Abstract
The germlines of metazoans contain transposable elements (TEs) causing genetic instability and affecting fitness. To protect the germline from TE activity, gonads of metazoans produce TE-derived PIWI-interacting RNAs (piRNAs) that silence TE expression. In Drosophila, our understanding of piRNA biogenesis is mainly based on studies of the Drosophila melanogaster female germline. However, it is not known whether piRNA functions are also important in the male germline or whether and how piRNAs are affected by the global genomic context. To address these questions, we compared genome sequences, transcriptomes, and small RNA libraries extracted from entire testes and ovaries of two sister species: D. melanogaster and Drosophila simulans. We found that most TE-derived piRNAs were produced in ovaries and that piRNA pathway genes were strongly overexpressed in ovaries compared with testes, indicating that the silencing of TEs by the piRNA pathway mainly took place in the female germline. To study the relationship between host piRNAs and TE landscape, we analyzed TE genomic features and how they correlate with piRNA production in the two species. In D. melanogaster, we found that TE-derived piRNAs target recently active TEs. In contrast, although Drosophila simulans TEs do not display any features of recent activity, the host still intensively produced silencing piRNAs targeting old TE relics. Together, our results show that the piRNA silencing response mainly takes place in Drosophila ovaries and indicate that the host piRNA response is implemented following a burst of TE activity and could persist long after the extinction of active TE families.
Highlights
In sexually reproducing organisms, germline cells transmit genetic information from generation to generation
The PIWI-interacting RNAs (piRNAs) clusters were analyzed according to their germline expression. (E, I) Stand for piRNA clusters expressed in both testes and ovaries, (F, J) for piRNA clusters exclusively expressed in ovaries, and (G, K) for piRNA clusters exclusively expressed in testes
We found that the tempo and the dynamics of Transposable elements (TEs) invasion are clearly different between two closely related species of Drosophila: D. simulans have experienced ancient waves of TE invasion, whereas D. melanogaster still undergo recent TE bursts
Summary
Germline cells transmit genetic information from generation to generation. The maintenance of genome integrity in these cells is crucial in ensuring the progeny an optimal fitness. Transposable elements (TEs) are selfish genetic elements that have the ability to insert at any genomic location, constituting an important source of genetic variability and instability within the germline. The host can take advantage of beneficial TE insertions to establish new genetic functions (Jangam et al 2017). Evolutionary trajectories of TEs rely on negative selective pressures acting against deleterious insertions (Petrov et al 2003; Le Rouzic and Deceliere 2005; Dolgin and Charlesworth 2008). The germline deploys important genetic and epigenetic resources to silence TEs and limit their harmful consequences on host genomes
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