Maelstrom Represses Canonical Polymerase II Transcription within Bi-Directional piRNA Clusters in Drosophila melanogaster

Abstract

In Drosophila, 23-30 nt long PIWI-interacting RNAs (piRNAs) direct the protein Piwi to silence germline transposon transcription. Most germline piRNAs derive from dual-strand piRNA clusters, heterochromatic transposon graveyards that are transcribed from both genomic strands. These piRNA sources are marked by the Heterochromatin Protein 1 homolog, Rhino (Rhi), which facilitates their promoter-independent transcription, suppresses splicing, and inhibits transcriptional termination. Here, we report that the protein Maelstrom (Mael) represses canonical, promoter-dependent transcription in dual-strand clusters, allowing Rhi to initiate piRNA precursor transcription. In addition to Mael, the piRNA biogenesis factors Armitage and Piwi, but not Rhi, are required to repress canonical transcription in dual-strand clusters. We propose that Armitage, Piwi, and Mael collaborate to repress potentially dangerous transcription of individual transposon mRNAs within clusters, while Rhi allows non-canonical transcription of the clusters into piRNA precursors without generating transposase-encoding mRNAs.