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.

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

  • 3,046
    views
  • 447
    downloads
  • 36
    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. Chromosomes and Gene Expression
    2. Genetics and Genomics
    Hans Tobias Gustafsson, Lucas Ferguson ... Oliver J Rando
    Research Article

    Among the major classes of RNAs in the cell, tRNAs remain the most difficult to characterize via deep sequencing approaches, as tRNA structure and nucleotide modifications can each interfere with cDNA synthesis by commonly-used reverse transcriptases (RTs). Here, we benchmark a recently-developed RNA cloning protocol, termed Ordered Two-Template Relay (OTTR), to characterize intact tRNAs and tRNA fragments in budding yeast and in mouse tissues. We show that OTTR successfully captures both full-length tRNAs and tRNA fragments in budding yeast and in mouse reproductive tissues without any prior enzymatic treatment, and that tRNA cloning efficiency can be further enhanced via AlkB-mediated demethylation of modified nucleotides. As with other recent tRNA cloning protocols, we find that a subset of nucleotide modifications leave misincorporation signatures in OTTR datasets, enabling their detection without any additional protocol steps. Focusing on tRNA cleavage products, we compare OTTR with several standard small RNA-Seq protocols, finding that OTTR provides the most accurate picture of tRNA fragment levels by comparison to "ground truth" Northern blots. Applying this protocol to mature mouse spermatozoa, our data dramatically alter our understanding of the small RNA cargo of mature mammalian sperm, revealing a far more complex population of tRNA fragments - including both 5′ and 3′ tRNA halves derived from the majority of tRNAs – than previously appreciated. Taken together, our data confirm the superior performance of OTTR to commercial protocols in analysis of tRNA fragments, and force a reappraisal of potential epigenetic functions of the sperm small RNA payload.

    1. Chromosomes and Gene Expression
    Ashwin Govindan, Nicholas K Conrad
    Research Article

    O-GlcNAcylation is the reversible post-translational addition of β-N-acetylglucosamine to serine and threonine residues of nuclear and cytoplasmic proteins. It plays an important role in several cellular processes through the modification of thousands of protein substrates. O-GlcNAcylation in humans is mediated by a single essential enzyme, O-GlcNAc transferase (OGT). OGT, together with the sole O-GlcNAcase OGA, form an intricate feedback loop to maintain O-GlcNAc homeostasis in response to changes in cellular O-GlcNAc using a dynamic mechanism involving nuclear retention of its fourth intron. However, the molecular mechanism of this dynamic regulation remains unclear. Using an O-GlcNAc responsive GFP reporter cell line, we identify SFSWAP, a poorly characterized splicing factor, as a trans-acting factor regulating OGT intron detention. We show that SFSWAP is a global regulator of retained intron splicing and exon skipping that primarily acts as a negative regulator of splicing. In contrast, knockdown of SFSWAP leads to reduced inclusion of a ‘decoy exon’ present in the OGT retained intron which may mediate its role in OGT intron detention. Global analysis of decoy exon inclusion in SFSWAP and UPF1 double knockdown cells indicate altered patterns of decoy exon usage. Together, these data indicate a role for SFSWAP as a global negative regulator of pre-mRNA splicing and positive regulator of intron retention.