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Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation

Eukaryotic centromeres contain the kinetochore, which connects chromosomes to the spindle allowing segregation. During meiosis, centromeres are suppressed for inter-homolog crossover, as recombination in these regions can cause chromosome missegregation and aneuploidy. Plant centromeres are surround...

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Autores principales: Underwood, Charles J., Choi, Kyuha, Lambing, Christophe, Zhao, Xiaohui, Serra, Heïdi, Borges, Filipe, Simorowski, Joe, Ernst, Evan, Jacob, Yannick, Henderson, Ian R., Martienssen, Robert A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880242/
https://www.ncbi.nlm.nih.gov/pubmed/29530927
http://dx.doi.org/10.1101/gr.227116.117
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author Underwood, Charles J.
Choi, Kyuha
Lambing, Christophe
Zhao, Xiaohui
Serra, Heïdi
Borges, Filipe
Simorowski, Joe
Ernst, Evan
Jacob, Yannick
Henderson, Ian R.
Martienssen, Robert A.
author_facet Underwood, Charles J.
Choi, Kyuha
Lambing, Christophe
Zhao, Xiaohui
Serra, Heïdi
Borges, Filipe
Simorowski, Joe
Ernst, Evan
Jacob, Yannick
Henderson, Ian R.
Martienssen, Robert A.
author_sort Underwood, Charles J.
collection PubMed
description Eukaryotic centromeres contain the kinetochore, which connects chromosomes to the spindle allowing segregation. During meiosis, centromeres are suppressed for inter-homolog crossover, as recombination in these regions can cause chromosome missegregation and aneuploidy. Plant centromeres are surrounded by transposon-dense pericentromeric heterochromatin that is epigenetically silenced by histone 3 lysine 9 dimethylation (H3K9me2), and DNA methylation in CG and non-CG sequence contexts. However, the role of these chromatin modifications in control of meiotic recombination in the pericentromeres is not fully understood. Here, we show that disruption of Arabidopsis thaliana H3K9me2 and non-CG DNA methylation pathways, for example, via mutation of the H3K9 methyltransferase genes KYP/SUVH4 SUVH5 SUVH6, or the CHG DNA methyltransferase gene CMT3, increases meiotic recombination in proximity to the centromeres. Using immunocytological detection of MLH1 foci and genotyping by sequencing of recombinant plants, we observe that H3K9me2 and non-CG DNA methylation pathway mutants show increased pericentromeric crossovers. Increased pericentromeric recombination in H3K9me2/non-CG mutants occurs in hybrid and inbred backgrounds and likely involves contributions from both the interfering and noninterfering crossover repair pathways. We also show that meiotic DNA double-strand breaks (DSBs) increase in H3K9me2/non-CG mutants within the pericentromeres, via purification and sequencing of SPO11-1-oligonucleotides. Therefore, H3K9me2 and non-CG DNA methylation exert a repressive effect on both meiotic DSB and crossover formation in plant pericentromeric heterochromatin. Our results may account for selection of enhancer trap Dissociation (Ds) transposons into the CMT3 gene by recombination with proximal transposon launch-pads.
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spelling pubmed-58802422018-04-13 Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation Underwood, Charles J. Choi, Kyuha Lambing, Christophe Zhao, Xiaohui Serra, Heïdi Borges, Filipe Simorowski, Joe Ernst, Evan Jacob, Yannick Henderson, Ian R. Martienssen, Robert A. Genome Res Research Eukaryotic centromeres contain the kinetochore, which connects chromosomes to the spindle allowing segregation. During meiosis, centromeres are suppressed for inter-homolog crossover, as recombination in these regions can cause chromosome missegregation and aneuploidy. Plant centromeres are surrounded by transposon-dense pericentromeric heterochromatin that is epigenetically silenced by histone 3 lysine 9 dimethylation (H3K9me2), and DNA methylation in CG and non-CG sequence contexts. However, the role of these chromatin modifications in control of meiotic recombination in the pericentromeres is not fully understood. Here, we show that disruption of Arabidopsis thaliana H3K9me2 and non-CG DNA methylation pathways, for example, via mutation of the H3K9 methyltransferase genes KYP/SUVH4 SUVH5 SUVH6, or the CHG DNA methyltransferase gene CMT3, increases meiotic recombination in proximity to the centromeres. Using immunocytological detection of MLH1 foci and genotyping by sequencing of recombinant plants, we observe that H3K9me2 and non-CG DNA methylation pathway mutants show increased pericentromeric crossovers. Increased pericentromeric recombination in H3K9me2/non-CG mutants occurs in hybrid and inbred backgrounds and likely involves contributions from both the interfering and noninterfering crossover repair pathways. We also show that meiotic DNA double-strand breaks (DSBs) increase in H3K9me2/non-CG mutants within the pericentromeres, via purification and sequencing of SPO11-1-oligonucleotides. Therefore, H3K9me2 and non-CG DNA methylation exert a repressive effect on both meiotic DSB and crossover formation in plant pericentromeric heterochromatin. Our results may account for selection of enhancer trap Dissociation (Ds) transposons into the CMT3 gene by recombination with proximal transposon launch-pads. Cold Spring Harbor Laboratory Press 2018-04 /pmc/articles/PMC5880242/ /pubmed/29530927 http://dx.doi.org/10.1101/gr.227116.117 Text en © 2018 Underwood et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by/4.0/ This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research
Underwood, Charles J.
Choi, Kyuha
Lambing, Christophe
Zhao, Xiaohui
Serra, Heïdi
Borges, Filipe
Simorowski, Joe
Ernst, Evan
Jacob, Yannick
Henderson, Ian R.
Martienssen, Robert A.
Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation
title Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation
title_full Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation
title_fullStr Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation
title_full_unstemmed Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation
title_short Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation
title_sort epigenetic activation of meiotic recombination near arabidopsis thaliana centromeres via loss of h3k9me2 and non-cg dna methylation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880242/
https://www.ncbi.nlm.nih.gov/pubmed/29530927
http://dx.doi.org/10.1101/gr.227116.117
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