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

Kyuha Choi, Xiaohui Zhao, Andrew J. Tock, Christophe Lambing, Charles J. Underwood, Thomas J. Hardcastle, Heïdi Serra, Juhyun Kim, Hyun Seob Cho, Jaeil Kim, Piotr A. Ziolkowski, Nataliya E. Yelina, Ildoo Hwang, Robert A. Martienssen, Ian R. Henderson

Research output: Contribution to journalArticle

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-oligonu-cleotides. 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.

Original languageEnglish (US)
Pages (from-to)532-546
Number of pages15
JournalGenome Research
Volume28
Issue number4
DOIs
StatePublished - Apr 1 2018
Externally publishedYes

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Nucleosomes
Nucleic Acid Regulatory Sequences
DNA Methylation
Arabidopsis
Plant Genome
Genetic Recombination
Genes
Chromatin
Retroelements
DNA Transposable Elements
Double-Stranded DNA Breaks
Heterochromatin
Centromere
Genomic Instability
Meiosis
Methyltransferases
Epigenomics
Introns
Immunity
Chromosomes

ASJC Scopus subject areas

  • Genetics
  • Genetics(clinical)

Cite this

Choi, K., Zhao, X., Tock, A. J., Lambing, C., Underwood, C. J., Hardcastle, T. J., ... Henderson, I. R. (2018). Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions. Genome Research, 28(4), 532-546. https://doi.org/10.1101/gr.225599.117

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

In: Genome Research, Vol. 28, No. 4, 01.04.2018, p. 532-546.

Research output: Contribution to journalArticle

Choi, K, Zhao, X, Tock, AJ, Lambing, C, Underwood, CJ, Hardcastle, TJ, Serra, H, Kim, J, Cho, HS, Kim, J, Ziolkowski, PA, Yelina, NE, Hwang, I, Martienssen, RA & Henderson, IR 2018, 'Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions', Genome Research, vol. 28, no. 4, pp. 532-546. https://doi.org/10.1101/gr.225599.117
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. / Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions. In: Genome Research. 2018 ; Vol. 28, No. 4. pp. 532-546.
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