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Stellate Genes and the piRNA Pathway in Speciation and Reproductive Isolation of Drosophila melanogaster

Adashev, Vladimir E. and Kotov, Alexei A. and Bazylev, Sergei S. and Shatskikh, Aleksei S. and Aravin, Alexei A. and Olenina, Ludmila V. (2021) Stellate Genes and the piRNA Pathway in Speciation and Reproductive Isolation of Drosophila melanogaster. Frontiers in Genetics, 11 . Art. No. 610665. ISSN 1664-8021. PMCID PMC7874207. https://resolver.caltech.edu/CaltechAUTHORS:20210219-120046711

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Abstract

One of the main conditions of the species splitting from a common precursor lineage is the prevention of a gene flow between diverging populations. The study of Drosophila interspecific hybrids allows to reconstruct the speciation mechanisms and to identify hybrid incompatibility factors that maintain post-zygotic reproductive isolation between closely related species. The regulation, evolution, and maintenance of the testis-specific Ste-Su(Ste) genetic system in Drosophila melanogaster is the subject of investigation worldwide. X-linked tandem testis-specific Stellate genes encode proteins homologous to the regulatory β-subunit of protein kinase CK2, but they are permanently repressed in wild-type flies by the piRNA pathway via piRNAs originating from the homologous Y-linked Su(Ste) locus. Derepression of Stellate genes caused by Su(Ste) piRNA biogenesis disruption leads to the accumulation of crystalline aggregates in spermatocytes, meiotic defects and male sterility. In this review we summarize current data about the origin, organization, evolution of the Ste-Su(Ste) system, and piRNA-dependent regulation of Stellate expression. The Ste-Su(Ste) system is fixed only in the D. melanogaster genome. According to our hypothesis, the acquisition of the Ste-Su(Ste) system by a part of the ancient fly population appears to be the causative factor of hybrid sterility in crosses of female flies with males that do not carry Y-linked Su(Ste) repeats. To support this scenario, we have directly demonstrated Stellate derepression and the corresponding meiotic disorders in the testes of interspecies hybrids between D. melanogaster and D. mauritiana. This finding embraces our hypothesis about the contribution of the Ste-Su(Ste) system and the piRNA pathway to the emergence of reproductive isolation of D. melanogaster lineage from initial species.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.3389/fgene.2020.610665DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc7874207/PubMed CentralArticle
ORCID:
AuthorORCID
Kotov, Alexei A.0000-0002-5866-3574
Aravin, Alexei A.0000-0002-6956-8257
Olenina, Ludmila V.0000-0002-7422-4387
Additional Information:© 2021 Adashev, Kotov, Bazylev, Shatskikh, Aravin and Olenina. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Received: 26 September 2020; Accepted: 29 December 2020; Published: 22 January 2021. We thank A. D. Stolyarenko for discussions on this manuscript. This work was funded by RFBR, project number #20-04-00562. Author Contributions. VA and LO prepared the initial version of the manuscript and created the figures. AK, SB, AS, and AA rigorously revised and improved the manuscript. VA, LO, AK, and AA polished the final version of the manuscript. All authors provided intellectual contribution, edited, and approved the manuscript for publication in its present version. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Funders:
Funding AgencyGrant Number
Russian Foundation for Basic Research20-04-00562
Subject Keywords:Drosophila, Stellate genes, piRNA pathway, reproductive isolation, hybrid sterility
PubMed Central ID:PMC7874207
Record Number:CaltechAUTHORS:20210219-120046711
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210219-120046711
Official Citation:Adashev VE, Kotov AA, Bazylev SS, Shatskikh AS, Aravin AA and Olenina LV (2021) Stellate Genes and the piRNA Pathway in Speciation and Reproductive Isolation of Drosophila melanogaster. Front. Genet. 11:610665. doi: 10.3389/fgene.2020.610665
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108124
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:22 Feb 2021 15:59
Last Modified:22 Feb 2021 15:59

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