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Retrotransposon addiction promotes centromere function via epigenetically activated small RNAs

Retrotransposons have invaded eukaryotic centromeres in cycles of repeat expansion and purging, but the function of centromeric retrotransposons, if any, has remained unclear. In Arabidopsis, centromeric ATHILA retrotransposons give rise to epigenetically activated short interfering RNAs (easiRNAs)...

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Autores principales: Shimada, Atsushi, Cahn, Jonathan, Ernst, Evan, Lynn, Jason, Grimanelli, Daniel, Henderson, Ian, Kakutani, Tetsuji, Martienssen, Robert A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10418216/
https://www.ncbi.nlm.nih.gov/pubmed/37577592
http://dx.doi.org/10.1101/2023.08.02.551486
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author Shimada, Atsushi
Cahn, Jonathan
Ernst, Evan
Lynn, Jason
Grimanelli, Daniel
Henderson, Ian
Kakutani, Tetsuji
Martienssen, Robert A.
author_facet Shimada, Atsushi
Cahn, Jonathan
Ernst, Evan
Lynn, Jason
Grimanelli, Daniel
Henderson, Ian
Kakutani, Tetsuji
Martienssen, Robert A.
author_sort Shimada, Atsushi
collection PubMed
description Retrotransposons have invaded eukaryotic centromeres in cycles of repeat expansion and purging, but the function of centromeric retrotransposons, if any, has remained unclear. In Arabidopsis, centromeric ATHILA retrotransposons give rise to epigenetically activated short interfering RNAs (easiRNAs) in mutants in DECREASE IN DNA METHYLATION1 (DDM1), which promote histone H3 lysine-9 di-methylation (H3K9me2). Here, we show that mutants which lose both DDM1 and RNA dependent RNA polymerase (RdRP) have pleiotropic developmental defects and mis-segregation of chromosome 5 during mitosis. Fertility defects are epigenetically inherited with the centromeric region of chromosome 5, and can be rescued by directing artificial small RNAs to a single family of ATHILA5 retrotransposons specifically embedded within this centromeric region. easiRNAs and H3K9me2 promote pericentromeric condensation, chromosome cohesion and proper chromosome segregation in mitosis. Insertion of ATHILA silences transcription, while simultaneously making centromere function dependent on retrotransposon small RNAs, promoting the selfish survival and spread of centromeric retrotransposons. Parallels are made with the fission yeast S. pombe, where chromosome segregation depends on RNAi, and with humans, where chromosome segregation depends on both RNAi and HELLS(DDM1).
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spelling pubmed-104182162023-08-12 Retrotransposon addiction promotes centromere function via epigenetically activated small RNAs Shimada, Atsushi Cahn, Jonathan Ernst, Evan Lynn, Jason Grimanelli, Daniel Henderson, Ian Kakutani, Tetsuji Martienssen, Robert A. bioRxiv Article Retrotransposons have invaded eukaryotic centromeres in cycles of repeat expansion and purging, but the function of centromeric retrotransposons, if any, has remained unclear. In Arabidopsis, centromeric ATHILA retrotransposons give rise to epigenetically activated short interfering RNAs (easiRNAs) in mutants in DECREASE IN DNA METHYLATION1 (DDM1), which promote histone H3 lysine-9 di-methylation (H3K9me2). Here, we show that mutants which lose both DDM1 and RNA dependent RNA polymerase (RdRP) have pleiotropic developmental defects and mis-segregation of chromosome 5 during mitosis. Fertility defects are epigenetically inherited with the centromeric region of chromosome 5, and can be rescued by directing artificial small RNAs to a single family of ATHILA5 retrotransposons specifically embedded within this centromeric region. easiRNAs and H3K9me2 promote pericentromeric condensation, chromosome cohesion and proper chromosome segregation in mitosis. Insertion of ATHILA silences transcription, while simultaneously making centromere function dependent on retrotransposon small RNAs, promoting the selfish survival and spread of centromeric retrotransposons. Parallels are made with the fission yeast S. pombe, where chromosome segregation depends on RNAi, and with humans, where chromosome segregation depends on both RNAi and HELLS(DDM1). Cold Spring Harbor Laboratory 2023-08-03 /pmc/articles/PMC10418216/ /pubmed/37577592 http://dx.doi.org/10.1101/2023.08.02.551486 Text en https://creativecommons.org/licenses/by/4.0/This work is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Shimada, Atsushi
Cahn, Jonathan
Ernst, Evan
Lynn, Jason
Grimanelli, Daniel
Henderson, Ian
Kakutani, Tetsuji
Martienssen, Robert A.
Retrotransposon addiction promotes centromere function via epigenetically activated small RNAs
title Retrotransposon addiction promotes centromere function via epigenetically activated small RNAs
title_full Retrotransposon addiction promotes centromere function via epigenetically activated small RNAs
title_fullStr Retrotransposon addiction promotes centromere function via epigenetically activated small RNAs
title_full_unstemmed Retrotransposon addiction promotes centromere function via epigenetically activated small RNAs
title_short Retrotransposon addiction promotes centromere function via epigenetically activated small RNAs
title_sort retrotransposon addiction promotes centromere function via epigenetically activated small rnas
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10418216/
https://www.ncbi.nlm.nih.gov/pubmed/37577592
http://dx.doi.org/10.1101/2023.08.02.551486
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