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Transposition favors the generation of large effect mutations that may facilitate rapid adaption

Author

Listed:
  • Leandro Quadrana

    (PSL Research University)

  • Mathilde Etcheverry

    (PSL Research University)

  • Arthur Gilly

    (Universite Paris-Saclay
    Wellcome Trust Sanger Institute)

  • Erwann Caillieux

    (PSL Research University)

  • Mohammed-Amin Madoui

    (Universite d’Evry, Universite Paris-Saclay)

  • Julie Guy

    (Universite Paris-Saclay)

  • Amanda Bortolini Silveira

    (PSL Research University
    PSL Research University)

  • Stefan Engelen

    (Universite Paris-Saclay)

  • Victoire Baillet

    (PSL Research University)

  • Patrick Wincker

    (Universite d’Evry, Universite Paris-Saclay)

  • Jean-Marc Aury

    (Universite Paris-Saclay)

  • Vincent Colot

    (PSL Research University)

Abstract

Transposable elements (TEs) are mobile parasitic sequences that have been repeatedly coopted during evolution to generate new functions and rewire gene regulatory networks. Yet, the contribution of active TEs to the creation of heritable mutations remains unknown. Using TE accumulation lines in Arabidopsis thaliana we show that once initiated, transposition produces an exponential spread of TE copies, which rapidly leads to high mutation rates. Most insertions occur near or within genes and targets differ between TE families. Furthermore, we uncover an essential role of the histone variant H2A.Z in the preferential integration of Ty1/copia retrotransposons within environmentally responsive genes and away from essential genes. We also show that epigenetic silencing of new Ty1/copia copies can affect their impact on major fitness-related traits, including flowering time. Our findings demonstrate that TEs are potent episodic (epi)mutagens that, thanks to marked chromatin tropisms, limit the mutation load and increase the potential for rapid adaptation.

Suggested Citation

  • Leandro Quadrana & Mathilde Etcheverry & Arthur Gilly & Erwann Caillieux & Mohammed-Amin Madoui & Julie Guy & Amanda Bortolini Silveira & Stefan Engelen & Victoire Baillet & Patrick Wincker & Jean-Mar, 2019. "Transposition favors the generation of large effect mutations that may facilitate rapid adaption," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-11385-5
    DOI: 10.1038/s41467-019-11385-5
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    Cited by:

    1. Hanne De Kort & Sylvain Legrand & Olivier Honnay & James Buckley, 2022. "Transposable elements maintain genome-wide heterozygosity in inbred populations," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Minghui Kang & Haolin Wu & Huanhuan Liu & Wenyu Liu & Mingjia Zhu & Yu Han & Wei Liu & Chunlin Chen & Yan Song & Luna Tan & Kangqun Yin & Yusen Zhao & Zhen Yan & Shangling Lou & Yanjun Zan & Jianquan , 2023. "The pan-genome and local adaptation of Arabidopsis thaliana," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Marine Duhamel & Michael E. Hood & Ricardo C. Rodríguez de la Vega & Tatiana Giraud, 2023. "Dynamics of transposable element accumulation in the non-recombining regions of mating-type chromosomes in anther-smut fungi," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Li He & Huan Huang & Mariem Bradai & Cheng Zhao & Yin You & Jun Ma & Lun Zhao & Rosa Lozano-Durán & Jian-Kang Zhu, 2022. "DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

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