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Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form

Author

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  • Michael S. Werner

    (Max Planck Institute for Biology Tübingen
    The University of Utah)

  • Tobias Loschko

    (Max Planck Institute for Biology Tübingen)

  • Thomas King

    (The University of Utah)

  • Shelley Reich

    (The University of Utah)

  • Tobias Theska

    (Max Planck Institute for Biology Tübingen)

  • Mirita Franz-Wachtel

    (University of Tübingen)

  • Boris Macek

    (University of Tübingen)

  • Ralf J. Sommer

    (Max Planck Institute for Biology Tübingen)

Abstract

Development can be altered to match phenotypes with the environment, and the genetic mechanisms that direct such alternative phenotypes are beginning to be elucidated. Yet, the rules that govern environmental sensitivity vs. invariant development, and potential epigenetic memory, remain unknown. Here, we show that plasticity of nematode mouth forms is determined by histone 4 lysine 5 and 12 acetylation (H4K5/12ac). Acetylation in early larval stages provides a permissive chromatin state, which is susceptible to induction during the critical window of environmental sensitivity. As development proceeds deacetylation shuts off switch gene expression to end the critical period. Inhibiting deacetylase enzymes leads to fixation of prior developmental trajectories, demonstrating that histone modifications in juveniles can carry environmental information to adults. Finally, we provide evidence that this regulation was derived from an ancient mechanism of licensing developmental speed. Altogether, our results show that H4K5/12ac enables epigenetic regulation of developmental plasticity that can be stored and erased by acetylation and deacetylation, respectively.

Suggested Citation

  • Michael S. Werner & Tobias Loschko & Thomas King & Shelley Reich & Tobias Theska & Mirita Franz-Wachtel & Boris Macek & Ralf J. Sommer, 2023. "Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37734-z
    DOI: 10.1038/s41467-023-37734-z
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    References listed on IDEAS

    as
    1. Linh T. Bui & Nicholas A. Ivers & Erik J. Ragsdale, 2018. "Author Correction: A sulfotransferase dosage-dependently regulates mouthpart polyphenism in the nematode Pristionchus pacificus," Nature Communications, Nature, vol. 9(1), pages 1-2, December.
    2. Alvaro Rada-Iglesias & Ruchi Bajpai & Tomek Swigut & Samantha A. Brugmann & Ryan A. Flynn & Joanna Wysocka, 2011. "A unique chromatin signature uncovers early developmental enhancers in humans," Nature, Nature, vol. 470(7333), pages 279-283, February.
    3. Gilberto Bento & Akira Ogawa & Ralf J. Sommer, 2010. "Co-option of the hormone-signalling module dafachronic acid–DAF-12 in nematode evolution," Nature, Nature, vol. 466(7305), pages 494-497, July.
    4. Linh T. Bui & Nicholas A. Ivers & Erik J. Ragsdale, 2018. "A sulfotransferase dosage-dependently regulates mouthpart polyphenism in the nematode Pristionchus pacificus," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    5. Vahan Serobyan & Hua Xiao & Suryesh Namdeo & Christian Rödelsperger & Bogdan Sieriebriennikov & Hanh Witte & Waltraud Röseler & Ralf J. Sommer, 2016. "Chromatin remodelling and antisense-mediated up-regulation of the developmental switch gene eud-1 control predatory feeding plasticity," Nature Communications, Nature, vol. 7(1), pages 1-8, November.
    6. Yupeng Zheng & Paul M. Thomas & Neil L. Kelleher, 2013. "Measurement of acetylation turnover at distinct lysines in human histones identifies long-lived acetylation sites," Nature Communications, Nature, vol. 4(1), pages 1-8, October.
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