件拷贝数持续增加超过 50 代。我们发现乒乓循环在 R2 中无法激活，尽管乒乓循环对其他 TE 完全有效。此外，R2 在 piRNA 簇和 siRNA 中都有插入，表明它们都不足以触发宿主防御。我们的工作表明，控制入侵的 TE 需要激活乒乓循环，并且这种激活是一个随机事件，在某些群体中可能会失败，导致 TE 的增殖，最终威胁宿主基因组的完整性。