Survival protection mechanisms and genetic variability induction after stress: two sides of the same Hsp70 coin

Abstract

AbstractPrevious studies have shown that heat shock stress may increase transcription levels and, in some cases, also the transposition of certain transposable elements (TEs) in Drosophila and other organisms. Other studies have also demonstrated that heat shock chaperones as Hsp90 and Hop are involved in repressing transposon’s activity in Drosophila melanogaster by their involvement in crucial steps of the biogenesis of Piwi-interacting RNAs (piRNAs), the largest class of germline-enriched small non-coding RNA implicated in the epigenetic silencing of TEs. However, a satisfying picture of how many chaperones and their respective functional roles could be involved in repressing transposons in germ cell is still unknown. Here we show that in Drosophila heat shock activates transposon′s expression at post-transcriptional level by disrupting a repressive chaperone complex by a decisive role of the stress-inducible chaperone Hsp70. We found that stress-induced transposons 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. In support of a significant role of Hsp70 in transposon activation after stress, we found that the expression under normal conditions of Hsp70 in transgenic flies increases the amount of transposon transcripts and displaces the components of chaperon machinery outside the nuage as observed after heat shock. So that, our results demonstrate that heat shock stress is capable to increase the expression of transposons at post-transcriptional level by affecting piRNA biogenesis through the action of the inducible chaperone Hsp70. We think that such mechanism proposes relevant evolutionary implications. In 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. This in turn should be translated into an increase of genetic variability inside the populations thus potentiating their evolutionary plasticity and evolvability.