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Extrachromosomal circular DNA and structural variants highlight genome instability in Arabidopsis epigenetic mutants

Author

Listed:
  • Panpan Zhang

    (Laboratory of Plant Genome and Development
    Laboratory of Plant Genome and Development
    University of Montpellier)

  • Assane Mbodj

    (Laboratory of Plant Genome and Development
    Laboratory of Plant Genome and Development)

  • Abirami Soundiramourtty

    (Laboratory of Plant Genome and Development
    University of Perpignan)

  • Christel Llauro

    (Laboratory of Plant Genome and Development
    Laboratory of Plant Genome and Development)

  • Alain Ghesquière

    (CIRAD)

  • Mathieu Ingouff

    (CIRAD)

  • R. Keith Slotkin

    (Donald Danforth Plant Science Center
    University of Missouri)

  • Frédéric Pontvianne

    (Laboratory of Plant Genome and Development)

  • Marco Catoni

    (University of Birmingham)

  • Marie Mirouze

    (Laboratory of Plant Genome and Development
    Laboratory of Plant Genome and Development)

Abstract

Abundant extrachromosomal circular DNA (eccDNA) is associated with transposable element (TE) activity. However, how the eccDNA compartment is controlled by epigenetic regulations and what is its impact on the genome is understudied. Here, using long reads, we sequence both the eccDNA compartment and the genome of Arabidopsis thaliana mutant plants affected in DNA methylation and post-transcriptional gene silencing. We detect a high load of TE-derived eccDNA with truncated and chimeric forms. On the genomic side, on top of truncated and full length TE neo-insertions, we detect complex structural variations (SVs) notably at a disease resistance cluster being a natural hotspot of SV. Finally, we serendipitously identify large tandem duplications in hypomethylated plants, suggesting that SVs could have been overlooked in epigenetic mutants. We propose that a high eccDNA load may alter DNA repair pathways leading to genome instability and the accumulation of SVs, at least in plants.

Suggested Citation

  • Panpan Zhang & Assane Mbodj & Abirami Soundiramourtty & Christel Llauro & Alain Ghesquière & Mathieu Ingouff & R. Keith Slotkin & Frédéric Pontvianne & Marco Catoni & Marie Mirouze, 2023. "Extrachromosomal circular DNA and structural variants highlight genome instability in Arabidopsis epigenetic mutants," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41023-0
    DOI: 10.1038/s41467-023-41023-0
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    References listed on IDEAS

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    1. Yuangao Wang & Meng Wang & Mohamed Nadhir Djekidel & Huan Chen & Di Liu & Frederick W. Alt & Yi Zhang, 2021. "eccDNAs are apoptotic products with high innate immunostimulatory activity," Nature, Nature, vol. 599(7884), pages 308-314, November.
    2. Diego H. Sanchez & Hervé Gaubert & Hajk-Georg Drost & Nicolae Radu Zabet & Jerzy Paszkowski, 2017. "High-frequency recombination between members of an LTR retrotransposon family during transposition bursts," Nature Communications, Nature, vol. 8(1), pages 1-7, December.
    3. Marie Mirouze & Jon Reinders & Etienne Bucher & Taisuke Nishimura & Korbinian Schneeberger & Stephan Ossowski & Jun Cao & Detlef Weigel & Jerzy Paszkowski & Olivier Mathieu, 2009. "Selective epigenetic control of retrotransposition in Arabidopsis," Nature, Nature, vol. 461(7262), pages 427-430, September.
    4. J. A. Kamp & R. Schendel & I. W. Dilweg & M. Tijsterman, 2020. "BRCA1-associated structural variations are a consequence of polymerase theta-mediated end-joining," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    5. Agnès Thierry & Varun Khanna & Sophie Créno & Ingrid Lafontaine & Laurence Ma & Christiane Bouchier & Bernard Dujon, 2015. "Macrotene chromosomes provide insights to a new mechanism of high-order gene amplification in eukaryotes," Nature Communications, Nature, vol. 6(1), pages 1-12, May.
    6. Fu Yang & Weijia Su & Oliver W. Chung & Lauren Tracy & Lu Wang & Dale A. Ramsden & ZZ Zhao Zhang, 2023. "Retrotransposons hijack alt-EJ for DNA replication and eccDNA biogenesis," Nature, Nature, vol. 620(7972), pages 218-225, August.
    7. Keith Durkin & Wouter Coppieters & Cord Drögemüller & Naima Ahariz & Nadine Cambisano & Tom Druet & Corinne Fasquelle & Aynalem Haile & Petr Horin & Lusheng Huang & Yohichiro Kamatani & Latifa Karim &, 2012. "Serial translocation by means of circular intermediates underlies colour sidedness in cattle," Nature, Nature, vol. 482(7383), pages 81-84, February.
    8. Sayuri Tsukahara & Akie Kobayashi & Akira Kawabe & Olivier Mathieu & Asuka Miura & Tetsuji Kakutani, 2009. "Bursts of retrotransposition reproduced in Arabidopsis," Nature, Nature, vol. 461(7262), pages 423-426, September.
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    1. Jundong Zhuang & Yaoxin Zhang & Congcong Zhou & Danlin Fan & Tao Huang & Qi Feng & Yiqi Lu & Yan Zhao & Qiang Zhao & Bin Han & Tingting Lu, 2024. "Dynamics of extrachromosomal circular DNA in rice," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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