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piRNA-mediated gene regulation and adaptation to sex-specific transposon expression in D. melanogaster male germline

Chen, Peiwei and Kotov, Alexei A. and Godneeva, Baira K. and Bazylev, Sergei S. and Olenina, Ludmila V. and Aravin, Alexei A. (2021) piRNA-mediated gene regulation and adaptation to sex-specific transposon expression in D. melanogaster male germline. Genes and Development, 35 (11-12). pp. 914-935. ISSN 0890-9369. PMCID PMC8168559. doi:10.1101/gad.345041.120. https://resolver.caltech.edu/CaltechAUTHORS:20200826-100150960

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Abstract

Small noncoding piRNAs act as sequence-specific guides to repress complementary targets in Metazoa. Prior studies in Drosophila ovaries have demonstrated the function of the piRNA pathway in transposon silencing and therefore genome defense. However, the ability of the piRNA program to respond to different transposon landscapes and the role of piRNAs in regulating host gene expression remain poorly understood. Here, we comprehensively analyzed piRNA expression and defined the repertoire of their targets in Drosophila melanogaster testes. Comparison of piRNA programs between sexes revealed sexual dimorphism in piRNA programs that parallel sex-specific transposon expression. Using a novel bioinformatic pipeline, we identified new piRNA clusters and established complex satellites as dual-strand piRNA clusters. While sharing most piRNA clusters, the two sexes employ them differentially to combat the sex-specific transposon landscape. We found two piRNA clusters that produce piRNAs antisense to four host genes in testis, including CG12717/pirate, a SUMO protease gene. piRNAs encoded on the Y chromosome silence pirate, but not its paralog, to exert sex- and paralog-specific gene regulation. Interestingly, pirate is targeted by endogenous siRNAs in a sibling species, Drosophila mauritiana, suggesting distinct but related silencing strategies invented in recent evolution to regulate a conserved protein-coding gene.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/gad.345041.120DOIArticle
http://genesdev.cshlp.org/content/35/11-12/914/suppl/DC1PublisherSupplementary Material
https://doi.org/10.1101/2020.08.25.266585DOIDiscussion Paper
ORCID:
AuthorORCID
Chen, Peiwei0000-0001-7160-6673
Kotov, Alexei A.0000-0002-5866-3574
Olenina, Ludmila V.0000-0002-7422-4387
Aravin, Alexei A.0000-0002-6956-8257
Additional Information:© 2021 Chen et al.; Published by Cold Spring Harbor Laboratory Press. This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/. Received September 21, 2020. Accepted April 8, 2021. Published in Advance May 13, 2021. Data availability: Sequencing data can be accessed via NCBI SRA with the following accession numbers: PRJNA646006 (rhi), PRJNA646216 (aub, zuc, and spn-E), and PRJNA719671 (degradome). We are grateful to William Theurkauf, Trudi Schüpbach, Julius Brennecke, and the Bloomington Drosophila Stock Center for fly stocks.We thank Katalin Fejes Toth and members of the Aravin laboratory for discussion, and Silke Jensen and Emilie Brasset for valuable comments on the preprint. We appreciate the help of Maria Ninova and Fan Gao (Bioinformatics Resource Center, California Institute of Technology) with bioinformatics analysis, the help of Pei-Hsuan Wu and Ildar Gainetdinov (Phil Zamore’s laboratory) with degradome-seq experiments, the help of Grace Shin and Maayan Schwarzkopf with HCR experiments, the help of Giada Spigolon and Andres Collazo (Biological Imaging Facility, California Institute of Technology) with microscopy, and the help of Igor Antoshechkin (Millard and Muriel Jacobs Genetics and Genomics Laboratory, California Institute of Technology) with sequencing. This work was supported by grants from the National Institutes of Health (R01 GM097363) and by the Howard Hughes Medical Institute Faculty Scholar Award to A.A.A. Author contributions: P.C. conducted most experiments and most bioinformatic analysis. B.K.G. performed testis RNA-seq. All authors designed experiments and analyzed the data. P.C. and A.A.A. wrote the manuscript with input from all other coauthors. The authors declare no competing interests.
Group:Millard and Muriel Jacobs Genetics and Genomics Laboratory
Funders:
Funding AgencyGrant Number
NIHR01 GM097363
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:Drosophila mauritiana; Drosophila melanogaster; Y chromosome; piRNA; satellite DNA; sexual dimorphism; spermatogenesis; transposable element
Issue or Number:11-12
PubMed Central ID:PMC8168559
DOI:10.1101/gad.345041.120
Record Number:CaltechAUTHORS:20200826-100150960
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200826-100150960
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:105115
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:26 Aug 2020 17:13
Last Modified:09 Jul 2021 21:07

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