Environmentally-induced epigenetic conversion of a piRNA cluster.

Transposable element (TE) activity is repressed in animal gonads by PIWI-Interacting RNAs (piRNAs), a class of small RNAs produced by heterochromatic loci enriched in TE fragments and called piRNA clusters. We have previously shown in Drosophila melanogaster, that maternally inherited piRNAs can epigenetically convert a homologous inactive cluster composed of tandemly repeated transgenes into a functional piRNA cluster. Here we show that the maternal inheritance dependency of activation can be circumvented when flies are developing at high temperature resulting in a rare but invasive epigenetic conversion. The newly acquired active state is stable through next generations even developed at a milder temperature. Silencing capacities, piRNA production and chromatin modifications are identical whether conversion occurred by maternal piRNA inheritance or by high temperature. Strikingly, heat conversion requires a copy of a homologous transgene located elsewhere in the genome. Altogether, these data report the first case of a piRNA cluster establishment due to environmental changes, highlighting how such variations might impact the long-term epigenome shaping.