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The composition of piRNA clusters in Drosophila melanogaster deviates from expectations under the trap model

BACKGROUND: It is widely assumed that the invasion of a transposable element (TE) in mammals and invertebrates is stopped when a copy of the TE jumps into a piRNA cluster (i.e., the trap model). However, recent works, which for example showed that deletion of three major piRNA clusters has no effect...

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Autores principales: Wierzbicki, Filip, Kofler, Robert
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10588112/
https://www.ncbi.nlm.nih.gov/pubmed/37858221
http://dx.doi.org/10.1186/s12915-023-01727-7
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author Wierzbicki, Filip
Kofler, Robert
author_facet Wierzbicki, Filip
Kofler, Robert
author_sort Wierzbicki, Filip
collection PubMed
description BACKGROUND: It is widely assumed that the invasion of a transposable element (TE) in mammals and invertebrates is stopped when a copy of the TE jumps into a piRNA cluster (i.e., the trap model). However, recent works, which for example showed that deletion of three major piRNA clusters has no effect on TE activity, cast doubt on the trap model. RESULTS: Here, we test the trap model from a population genetics perspective. Our simulations show that the composition of regions that act as transposon traps (i.e., potentially piRNA clusters) ought to deviate from regions that have no effect on TE activity. We investigated TEs in five Drosophila melanogaster strains using three complementary approaches to test whether the composition of piRNA clusters matches these expectations. We found that the abundance of TE families inside and outside of piRNA clusters is highly correlated, although this is not expected under the trap model. Furthermore, the distribution of the number of TE insertions in piRNA clusters is also much broader than expected. CONCLUSIONS: We found that the observed composition of piRNA clusters is not in agreement with expectations under the simple trap model. Dispersed piRNA producing TE insertions and temporal as well as spatial heterogeneity of piRNA clusters may account for these deviations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01727-7.
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spelling pubmed-105881122023-10-21 The composition of piRNA clusters in Drosophila melanogaster deviates from expectations under the trap model Wierzbicki, Filip Kofler, Robert BMC Biol Research Article BACKGROUND: It is widely assumed that the invasion of a transposable element (TE) in mammals and invertebrates is stopped when a copy of the TE jumps into a piRNA cluster (i.e., the trap model). However, recent works, which for example showed that deletion of three major piRNA clusters has no effect on TE activity, cast doubt on the trap model. RESULTS: Here, we test the trap model from a population genetics perspective. Our simulations show that the composition of regions that act as transposon traps (i.e., potentially piRNA clusters) ought to deviate from regions that have no effect on TE activity. We investigated TEs in five Drosophila melanogaster strains using three complementary approaches to test whether the composition of piRNA clusters matches these expectations. We found that the abundance of TE families inside and outside of piRNA clusters is highly correlated, although this is not expected under the trap model. Furthermore, the distribution of the number of TE insertions in piRNA clusters is also much broader than expected. CONCLUSIONS: We found that the observed composition of piRNA clusters is not in agreement with expectations under the simple trap model. Dispersed piRNA producing TE insertions and temporal as well as spatial heterogeneity of piRNA clusters may account for these deviations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01727-7. BioMed Central 2023-10-20 /pmc/articles/PMC10588112/ /pubmed/37858221 http://dx.doi.org/10.1186/s12915-023-01727-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Wierzbicki, Filip
Kofler, Robert
The composition of piRNA clusters in Drosophila melanogaster deviates from expectations under the trap model
title The composition of piRNA clusters in Drosophila melanogaster deviates from expectations under the trap model
title_full The composition of piRNA clusters in Drosophila melanogaster deviates from expectations under the trap model
title_fullStr The composition of piRNA clusters in Drosophila melanogaster deviates from expectations under the trap model
title_full_unstemmed The composition of piRNA clusters in Drosophila melanogaster deviates from expectations under the trap model
title_short The composition of piRNA clusters in Drosophila melanogaster deviates from expectations under the trap model
title_sort composition of pirna clusters in drosophila melanogaster deviates from expectations under the trap model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10588112/
https://www.ncbi.nlm.nih.gov/pubmed/37858221
http://dx.doi.org/10.1186/s12915-023-01727-7
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