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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. (2020) piRNA-mediated gene regulation and adaptation to sex-specific transposon expression in D. melanogaster male germline. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20200826-100150960

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Abstract

Small non-coding piRNAs act as sequence-specific guides to repress complementary targets in Metazoa. Prior studies in Drosophila ovaries have demonstrated the function of piRNA pathway in transposon silencing and therefore genome defense. However, the ability of piRNA program to respond to different transposon landscape 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, two sexes employ them differentially to combat sex-specific transposon landscape. We found several host genes targeted by piRNAs in testis, including CG12717/pita, a SUMO protease gene. piRNAs encoded on Y chromosome silence pita, but not its paralog, to exert sex- and paralog-specific gene regulation. Interestingly, pita 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-encoding gene.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
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: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-NC-ND 4.0 International license. Posted August 25, 2020. We are grateful to William Theurkauf, Trudi Schüpbach, Julius Brennecke and Bloomington Drosophila Stock Center for fly stocks. We thank Katalin Fejes Toth and members of Aravin lab for discussion and comments. We appreciate the help of Maria Ninova and Fan Gao (Bioinformatics Resource Center, Caltech) with bioinformatics analysis, the help of Grace Shin and Maayan Schwarzkopf with HCR experiments, the help of Giada Spigolon and Andres Collazo (Biological Imaging Facility, Caltech) with microscopy, and the help of Igor Antoshechkin (Millard and Muriel Jacobs Genetics and Genomics Laboratory, Caltech) with sequencing. This work was supported by grants from the National Institutes of Health (R01 GM097363) and by the HHMI Faculty Scholar Award to A.A.A. The authors declare no competing interests. Data and code availability: Sequencing data will be uploaded to NCBI SRA.
Funders:
Funding AgencyGrant Number
NIHR01 GM097363
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Record Number:CaltechAUTHORS:20200826-100150960
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200826-100150960
Official Citation:piRNA-mediated gene regulation and adaptation to sex-specific transposon expression in D. melanogaster male germline. Peiwei Chen, Alexei A Kotov, Baira K Godneeva, Sergei S Bazylev, Ludmila V Olenina, Alexei A Aravin. bioRxiv 2020.08.25.266585; doi: https://doi.org/10.1101/2020.08.25.266585
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:26 Aug 2020 17:13

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