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Epigenetic modifications affect the rate of spontaneous mutations in a pathogenic fungus

Author

Listed:
  • Michael Habig

    (Environmental Genomics, Christian-Albrechts University of Kiel
    Max Planck Institute for Evolutionary Biology)

  • Cecile Lorrain

    (Environmental Genomics, Christian-Albrechts University of Kiel
    Max Planck Institute for Evolutionary Biology)

  • Alice Feurtey

    (Environmental Genomics, Christian-Albrechts University of Kiel
    Max Planck Institute for Evolutionary Biology)

  • Jovan Komluski

    (Environmental Genomics, Christian-Albrechts University of Kiel
    Max Planck Institute for Evolutionary Biology)

  • Eva H. Stukenbrock

    (Environmental Genomics, Christian-Albrechts University of Kiel
    Max Planck Institute for Evolutionary Biology)

Abstract

Mutations are the source of genetic variation and the substrate for evolution. Genome-wide mutation rates appear to be affected by selection and are probably adaptive. Mutation rates are also known to vary along genomes, possibly in response to epigenetic modifications, but causality is only assumed. In this study we determine the direct impact of epigenetic modifications and temperature stress on mitotic mutation rates in a fungal pathogen using a mutation accumulation approach. Deletion mutants lacking epigenetic modifications confirm that histone mark H3K27me3 increases whereas H3K9me3 decreases the mutation rate. Furthermore, cytosine methylation in transposable elements (TE) increases the mutation rate 15-fold resulting in significantly less TE mobilization. Also accessory chromosomes have significantly higher mutation rates. Finally, we find that temperature stress substantially elevates the mutation rate. Taken together, we find that epigenetic modifications and environmental conditions modify the rate and the location of spontaneous mutations in the genome and alter its evolutionary trajectory.

Suggested Citation

  • Michael Habig & Cecile Lorrain & Alice Feurtey & Jovan Komluski & Eva H. Stukenbrock, 2021. "Epigenetic modifications affect the rate of spontaneous mutations in a pathogenic fungus," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26108-y
    DOI: 10.1038/s41467-021-26108-y
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    References listed on IDEAS

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    1. Cai Li & Nicholas M. Luscombe, 2020. "Nucleosome positioning stability is a modulator of germline mutation rate variation across the human genome," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Li-Jun Ma & H. Charlotte van der Does & Katherine A. Borkovich & Jeffrey J. Coleman & Marie-Josée Daboussi & Antonio Di Pietro & Marie Dufresne & Michael Freitag & Manfred Grabherr & Bernard Henrissat, 2010. "Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium," Nature, Nature, vol. 464(7287), pages 367-373, March.
    3. Benjamin Schuster-Böckler & Ben Lehner, 2012. "Chromatin organization is a major influence on regional mutation rates in human cancer cells," Nature, Nature, vol. 488(7412), pages 504-507, August.
    4. Radhakrishnan Sabarinathan & Loris Mularoni & Jordi Deu-Pons & Abel Gonzalez-Perez & Núria López-Bigas, 2016. "Nucleotide excision repair is impaired by binding of transcription factors to DNA," Nature, Nature, vol. 532(7598), pages 264-267, April.
    5. Paul D. Sniegowski & Philip J. Gerrish & Richard E. Lenski, 1997. "Evolution of high mutation rates in experimental populations of E. coli," Nature, Nature, vol. 387(6634), pages 703-705, June.
    6. Paz Polak & Rosa Karlić & Amnon Koren & Robert Thurman & Richard Sandstrom & Michael S. Lawrence & Alex Reynolds & Eric Rynes & Kristian Vlahoviček & John A. Stamatoyannopoulos & Shamil R. Sunyaev, 2015. "Cell-of-origin chromatin organization shapes the mutational landscape of cancer," Nature, Nature, vol. 518(7539), pages 360-364, February.
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