Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions
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Published:2018-03-12
Issue:4
Volume:28
Page:532-546
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ISSN:1088-9051
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Container-title:Genome Research
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language:en
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Short-container-title:Genome Res.
Author:
Choi Kyuha,Zhao Xiaohui,Tock Andrew J.,Lambing Christophe,Underwood Charles J.,Hardcastle Thomas J.,Serra Heïdi,Kim Juhyun,Cho Hyun Seob,Kim Jaeil,Ziolkowski Piotr A.,Yelina Nataliya E.,Hwang Ildoo,Martienssen Robert A.,Henderson Ian R.
Abstract
Meiotic recombination initiates from DNA double-strand breaks (DSBs) generated by SPO11 topoisomerase-like complexes. Meiotic DSB frequency varies extensively along eukaryotic chromosomes, with hotspots controlled by chromatin and DNA sequence. To map meiotic DSBs throughout a plant genome, we purified and sequenced Arabidopsis thaliana SPO11-1-oligonucleotides. SPO11-1-oligos are elevated in gene promoters, terminators, and introns, which is driven by AT-sequence richness that excludes nucleosomes and allows SPO11-1 access. A positive relationship was observed between SPO11-1-oligos and crossovers genome-wide, although fine-scale correlations were weaker. This may reflect the influence of interhomolog polymorphism on crossover formation, downstream from DSB formation. Although H3K4me3 is enriched in proximity to SPO11-1-oligo hotspots at gene 5′ ends, H3K4me3 levels do not correlate with DSBs. Repetitive transposons are thought to be recombination silenced during meiosis, to prevent nonallelic interactions and genome instability. Unexpectedly, we found high SPO11-1-oligo levels in nucleosome-depleted Helitron/Pogo/Tc1/Mariner DNA transposons, whereas retrotransposons were coldspots. High SPO11-1-oligo transposons are enriched within gene regulatory regions and in proximity to immunity genes, suggesting a role as recombination enhancers. As transposon mobility in plant genomes is restricted by DNA methylation, we used the met1 DNA methyltransferase mutant to investigate the role of heterochromatin in SPO11-1-oligo distributions. Epigenetic activation of meiotic DSBs in proximity to centromeres and transposons occurred in met1 mutants, coincident with reduced nucleosome occupancy, gain of transcription, and H3K4me3. Together, our work reveals a complex relationship between chromatin and meiotic DSBs within A. thaliana genes and transposons, with significance for the diversity and evolution of plant genomes.
Funder
Royal Society University Research Fellowship
Gatsby Charitable Foundation
BBSRC
BBSRC-Meiogenix IPA
ERA-CAPS/BBSRC “DeCOP”
ERC “SynthHotSpot” Consolidator
National Natural Science Foundation of China
RDA Next-Generation BioGreen 21 Program
NRF Basic Science Research Program
POSTECH Basic Research Institute
EMBO long-term postdoctoral fellowship
Publisher
Cold Spring Harbor Laboratory
Subject
Genetics(clinical),Genetics
Cited by
165 articles.
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