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piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila melanogaster

Kotov, Alexei A. and Adashev, Vladimir E. and Godneeva, Baira K. and Ninova, Maria and Shatskikh, Aleksei S. and Bazylev, Sergei S. and Aravin, Alexei A. and Olenina, Ludmila V. (2019) piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila melanogaster. Nucleic Acids Research, 47 (8). pp. 4255-4271. ISSN 0305-1048. PMCID PMC6486647. https://resolver.caltech.edu/CaltechAUTHORS:20190225-104840462

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Abstract

The piRNA pathway is an adaptive mechanism that maintains genome stability by repression of selfish genomic elements. In the male germline of Drosophila melanogaster repression of Stellate genes by piRNAs generated from Supressor of Stellate (Su(Ste)) locus is required for male fertility, but both Su(Ste) piRNAs and their targets are absent in other Drosophila species. We found that D. melanogaster genome contains multiple X-linked non-coding genomic repeats that have sequence similarity to the protein-coding host gene vasa. In the male germline, these vasa-related AT-chX repeats produce abundant piRNAs that are antisense to vasa; however, vasa mRNA escapes silencing due to imperfect complementarity to AT-chX piRNAs. Unexpectedly, we discovered AT-chX piRNAs target vasa of Drosophila mauritiana in the testes of interspecies hybrids. In the majority of hybrid flies, the testes were strongly reduced in size and germline content. A minority of hybrids maintained wild-type array of premeiotic germ cells in the testes, but in them harmful Stellate genes were derepressed due to the absence of Su(Ste) piRNAs, and meiotic failures were observed. Thus, the piRNA pathway contributes to reproductive isolation between D. melanogaster and closely related species, causing hybrid male sterility via misregulation of two different host protein factors.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1093/nar/gkz130DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6486647PubMed CentralArticle
ORCID:
AuthorORCID
Ninova, Maria0000-0001-5051-5502
Additional Information:© 2019 The Author(s). Published by Oxford University Press on behalf of Nucleic Acids Research. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. Received October 01, 2018; Revised February 12, 2019; Editorial Decision February 14, 2019; Accepted February 16, 2019. Published: 21 February 2019. Data Availability: GEO accession number for the library data is GSE120802. We thank the Developmental Studies Hybridoma Bank for maintaining some of the antibodies used in this study. We thank M. Siomi, E. Gracheva, R. Lehmann, and D. Dodt for antibodies and O. M. Olenkina for help with fly manipulations. We thank R. Sachidanandam for help with bioinformatics analysis. The authors thank the Common Use Center of scientific equipment of the Institute of Molecular Genetics RAS, for providing the equipment. Funding: Ministry of Education and Science of Russian Federation [14.W03.31.0007]. Funding for open access charge: Ministry of Education and Science of Russian Federation [14.W03.31.0007]. Conflict of interest statement: None declared.
Funders:
Funding AgencyGrant Number
Ministry of Education and Science of Russian Federation14.W03.31.0007
Issue or Number:8
PubMed Central ID:PMC6486647
Record Number:CaltechAUTHORS:20190225-104840462
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190225-104840462
Official Citation:Alexei A Kotov, Vladimir E Adashev, Baira K Godneeva, Maria Ninova, Aleksei S Shatskikh, Sergei S Bazylev, Alexei A Aravin, Ludmila V Olenina, piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila melanogaster, Nucleic Acids Research, Volume 47, Issue 8, 07 May 2019, Pages 4255–4271, https://doi.org/10.1093/nar/gkz130
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:93222
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:25 Feb 2019 18:57
Last Modified:03 Oct 2019 20:52

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