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Journal article

Transcriptional regulation of the piRNA pathway by Ovo in animal ovarian germ cells

Abstract:

The gene-regulatory mechanisms controlling the expression of the germline PIWI-interacting RNA (piRNA) pathway components within the gonads of metazoan species remain largely unexplored. In contrast to the male germline piRNA pathway, which in mice is known to be activated by the testis-specific transcription factor A-MYB, the nature of the ovary-specific gene-regulatory network driving the female germline piRNA pathway remains a mystery. Here, using Drosophila as a model, we combined multiple genomics approaches to reveal the transcription factor Ovo as regulator of the germline piRNA pathway in ovarian germ cells. Ectopic expression of Ovo in ovarian somatic cells activates germline piRNA pathway components, including the ping-pong factors Aubergine, Argonaute-3, and Vasa, leading to assembly of perinuclear cellular structures resembling nuage bodies of germ cells. We found that in ovarian somatic cells, transcription of ovo is repressed by l(3)mbt, thus preventing expression of germline piRNA pathway genes in the soma. Cross-species ChIP-seq and motif analyses demonstrate that Ovo is binding to genomic CCGTTA motifs within the promoters of germline piRNA pathway genes, suggesting a regulation by Ovo in ovaries analogous to that of A-MYB in testes. Our results also show consistent engagement of the Ovo transcription factor family at ovarian piRNA clusters across metazoan species, reflecting a deep evolutionary conservation of this regulatory paradigm from insects to humans.

Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1101/gad.352120.124

Authors

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Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Role:
Author
ORCID:
0000-0002-2313-965X
More by this author
Role:
Author
ORCID:
0000-0003-4021-3898
More by this author
Role:
Author
ORCID:
0000-0001-8471-0007


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Funder identifier:
https://ror.org/029chgv08
Grant:
226627/Z/22/Z


Publisher:
Cold Spring Harbor Laboratory Press
Journal:
Genes and Development More from this journal
Volume:
39
Issue:
3-4
Pages:
221-241
Publication date:
2024-12-20
Acceptance date:
2024-11-11
DOI:
EISSN:
1549-5477
ISSN:
0890-9369
Pmid:
39797761


Language:
English
Keywords:
Pubs id:
2080863
Local pid:
pubs:2080863
Deposit date:
2025-02-19
ARK identifier:

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