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Taming active transposons at Drosophila telomeres: The interconnection between HipHop’s roles in capping and transcriptional silencing

Drosophila chromosomes are elongated by retrotransposon attachment, a process poorly understood. Here we characterized a mutation affecting the HipHop telomere-capping protein. In mutant ovaries and the embryos that they produce, telomere retrotransposons are activated and transposon RNP accumulates...

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Autores principales: Cui, Min, Bai, Yaofu, Li, Kaili, Rong, Yikang S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8651111/
https://www.ncbi.nlm.nih.gov/pubmed/34813587
http://dx.doi.org/10.1371/journal.pgen.1009925
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author Cui, Min
Bai, Yaofu
Li, Kaili
Rong, Yikang S.
author_facet Cui, Min
Bai, Yaofu
Li, Kaili
Rong, Yikang S.
author_sort Cui, Min
collection PubMed
description Drosophila chromosomes are elongated by retrotransposon attachment, a process poorly understood. Here we characterized a mutation affecting the HipHop telomere-capping protein. In mutant ovaries and the embryos that they produce, telomere retrotransposons are activated and transposon RNP accumulates. Genetic results are consistent with that this hiphop mutation weakens the efficacy of HP1-mediated silencing while leaving piRNA-based mechanisms largely intact. Remarkably, mutant females display normal fecundity suggesting that telomere de-silencing is compatible with germline development. Moreover, unlike prior mutants with overactive telomeres, the hiphop stock does not over-accumulate transposons for hundreds of generations. This is likely due to the loss of HipHop’s abilities both to silence transcription and to recruit transposons to telomeres in the mutant. Furthermore, embryos produced by mutant mothers experience a checkpoint activation, and a further loss of maternal HipHop leads to end-to-end fusion and embryonic arrest. Telomeric retroelements fulfill an essential function yet maintain a potentially conflicting relationship with their Drosophila host. Our study thus showcases a possible intermediate in this arm race in which the host is adapting to over-activated transposons while maintaining genome stability. Our results suggest that the collapse of such a relationship might only occur when the selfish element acquires the ability to target non-telomeric regions of the genome. HipHop is likely part of this machinery restricting the elements to the gene-poor region of telomeres. Lastly, our hiphop mutation behaves as a recessive suppressor of PEV that is mediated by centric heterochromatin, suggesting its broader effect on chromatin not limited to telomeres.
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spelling pubmed-86511112021-12-08 Taming active transposons at Drosophila telomeres: The interconnection between HipHop’s roles in capping and transcriptional silencing Cui, Min Bai, Yaofu Li, Kaili Rong, Yikang S. PLoS Genet Research Article Drosophila chromosomes are elongated by retrotransposon attachment, a process poorly understood. Here we characterized a mutation affecting the HipHop telomere-capping protein. In mutant ovaries and the embryos that they produce, telomere retrotransposons are activated and transposon RNP accumulates. Genetic results are consistent with that this hiphop mutation weakens the efficacy of HP1-mediated silencing while leaving piRNA-based mechanisms largely intact. Remarkably, mutant females display normal fecundity suggesting that telomere de-silencing is compatible with germline development. Moreover, unlike prior mutants with overactive telomeres, the hiphop stock does not over-accumulate transposons for hundreds of generations. This is likely due to the loss of HipHop’s abilities both to silence transcription and to recruit transposons to telomeres in the mutant. Furthermore, embryos produced by mutant mothers experience a checkpoint activation, and a further loss of maternal HipHop leads to end-to-end fusion and embryonic arrest. Telomeric retroelements fulfill an essential function yet maintain a potentially conflicting relationship with their Drosophila host. Our study thus showcases a possible intermediate in this arm race in which the host is adapting to over-activated transposons while maintaining genome stability. Our results suggest that the collapse of such a relationship might only occur when the selfish element acquires the ability to target non-telomeric regions of the genome. HipHop is likely part of this machinery restricting the elements to the gene-poor region of telomeres. Lastly, our hiphop mutation behaves as a recessive suppressor of PEV that is mediated by centric heterochromatin, suggesting its broader effect on chromatin not limited to telomeres. Public Library of Science 2021-11-23 /pmc/articles/PMC8651111/ /pubmed/34813587 http://dx.doi.org/10.1371/journal.pgen.1009925 Text en © 2021 Cui et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
Cui, Min
Bai, Yaofu
Li, Kaili
Rong, Yikang S.
Taming active transposons at Drosophila telomeres: The interconnection between HipHop’s roles in capping and transcriptional silencing
title Taming active transposons at Drosophila telomeres: The interconnection between HipHop’s roles in capping and transcriptional silencing
title_full Taming active transposons at Drosophila telomeres: The interconnection between HipHop’s roles in capping and transcriptional silencing
title_fullStr Taming active transposons at Drosophila telomeres: The interconnection between HipHop’s roles in capping and transcriptional silencing
title_full_unstemmed Taming active transposons at Drosophila telomeres: The interconnection between HipHop’s roles in capping and transcriptional silencing
title_short Taming active transposons at Drosophila telomeres: The interconnection between HipHop’s roles in capping and transcriptional silencing
title_sort taming active transposons at drosophila telomeres: the interconnection between hiphop’s roles in capping and transcriptional silencing
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8651111/
https://www.ncbi.nlm.nih.gov/pubmed/34813587
http://dx.doi.org/10.1371/journal.pgen.1009925
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