We have identified, by genetic and cytological analyses, the minimal components of a chaperone complex involved in transposon (TE) silencing in Drosophila germ cells. We found that, after heat shock, the stress-inducible Hsp70 chaperone interacts with the chaperone complex and factors involved in piRNAs biogenesis in both ovaries and testes. Hsp70 induces displacement of these factors to the lysosomes. Concomitantly, we observed a significant activation of TEs at the posttranscriptional level, suggesting an involvement of Hsp70 in TE activation after stress. We propose that such a mechanism has evolutionary implications for the genome’s response to environmental stress.

Abstract

Previous studies have shown that heat shock stress may activate transposable elements (TEs) in Drosophila and other organisms. Such an effect depends on the disruption of a chaperone complex that is normally involved in biogenesis of Piwi-interacting RNAs (piRNAs), the largest class of germline-enriched small noncoding RNAs implicated in the epigenetic silencing of TEs. However, a satisfying picture of how chaperones could be involved in repressing TEs in germ cells is still unknown. Here we show that, in Drosophila, heat shock stress increases the expression of TEs at a posttranscriptional level by affecting piRNA biogenesis through the action of the inducible chaperone Hsp70. We found that stress-induced TE activation is triggered by an interaction of Hsp70 with the Hsc70−Hsp90 complex and other factors all involved in piRNA biogenesis in both ovaries and testes. Such interaction induces a displacement of all such factors to the lysosomes, resulting in a functional collapse of piRNA biogenesis. This mechanism has clear evolutionary implications. In the presence of drastic environmental changes, Hsp70 plays a key dual role in increasing both the survival probability of individuals and the genetic variability in their germ cells. The consequent increase of genetic variation in a population potentiates evolutionary plasticity and evolvability.