A novel form of bivalent chromatin associates with rapid induction of camalexin biosynthesis genes in response to a pathogen signal in Arabidopsis

  1. Kangmei Zhao
  2. Deze Kong
  3. Benjamin Jin
  4. Christina D Smolke
  5. Seung Yon Rhee  Is a corresponding author
  1. Carnegie Institution for Science, United States
  2. Stanford University, United States

Abstract

Temporal dynamics of gene expression underpin responses to internal and environmental stimuli. In eukaryotes, regulation of gene induction includes changing chromatin states at target genes and recruiting the transcriptional machinery that includes transcription factors. As one of the most potent defense compounds in Arabidopsis thaliana, camalexin can be rapidly induced by bacterial and fungal infections. Though several transcription factors controlling camalexin biosynthesis genes have been characterized, how the rapid activation of genes in this pathway upon a pathogen signal is enabled remains unknown. By combining publicly available epigenomic data with in vivo chromatin modification mapping, we found that camalexin biosynthesis genes are marked with two epigenetic modifications with opposite effects on gene expression, H3K27me3 (repression) and H3K18ac (activation), to form a previously uncharacterized type of bivalent chromatin. Mutants with reduced H3K27m3 or H3K18ac suggested that both modifications were required to determine the timing of gene expression and metabolite accumulation at an early stage of the stress response. Our study indicates that the H3K27me3-H3K18ac bivalent chromatin, which we name a kairostat, plays an important role controlling the timely induction of gene expression upon stimuli in plants.

Data availability

The data that support the findings of this study are available within the article and its supplementary information files. Arabidopsis metabolic genes and pathways are available at Plant Metabolic Network (https://plantcyc.org/).

Article and author information

Author details

  1. Kangmei Zhao

    Carnegie Institution for Science, Palo Alto, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1472-4993
  2. Deze Kong

    Stanford University, Palo Alto, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4334-5888
  3. Benjamin Jin

    Carnegie Institution for Science, Palo Alto, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Christina D Smolke

    Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5449-8495
  5. Seung Yon Rhee

    Department of Plant Biology, Carnegie Institution for Science, Stanford, United States
    For correspondence
    srhee@CarnegieScience.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7572-4762

Funding

National Science Foundation (IOS-1546838 and IOS-1026003)

  • Kangmei Zhao
  • Benjamin Jin
  • Seung Yon Rhee

National Institute for Health Research (1U01GM110699-01A1)

  • Kangmei Zhao
  • Deze Kong
  • Christina D Smolke
  • Seung Yon Rhee

U.S. Department of Energy (DE-SC0018277,DE-SC0008769,DE-SC0020366)

  • Kangmei Zhao
  • Seung Yon Rhee

Carnegie Institution for Science (Endowment)

  • Kangmei Zhao
  • Benjamin Jin
  • Seung Yon Rhee

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Nicola J Patron, The Earlham Institute, United Kingdom

Version history

  1. Received: April 17, 2021
  2. Accepted: September 14, 2021
  3. Accepted Manuscript published: September 15, 2021 (version 1)
  4. Version of Record published: October 26, 2021 (version 2)

Copyright

© 2021, Zhao et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Kangmei Zhao
  2. Deze Kong
  3. Benjamin Jin
  4. Christina D Smolke
  5. Seung Yon Rhee
(2021)
A novel form of bivalent chromatin associates with rapid induction of camalexin biosynthesis genes in response to a pathogen signal in Arabidopsis
eLife 10:e69508.
https://doi.org/10.7554/eLife.69508

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https://doi.org/10.7554/eLife.69508

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