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Transcriptional factor Tj is the master regulator of the somatic piRNA pathway in the Drosophila ovarian follicle cells [smallRNA-seq]

ABSTRACT: Transposable elements (TEs) pose a threat to genome integrity, and the piRNA pathway in animal gonads plays a crucial role in silencing TE activity. While the transcriptional regulation of piRNA pathway components in germline cells is well understood, the mechanisms orchestrating the transcriptional program of the somatic piRNA pathway in surrounding somatic cells remains poorly defined. Here, we demonstrate that Traffic Jam (Tj), an orthologue of a large Maf transcription factor in mammals, is a master regulator of the somatic piRNA pathway playing a crucial role in maintaining TE silencing and genomic integrity in somatic tissues . We show that Tj directly binds to the promoters of piRNA factors such as fs(1)Yb, nxf2, panx, and armi, as well as the flamenco piRNA cluster, a major locus for TE silencing in somatic cells. Knockdown of Tj in somatic follicle cells results in significant downregulation of these piRNA factors, a complete loss of flam expression, and derepression of TEs. We have identified an enhancer downstream of the flam promoter, including TJ binding sites, essential for high and specific flam expression in ovarian follicle cells in adult ovaries. This work uncovers a previously unappreciated layer of transcriptional regulation oc the piRNA pathway and we propose that Tj evolved to orchestrate the somatic piRNA pathway expression, ensuring efficient TE silencing in somatic cells that support germ cells, thereby preventing instability from being transmitted to the offspring.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE282039 | GEO | 2025/04/11

REPOSITORIES: GEO

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Transcriptional factor Tj is the master regulator of the somatic piRNA pathway in the Drosophila ovarian follicle cells [RNA-seq]

Project description:Transposable elements (TEs) pose a threat to genome integrity, and the piRNA pathway in animal gonads plays a crucial role in silencing TE activity. While the transcriptional regulation of piRNA pathway components in germline cells is well understood, the mechanisms orchestrating the transcriptional program of the somatic piRNA pathway in surrounding somatic cells remains poorly defined. Here, we demonstrate that Traffic Jam (Tj), an orthologue of a large Maf transcription factor in mammals, is a master regulator of the somatic piRNA pathway playing a crucial role in maintaining TE silencing and genomic integrity in somatic tissues . We show that Tj directly binds to the promoters of piRNA factors such as fs(1)Yb, nxf2, panx, and armi, as well as the flamenco piRNA cluster, a major locus for TE silencing in somatic cells. Knockdown of Tj in somatic follicle cells results in significant downregulation of these piRNA factors, a complete loss of flam expression, and derepression of TEs. We have identified an enhancer downstream of the flam promoter, including TJ binding sites, essential for high and specific flam expression in ovarian follicle cells in adult ovaries. This work uncovers a previously unappreciated layer of transcriptional regulation oc the piRNA pathway and we propose that Tj evolved to orchestrate the somatic piRNA pathway expression, ensuring efficient TE silencing in somatic cells that support germ cells, thereby preventing instability from being transmitted to the offspring.

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