Repeated origins, widespread gene flow, and allelic interactions of target-site herbicide resistance mutations

  1. Julia M Kreiner  Is a corresponding author
  2. George Sandler
  3. Aaron J Stern
  4. Patrick J Tranel
  5. Detlef Weigel
  6. John Stinchcombe
  7. Stephen Isaac Wright
  1. University of Toronto, Canada
  2. University of California, Berkeley, United States
  3. University of Illinois Urbana-Champaign, United States
  4. Max Planck Institute for Developmental Biology, Germany

Abstract

Causal mutations and their frequency in agricultural fields are well-characterized for herbicide resistance. However, we still lack understanding of their evolutionary history: the extent of parallelism in the origins of target-site resistance (TSR), how long these mutations persist, how quickly they spread, and allelic interactions that mediate their selective advantage. We addressed these questions with genomic data from 18 agricultural populations of common waterhemp (Amaranthus tuberculatus), which we show to have undergone a massive expansion over the past century, with a contemporary effective population size (Ne) estimate of 8x107. We found variation at seven characterized TSR loci, two of which had multiple amino acid substitutions, and three of which were common. These three common resistance variants show parallelism in their mutational origins, with gene flow having shaped their distribution across the landscape. Allele age estimates supported a strong role of adaptation from de novo mutations, with a median allele age of 30 suggesting that most resistance alleles arose soon after the onset of herbicide use. However, resistant lineages varied in both their age and evidence for selection over two different timescales, implying considerable heterogeneity in the forces that govern their persistence. The evolutionary history of TSR has also been shaped by both intra- and inter-locus allelic interactions. We report a signal of extended haplotype competition between two common TSR alleles, and extreme linkage with genome-wide alleles with known functions in resistance adaptation. Together, this work reveals a remarkable example of spatial parallel evolution in a metapopulation, with important implications for the management of herbicide resistance.

Data availability

Sequencing data used in this paper were previously deposited in ENA under project number PRJEB31711, and reference genome is available on CoGe (reference ID = 54057). Code used to generate results in this paper is available at https://github.com/jkreinz/TSRevolution.

The following previously published data sets were used

Article and author information

Author details

  1. Julia M Kreiner

    Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada
    For correspondence
    julia.kreiner@mail.utoronto.ca
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8593-1394
  2. George Sandler

    Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada
    Competing interests
    No competing interests declared.
  3. Aaron J Stern

    Graduate Group in Computational Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  4. Patrick J Tranel

    Department of Crop Sciences, University of Illinois Urbana-Champaign, Urbana, United States
    Competing interests
    No competing interests declared.
  5. Detlef Weigel

    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    Detlef Weigel, Deputy editor of eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2114-7963
  6. John Stinchcombe

    Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3349-2964
  7. Stephen Isaac Wright

    Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada
    Competing interests
    No competing interests declared.

Funding

Natural Sciences and Engineering Research Council of Canada (PGS-D)

  • Julia M Kreiner

Society for the Study of Evolution (Rosemary Grant Advanced Award)

  • Julia M Kreiner

Natural Sciences and Engineering Research Council of Canada (Discovery Grant)

  • John Stinchcombe
  • Stephen Isaac Wright

Canada Research Chairs (Population Genomics)

  • Stephen Isaac Wright

Max Planck Institute for Dynamics of Complex Technical Systems Magdeburg

  • Detlef Weigel

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

Reviewing Editor

  1. Philipp W Messer, Cornell University, United States

Publication history

  1. Preprint posted: May 10, 2021 (view preprint)
  2. Received: May 11, 2021
  3. Accepted: January 16, 2022
  4. Accepted Manuscript published: January 17, 2022 (version 1)
  5. Version of Record published: January 28, 2022 (version 2)

Copyright

© 2022, Kreiner 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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  1. Julia M Kreiner
  2. George Sandler
  3. Aaron J Stern
  4. Patrick J Tranel
  5. Detlef Weigel
  6. John Stinchcombe
  7. Stephen Isaac Wright
(2022)
Repeated origins, widespread gene flow, and allelic interactions of target-site herbicide resistance mutations
eLife 11:e70242.
https://doi.org/10.7554/eLife.70242

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