The transcription factor Traffic jam orchestrates the somatic piRNA pathway in Drosophila ovaries

Abstract

The PIWI-interacting RNA (piRNA) pathway is essential for transposable element (TE) silencing in animal gonads. While the transcriptional regulation of piRNA pathway components in germ cells has been documented in mice and flies, their control in somatic cells of Drosophila ovaries remains unresolved. Here, we demonstrate that Traffic jam (Tj), the Drosophila orthologue of large Maf transcription factors in mammals, is a master regulator of the somatic piRNA pathway. Tj binds to regulatory regions of somatic piRNA factors and the major piRNA cluster flamenco, which carries a Tj-bound enhancer downstream of its promoter. Depletion of Tj in somatic follicle cells causes downregulation of piRNA factors, loss of flam expression and de-repression of gypsy-family TEs. We propose that the arms race between the host and TEs led to the co-evolution of promoters in piRNA pathway genes as well as TE regulatory regions that both rely on a shared transcription factor. Highlights- Traffic jam (Tj) acts as a master regulator of the somatic piRNA pathway in Drosophila. - Tj regulates a network of piRNA pathway genes, mirroring the gene-regulatory mechanism of A-MYB in the mouse testis and Ovo in fly ovaries. - Cis-regulatory elements with Tj motifs are present at the promoters of somatic piRNA pathway genes. - The expression of the flamenco piRNA cluster is directly controlled by Tj.