1. Chromosomes and Gene Expression
  2. Plant Biology
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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
Research Article
  • Cited 8
  • Views 1,984
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Cite this article as: eLife 2020;9:e57671 doi: 10.7554/eLife.57671

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

Publication 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.

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