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, 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, Chinese Academy of Sciences, Shanghai, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Xiao Luo

    Institute of Advanced Agricultural Sciences, Peking University, 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, Peking University, Weifang, 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.

Metrics

  • 2,751
    views
  • 465
    downloads
  • 10
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Cell Biology
    2. Chromosomes and Gene Expression
    Lucie Crhak Khaitova, Pavlina Mikulkova ... Karel Riha
    Research Article

    Heat stress is a major threat to global crop production, and understanding its impact on plant fertility is crucial for developing climate-resilient crops. Despite the known negative effects of heat stress on plant reproduction, the underlying molecular mechanisms remain poorly understood. Here, we investigated the impact of elevated temperature on centromere structure and chromosome segregation during meiosis in Arabidopsis thaliana. Consistent with previous studies, heat stress leads to a decline in fertility and micronuclei formation in pollen mother cells. Our results reveal that elevated temperature causes a decrease in the amount of centromeric histone and the kinetochore protein BMF1 at meiotic centromeres with increasing temperature. Furthermore, we show that heat stress increases the duration of meiotic divisions and prolongs the activity of the spindle assembly checkpoint during meiosis I, indicating an impaired efficiency of the kinetochore attachments to spindle microtubules. Our analysis of mutants with reduced levels of centromeric histone suggests that weakened centromeres sensitize plants to elevated temperature, resulting in meiotic defects and reduced fertility even at moderate temperatures. These results indicate that the structure and functionality of meiotic centromeres in Arabidopsis are highly sensitive to heat stress, and suggest that centromeres and kinetochores may represent a critical bottleneck in plant adaptation to increasing temperatures.

    1. Chromosomes and Gene Expression
    Allison Coté, Aoife O'Farrell ... Arjun Raj
    Research Article

    Splicing is the stepwise molecular process by which introns are removed from pre-mRNA and exons are joined together to form mature mRNA sequences. The ordering and spatial distribution of these steps remain controversial, with opposing models suggesting splicing occurs either during or after transcription. We used single-molecule RNA FISH, expansion microscopy, and live-cell imaging to reveal the spatiotemporal distribution of nascent transcripts in mammalian cells. At super-resolution levels, we found that pre-mRNA formed clouds around the transcription site. These clouds indicate the existence of a transcription-site-proximal zone through which RNA move more slowly than in the nucleoplasm. Full-length pre-mRNA undergo continuous splicing as they move through this zone following transcription, suggesting a model in which splicing can occur post-transcriptionally but still within the proximity of the transcription site, thus seeming co-transcriptional by most assays. These results may unify conflicting reports of co-transcriptional versus post-transcriptional splicing.