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Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions.

Published version
Peer-reviewed

Type

Article

Change log

Authors

Choi, Kyuha 
Tock, Andrew J 
Lambing, Christophe 
Underwood, Charles J 

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.

Description

Keywords

Arabidopsis, Arabidopsis Proteins, Chromosomes, Fungal, DNA Breaks, Double-Stranded, DNA Methylation, DNA Transposable Elements, Epigenesis, Genetic, Meiosis, Nucleosomes, Regulatory Sequences, Nucleic Acid

Journal Title

Genome Res

Conference Name

Journal ISSN

1088-9051
1549-5469

Volume Title

28

Publisher

Cold Spring Harbor Laboratory
Sponsorship
The Royal Society (uf0762030)
Isaac Newton Trust (1026(ab))
Gatsby Charitable Foundation (GAT2962)
Biotechnology and Biological Sciences Research Council (BB/K007882/1)
Biotechnology and Biological Sciences Research Council (BB/L006847/1)
Biotechnology and Biological Sciences Research Council (BB/M004937/1)
The Royal Society (uf120133)
Biotechnology and Biological Sciences Research Council (BB/N007557/1)
European Research Council (681987)
BBSRC (via University of Bristol) (FSCI1554768)
European Research Council (340642)