Vernalization-triggered expression of the antisense transcript COOLAIR is mediated by CBF genes

  1. Myeongjune Jeon
  2. Goowon Jeong
  3. Yupeng Yang
  4. Xiao Luo
  5. Daesong Jeong
  6. Jinseul Kyung
  7. Youbong Hyun
  8. Yuehui He  Is a corresponding author
  9. Ilha Lee  Is a corresponding author
  1. Seoul National University, Republic of Korea
  2. Chinese Academy of Sciences, Japan
  3. Peking University Institute of Advanced Agricultural Sciences, China
  4. Chinese Academy of Sciences, China

Abstract

To synchronize flowering time with spring, many plants undergo vernalization, a floral-promotion process triggered by exposure to long-term winter cold. In Arabidopsis thaliana, this is achieved through cold-mediated epigenetic silencing of the floral repressor, FLOWERING LOCUS C (FLC). COOLAIR, a cold-induced antisense RNA transcribed from the FLC locus, has been proposed to facilitate FLC silencing. Here, we show that C-repeat (CRT)/dehydration-responsive elements (DREs) at the 3′-end of FLC and CRT/DRE-binding factors (CBFs) are required for cold-mediated expression of COOLAIR. CBFs bind to CRT/DREs at the 3′-end of FLC, both in vitro and in vivo, and CBF levels increase gradually during vernalization. Cold-induced COOLAIR expression is severely impaired in cbfs mutants in which all CBF genes are knocked-out. Conversely, CBF-overexpressing plants show increased COOLAIR levels even at warm temperatures. We show that COOLAIR is induced by CBFs during early stages of vernalization but COOLAIR levels decrease in later phases as FLC chromatin transitions to an inactive state to which CBFs can no longer bind. We also demonstrate that cbfs and FLCΔCOOLAIR mutants exhibit a normal vernalization response despite their inability to activate COOLAIR expression during cold, revealing that COOLAIR is not required for the vernalization process.

Data availability

No new data have been generated for this manuscript. Previously published datasets used for this study are deposited in NCBI, under BioProject accession codes PRJNA416120 and PRJNA732005.

The following previously published data sets were used

Article and author information

Author details

  1. Myeongjune Jeon

    School of Biological Sciences, Seoul National University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9195-1810
  2. Goowon Jeong

    School of Biological Sciences, Seoul National University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5023-920X
  3. Yupeng Yang

    Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Xiao Luo

    Peking University Institute of Advanced Agricultural Sciences, Weifang, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Daesong Jeong

    School of Biological Sciences, Seoul National University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  6. Jinseul Kyung

    School of Biological Sciences, Seoul National University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  7. Youbong Hyun

    School of Biological Sciences, Seoul National University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  8. Yuehui He

    Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanhai, China
    For correspondence
    yhhe@pku.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  9. Ilha Lee

    School of Biological Sciences, Seoul National University, Seoul, Republic of Korea
    For correspondence
    ilhalee@snu.ac.kr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3516-4326

Funding

National Research Foundation of Korea (2019R1A2C2004313)

  • Ilha Lee

National Research Foundation of Korea (2022R1A2C1091491)

  • Ilha Lee

National Natural Science Foundation of China (31830049)

  • Yuehui He

National Natural Science Foundation of China (31721001)

  • Yuehui He

National Research Foundation of Korea (2021R1A5A1032428)

  • Ilha Lee

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

Reviewing Editor

  1. Richard Amasino, University of Wisconsin Madison, United States

Version history

  1. Preprint posted: October 9, 2021 (view preprint)
  2. Received: October 31, 2022
  3. Accepted: January 31, 2023
  4. Accepted Manuscript published: February 1, 2023 (version 1)
  5. Accepted Manuscript updated: February 7, 2023 (version 2)
  6. Version of Record published: March 23, 2023 (version 3)

Copyright

© 2023, Jeon 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. Myeongjune Jeon
  2. Goowon Jeong
  3. Yupeng Yang
  4. Xiao Luo
  5. Daesong Jeong
  6. Jinseul Kyung
  7. Youbong Hyun
  8. Yuehui He
  9. Ilha Lee
(2023)
Vernalization-triggered expression of the antisense transcript COOLAIR is mediated by CBF genes
eLife 12:e84594.
https://doi.org/10.7554/eLife.84594

Share this article

https://doi.org/10.7554/eLife.84594

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