Rapid disassembly and Piwi-independent reassembly of Drosophila piRNA cluster heterochromatin following acute heat shock

TL;DR

Heat shock disrupts piRNA cluster heterochromatin in fruit flies, revealing new insights into how stress affects transposon silencing and piRNA regulation.

Contribution

The study reveals that RDC localization and piRNA cluster regulation are rapidly and reversibly altered by heat shock, independent of Piwi.

Findings

Acute heat shock causes rapid, reversible loss of RDC localization and cluster transcript expression.

Maternal piRNAs are not required for RDC localization to the 42AB cluster.

THO complex disruption delays RDC relocalization after heat shock.

Abstract

Environmental stress activates transposons and is proposed to generate genetic diversity that facilitates adaptive evolution. piRNAs guide germline transposon silencing, but the impact of stress on the piRNA pathway is not well understood. In Drosophila, the Rhino-Deadlock-Cuff complex (RDC) drives transcription of clusters composed of nested transposon fragments, generating precursors that are processed into mature piRNAs in the cytoplasm. We show that acute heat shock triggers rapid, reversible loss of RDC localization and cluster transcript expression with coordinate changes in the cytoplasmic processing machinery. Maternal piRNAs bound to Piwi are proposed to guide Rhino localization to clusters during early embryogenesis. However, RDC relocalization after heat shock is accelerated in piwi mutants and delayed in thoc7 mutants, which disrupt piRNA precursor binding to THO complex, and we show that maternally deposited piRNAs are dispensable for RDC localization to the major 42AB cluster. Cluster specification is reconsidered in light of these findings.

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