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Natural variation of piRNA expression affects immunity to transposable elements
In the Drosophila germline, transposable elements (TEs) are silenced by PIWI-interacting RNA (piRNA) that originate from distinct genomic regions termed piRNA clusters and are processed by PIWI-subfamily Argonaute proteins. Here, we explore the variation in the ability to restrain an alien TE in dif...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5407775/ https://www.ncbi.nlm.nih.gov/pubmed/28448516 http://dx.doi.org/10.1371/journal.pgen.1006731 |
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author | Ryazansky, Sergei Radion, Elizaveta Mironova, Anastasia Akulenko, Natalia Abramov, Yuri Morgunova, Valeriya Kordyukova, Maria Y. Olovnikov, Ivan Kalmykova, Alla |
author_facet | Ryazansky, Sergei Radion, Elizaveta Mironova, Anastasia Akulenko, Natalia Abramov, Yuri Morgunova, Valeriya Kordyukova, Maria Y. Olovnikov, Ivan Kalmykova, Alla |
author_sort | Ryazansky, Sergei |
collection | PubMed |
description | In the Drosophila germline, transposable elements (TEs) are silenced by PIWI-interacting RNA (piRNA) that originate from distinct genomic regions termed piRNA clusters and are processed by PIWI-subfamily Argonaute proteins. Here, we explore the variation in the ability to restrain an alien TE in different Drosophila strains. The I-element is a retrotransposon involved in the phenomenon of I-R hybrid dysgenesis in Drosophila melanogaster. Genomes of R strains do not contain active I-elements, but harbour remnants of ancestral I-related elements. The permissivity to I-element activity of R females, called reactivity, varies considerably in natural R populations, indicating the existence of a strong natural polymorphism in defense systems targeting transposons. To reveal the nature of such polymorphisms, we compared ovarian small RNAs between R strains with low and high reactivity and show that reactivity negatively correlates with the ancestral I-element-specific piRNA content. Analysis of piRNA clusters containing remnants of I-elements shows increased expression of the piRNA precursors and enrichment by the Heterochromatin Protein 1 homolog, Rhino, in weak R strains, which is in accordance with stronger piRNA expression by these regions. To explore the nature of the differences in piRNA production, we focused on two R strains, weak and strong, and showed that the efficiency of maternal inheritance of piRNAs as well as the I-element copy number are very similar in both strains. At the same time, germline and somatic uni-strand piRNA clusters generate more piRNAs in strains with low reactivity, suggesting the relationship between the efficiency of primary piRNA production and variable response to TE invasions. The strength of adaptive genome defense is likely driven by naturally occurring polymorphisms in the rapidly evolving piRNA pathway proteins. We hypothesize that hyper-efficient piRNA production is contributing to elimination of a telomeric retrotransposon HeT-A, which we have observed in one particular transposon-resistant R strain. |
format | Online Article Text |
id | pubmed-5407775 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-54077752017-05-14 Natural variation of piRNA expression affects immunity to transposable elements Ryazansky, Sergei Radion, Elizaveta Mironova, Anastasia Akulenko, Natalia Abramov, Yuri Morgunova, Valeriya Kordyukova, Maria Y. Olovnikov, Ivan Kalmykova, Alla PLoS Genet Research Article In the Drosophila germline, transposable elements (TEs) are silenced by PIWI-interacting RNA (piRNA) that originate from distinct genomic regions termed piRNA clusters and are processed by PIWI-subfamily Argonaute proteins. Here, we explore the variation in the ability to restrain an alien TE in different Drosophila strains. The I-element is a retrotransposon involved in the phenomenon of I-R hybrid dysgenesis in Drosophila melanogaster. Genomes of R strains do not contain active I-elements, but harbour remnants of ancestral I-related elements. The permissivity to I-element activity of R females, called reactivity, varies considerably in natural R populations, indicating the existence of a strong natural polymorphism in defense systems targeting transposons. To reveal the nature of such polymorphisms, we compared ovarian small RNAs between R strains with low and high reactivity and show that reactivity negatively correlates with the ancestral I-element-specific piRNA content. Analysis of piRNA clusters containing remnants of I-elements shows increased expression of the piRNA precursors and enrichment by the Heterochromatin Protein 1 homolog, Rhino, in weak R strains, which is in accordance with stronger piRNA expression by these regions. To explore the nature of the differences in piRNA production, we focused on two R strains, weak and strong, and showed that the efficiency of maternal inheritance of piRNAs as well as the I-element copy number are very similar in both strains. At the same time, germline and somatic uni-strand piRNA clusters generate more piRNAs in strains with low reactivity, suggesting the relationship between the efficiency of primary piRNA production and variable response to TE invasions. The strength of adaptive genome defense is likely driven by naturally occurring polymorphisms in the rapidly evolving piRNA pathway proteins. We hypothesize that hyper-efficient piRNA production is contributing to elimination of a telomeric retrotransposon HeT-A, which we have observed in one particular transposon-resistant R strain. Public Library of Science 2017-04-27 /pmc/articles/PMC5407775/ /pubmed/28448516 http://dx.doi.org/10.1371/journal.pgen.1006731 Text en © 2017 Ryazansky et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Ryazansky, Sergei Radion, Elizaveta Mironova, Anastasia Akulenko, Natalia Abramov, Yuri Morgunova, Valeriya Kordyukova, Maria Y. Olovnikov, Ivan Kalmykova, Alla Natural variation of piRNA expression affects immunity to transposable elements |
title | Natural variation of piRNA expression affects immunity to transposable elements |
title_full | Natural variation of piRNA expression affects immunity to transposable elements |
title_fullStr | Natural variation of piRNA expression affects immunity to transposable elements |
title_full_unstemmed | Natural variation of piRNA expression affects immunity to transposable elements |
title_short | Natural variation of piRNA expression affects immunity to transposable elements |
title_sort | natural variation of pirna expression affects immunity to transposable elements |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5407775/ https://www.ncbi.nlm.nih.gov/pubmed/28448516 http://dx.doi.org/10.1371/journal.pgen.1006731 |
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