1. Evolutionary Biology
  2. Genetics and Genomics
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Drought adaptation in Arabidopsis thaliana by extensive genetic loss-of-function

  1. John Grey Monroe  Is a corresponding author
  2. Tyler Powell
  3. Nicholas Price
  4. Jack L Mullen
  5. Anne Howard
  6. Kyle Evans
  7. John T Lovell
  8. John K McKay
  1. Colorado State University, United States
  2. HudsonAlpha Institute for Biotechnology, United States
Research Article
  • Cited 32
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Cite this article as: eLife 2018;7:e41038 doi: 10.7554/eLife.41038

Abstract

Interdisciplinary syntheses are needed to scale up discovery of the environmental drivers and molecular basis of adaptation in nature. Here we integrated novel approaches using whole genome sequences, satellite remote sensing, and transgenic experiments to study natural loss-of-function alleles associated with drought histories in wild Arabidopsis thaliana. The genes we identified exhibit population genetic signatures of parallel molecular evolution, selection for loss-of-function, and shared associations with flowering time phenotypes in directions consistent with longstanding adaptive hypotheses 7 times more often than expected by chance. We then confirmed predicted phenotypes experimentally in transgenic knockout lines. These findings reveal the importance of drought timing to explain the evolution of alternative drought tolerance strategies and further challenge popular assumptions about the adaptive value of genetic loss-of-function in nature. These results also motivate improved species-wide sequencing efforts to better identify loss-of-function variants and inspire new opportunities for engineering climate resilience in crops.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files.

The following previously published data sets were used
    1. Kogan F
    (1995) Vegetative Health Index
    National Oceanic and Atmospheric Administration, VHI.

Article and author information

Author details

  1. John Grey Monroe

    Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States
    For correspondence
    greymonroe@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4025-5572
  2. Tyler Powell

    Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Nicholas Price

    Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jack L Mullen

    Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Anne Howard

    Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Kyle Evans

    Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. John T Lovell

    Institute for Biotechnology, HudsonAlpha Institute for Biotechnology, Huntsville, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. John K McKay

    Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Foundation (1022196)

  • John K McKay

National Science Foundation (1556262)

  • John K McKay

National Science Foundation (1701918)

  • John Grey Monroe

U.S. Department of Agriculture (2014- 38420-21801)

  • John Grey Monroe

Cargill (Research support)

  • John K McKay

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

Reviewing Editor

  1. Daniel J Kliebenstein, University of California, Davis, United States

Publication history

  1. Received: August 12, 2018
  2. Accepted: December 6, 2018
  3. Accepted Manuscript published: December 6, 2018 (version 1)
  4. Version of Record published: January 9, 2019 (version 2)

Copyright

© 2018, Monroe 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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