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Published October 2023 | Published
Journal Article Open

A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila

Abstract

In animals, PIWI-interacting RNAs (piRNAs) direct PIWI proteins to silence complementary targets such as transposons. In Drosophila and other species with a maternally specified germline, piRNAs deposited in the egg initiate piRNA biogenesis in the progeny. However, Y chromosome loci cannot participate in such a chain of intergenerational inheritance. How then can the biogenesis of Y-linked piRNAs be initiated? Here, using Suppressor of Stellate (Su(Ste)), a Y-linked Drosophila melanogaster piRNA locus as a model, we show that Su(Ste) piRNAs are made in the early male germline via 5′-to-3′ phased piRNA biogenesis initiated by maternally deposited 1360/Hoppel transposon piRNAs. Notably, deposition of Su(Ste) piRNAs from XXY mothers obviates the need for phased piRNA biogenesis in sons. Together, our study uncovers a developmentally programmed, intergenerational mechanism that allows fly mothers to protect their sons using a Y-linked piRNA locus.

Copyright and License

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

Acknowledgement

We thank the Bloomington Drosophila Stock Center and the Developmental Studies Hybridoma Bank for reagents. We thank Z. Zhang and N. Lau for their helpful discussions and the Yamashita lab members for comments on the paper. The research was supported by the Howard Hughes Medical Institute (Y.M.Y., P.D.Z. and S.E.J.), National Institute of Health (NIH R01 HD109667 to J.K.K., R35 GM136275 to P.D.Z., R01GM097363 to A.A.A. and R35 GM130272 to S.E.J.) and the Whitehead Institute for Biomedical Research (Y.M.Y.).

Contributions

These authors contributed equally: Zsolt G. Venkei, Ildar Gainetdinov.

Z.G.V. and Y.M.Y. conceived the project. Z.G.V., I.G., S.E.J., J.K.K., P.D.Z. and Y.M.Y. designed experiments and interpreted the results. Z.G.V., I.G., A.B., C.B., J.M.F. and Y.M.Y. conducted experiments. Z.G.V., I.G., M.R.S., C.P.C., T.W.W., G.W.B. and S.F. analysed data. P.C. and A.A.A. contributed critical information in the course of the investigation. Z.G.V., I.G., Y.M.Y. and P.D.Z. wrote and edited the paper with the input from other authors. Y.M.Y. and P.D.Z. supervised the research.

Data Availability

Sequencing data generated in this study have been deposited in the National Center for Biotechnology Information Short Read Archive database under accession code PRJNA879723. Fly genome sequence and annotation (build dm6/BDGP6.22 release 98) used in this study were downloaded from Ensembl at ftp://ftp.ensembl.org/pub/release-98/fasta/drosophila_melanogaster/ and ftp://ftp.ensembl.org/pub/release-98/gtf/drosophila_melanogaster/; fly rRNA sequences were downloaded from SILVA rRNA database at https://www.arb-silva.de/. Source data are provided with this paper. All other data supporting the findings of this study are available from the corresponding authors upon request.

Code Availability

Code used in this work is deposited at https://github.com/ildargv/Venkei_et_al_2023.

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Additional details

Created:
November 3, 2023
Modified:
January 9, 2024