Natural variation in autumn expression is the major adaptive determinant distinguishing Arabidopsis FLC haplotypes

  1. Jo Hepworth
  2. Rea L Antoniou-Kourounioti
  3. Kristina Berggren
  4. Catja Selga
  5. Eleri H Tudor
  6. Bryony Yates
  7. Deborah Cox
  8. Barley Rose Collier Harris
  9. Judith A Irwin
  10. Martin Howard
  11. Torbjörn Säll
  12. Svante Holm  Is a corresponding author
  13. Caroline Dean  Is a corresponding author
  1. John Innes Centre, United Kingdom
  2. Mid Sweden University, Sweden
  3. Swedish University of Agricultural Sciences, Sweden
  4. University of Oxford, United Kingdom
  5. Lund University, Sweden
  6. Mid-Sweden University, Sweden

Abstract

In Arabidopsis thaliana, winter is registered during vernalization through the temperature-dependent repression and epigenetic silencing of floral repressor FLOWERING LOCUS C (FLC). Natural Arabidopsis accessions show considerable variation in vernalization. However, which aspect of the FLC repression mechanism is most important for adaptation to different environments is unclear. By analyzing FLC dynamics in natural variants and mutants throughout winter in three field sites, we find that autumnal FLC expression, rather than epigenetic silencing, is the major variable conferred by the distinct Arabidopsis FLC haplotypes. This variation influences flowering responses of Arabidopsis accessions resulting in an interplay between promotion and delay of flowering in different climates to balance survival and, through a post-vernalization effect, reproductive output. These data reveal how expression variation through non-coding cis variation at FLC has enabled Arabidopsis accessions to adapt to different climatic conditions and year-on-year fluctuations.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.

Article and author information

Author details

  1. Jo Hepworth

    Crop Genetics, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4621-8414
  2. Rea L Antoniou-Kourounioti

    Computational and Systems Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Kristina Berggren

    Department of Natural Sciences, Mid Sweden University, Sundsvall, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7859-9928
  4. Catja Selga

    Department of Plant Breeding, Swedish University of Agricultural Sciences, Alnarp, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8683-1291
  5. Eleri H Tudor

    Crop Genetics, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Bryony Yates

    Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Deborah Cox

    Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Barley Rose Collier Harris

    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5745-1812
  9. Judith A Irwin

    Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Martin Howard

    Computational and Systems Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7670-0781
  11. Torbjörn Säll

    Department of Biology, Lund University, Lund, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  12. Svante Holm

    Mid-Sweden University, Sundsvall, Sweden
    For correspondence
    Svante.Holm@miun.se
    Competing interests
    The authors declare that no competing interests exist.
  13. Caroline Dean

    Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    For correspondence
    caroline.dean@jic.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6555-3525

Funding

Horizon 2020 Framework Programme (MEXTIM)

  • Jo Hepworth
  • Rea L Antoniou-Kourounioti
  • Kristina Berggren
  • Catja Selga
  • Eleri H Tudor
  • Deborah Cox
  • Barley Rose Collier Harris
  • Judith A Irwin
  • Martin Howard
  • Torbjörn Säll
  • Svante Holm
  • Caroline Dean

Biotechnology and Biological Sciences Research Council (BB/J004588/1)

  • Jo Hepworth
  • Rea L Antoniou-Kourounioti
  • Eleri H Tudor
  • Deborah Cox
  • Barley Rose Collier Harris
  • Judith A Irwin
  • Martin Howard
  • Caroline Dean

Biotechnology and Biological Sciences Research Council (BB/P013511/1)

  • Jo Hepworth
  • Rea L Antoniou-Kourounioti
  • Eleri H Tudor
  • Bryony Yates
  • Deborah Cox
  • Barley Rose Collier Harris
  • Judith A Irwin
  • Martin Howard
  • Caroline Dean

Biotechnology and Biological Sciences Research Council (BB/P003095/1)

  • Jo Hepworth
  • Eleri H Tudor
  • Judith A Irwin

Biotechnology and Biological Sciences Research Council (BB/L016079/1)

  • Eleri H Tudor

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

Reviewing Editor

  1. Hao Yu, National University of Singapore & Temasek Life Sciences Laboratory, Singapore

Version history

  1. Received: April 8, 2020
  2. Accepted: September 8, 2020
  3. Accepted Manuscript published: September 9, 2020 (version 1)
  4. Version of Record published: September 25, 2020 (version 2)

Copyright

© 2020, Hepworth 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

  • 2,839
    views
  • 423
    downloads
  • 30
    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. Jo Hepworth
  2. Rea L Antoniou-Kourounioti
  3. Kristina Berggren
  4. Catja Selga
  5. Eleri H Tudor
  6. Bryony Yates
  7. Deborah Cox
  8. Barley Rose Collier Harris
  9. Judith A Irwin
  10. Martin Howard
  11. Torbjörn Säll
  12. Svante Holm
  13. Caroline Dean
(2020)
Natural variation in autumn expression is the major adaptive determinant distinguishing Arabidopsis FLC haplotypes
eLife 9:e57671.
https://doi.org/10.7554/eLife.57671

Share this article

https://doi.org/10.7554/eLife.57671

Further reading

    1. Biochemistry and Chemical Biology
    2. Chromosomes and Gene Expression
    Ramona Weber, Chung-Te Chang
    Research Article

    Recent findings indicate that the translation elongation rate influences mRNA stability. One of the factors that has been implicated in this link between mRNA decay and translation speed is the yeast DEAD-box helicase Dhh1p. Here, we demonstrated that the human ortholog of Dhh1p, DDX6, triggers the deadenylation-dependent decay of inefficiently translated mRNAs in human cells. DDX6 interacts with the ribosome through the Phe-Asp-Phe (FDF) motif in its RecA2 domain. Furthermore, RecA2-mediated interactions and ATPase activity are both required for DDX6 to destabilize inefficiently translated mRNAs. Using ribosome profiling and RNA sequencing, we identified two classes of endogenous mRNAs that are regulated in a DDX6-dependent manner. The identified targets are either translationally regulated or regulated at the steady-state-level and either exhibit signatures of poor overall translation or of locally reduced ribosome translocation rates. Transferring the identified sequence stretches into a reporter mRNA caused translation- and DDX6-dependent degradation of the reporter mRNA. In summary, these results identify DDX6 as a crucial regulator of mRNA translation and decay triggered by slow ribosome movement and provide insights into the mechanism by which DDX6 destabilizes inefficiently translated mRNAs.

    1. Chromosomes and Gene Expression
    Marwan Anoud, Emmanuelle Delagoutte ... Jean-Paul Concordet
    Research Article

    Tardigrades are microscopic animals renowned for their ability to withstand extreme conditions, including high doses of ionizing radiation (IR). To better understand their radio-resistance, we first characterized induction and repair of DNA double- and single-strand breaks after exposure to IR in the model species Hypsibius exemplaris. Importantly, we found that the rate of single-strand breaks induced was roughly equivalent to that in human cells, suggesting that DNA repair plays a predominant role in tardigrades’ radio-resistance. To identify novel tardigrade-specific genes involved, we next conducted a comparative transcriptomics analysis across three different species. In all three species, many DNA repair genes were among the most strongly overexpressed genes alongside a novel tardigrade-specific gene, which we named Tardigrade DNA damage Response 1 (TDR1). We found that TDR1 protein interacts with DNA and forms aggregates at high concentration suggesting it may condensate DNA and preserve chromosome organization until DNA repair is accomplished. Remarkably, when expressed in human cells, TDR1 improved resistance to Bleomycin, a radiomimetic drug. Based on these findings, we propose that TDR1 is a novel tardigrade-specific gene conferring resistance to IR. Our study sheds light on mechanisms of DNA repair helping cope with high levels of DNA damage inflicted by IR.