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Published March 28, 2023 | Submitted + Supplemental Material
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Drosophila Males Use 5′-to-3′ Phased Biogenesis to Make Stellate-silencing piRNAs that Lack Homology to Maternally Deposited piRNA Guides

Abstract

PIWI-interacting RNAs (piRNAs) direct PIWI proteins to silence complementary targets such as transposons. In animals with a maternally specified germline, e.g. Drosophila melanogaster, maternally deposited piRNAs initiate piRNA biogenesis in the progeny. Normal fertility in D. melanogaster males requires repression of tandemly repeated Stellate genes by piRNAs from Suppressor of Stellate [Su(Ste)]. Because the Su(Ste) loci are on the Y chromosome, Su(Ste) piRNAs are not deposited in oocytes. How the male germline produces Su(Ste) piRNAs in the absence of maternally deposited Su(Ste) piRNAs is unknown. Here, we show that Su(Ste) piRNAs are made in the early male germline via 5′-to-3′ phased piRNA biogenesis triggered by maternally deposited 1360/Hoppel transposon piRNAs. Strikingly, deposition of Su(Ste) piRNAs from XXY mothers obviates the need for phased piRNA biogenesis in sons. Together, our study uncovers the developmentally programmed mechanism that allows fly mothers to protect their sons using a Y-linked piRNA locus.

Additional Information

The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license. We thank the Bloomington Drosophila Stock Center and the Developmental Studies Hybridoma Bank for reagents. We thank Zhao Zhang and Nelson Lau for their helpful discussions, and the Yamashita lab members for comments on the manuscript. The research was supported by the Howard Hughes Medical Institute (YMY, PDZ, SEJ), National Institute of Health (NIH R01 HD109667 to JKK, R35 GM136275 to PDZ, R01GM097363 to AAA and R35 GM130272 to SEJ), and the Whitehead Institute for Biomedical Research (YMY). Author contributions. ZGV and YMY conceived the project. ZV, IG, CB and YMY conducted experiments. ZGV, IG, YMY, PDZ designed experiments and interpreted the results. ZGV, IG, MRS, CPC, JKK, TWW, and BWB conducted bioinformatics analysis. PC and AA contributed critical information in the course of the investigation. ZGV, IG, YMY, PDZ wrote and edited the manuscript with the inputs from other authors. YMY and PDZ supervised the research. Data Availability. Sequencing data are available from the National Center for Biotechnology Information Small Read Archive using accession number PRJNA879723.

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Submitted - 2022.09.12.507655v1.full.pdf

Supplemental Material - media-1.pdf

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Additional details

Created:
August 20, 2023
Modified:
December 13, 2023