Genetic variation, environment and demography intersect to shape Arabidopsis defense metabolite variation across Europe

  1. Ella Katz  Is a corresponding author
  2. Jia-Jie Li
  3. Benjamin Jaegle
  4. Haim Ashkenazy
  5. R Shawn Abrahams
  6. Clement Bagaza
  7. Samuel Holden
  8. J Chris Pires
  9. Ruthie Angelovici
  10. Daniel J Kliebenstein
  1. University of California, Davis, United States
  2. Gregor Mendel Institute, Austrian Academy of Sciences, Austria
  3. Max Planck Institute for Developmental Biology, Germany
  4. University of Missouri, United States

Abstract

Plants produce diverse metabolites to cope with the challenges presented by complex and ever-changing environments. These challenges drive the diversification of specialized metabolites within and between plant species. However, we are just beginning to understand how frequently new alleles arise controlling specialized metabolite diversity and how the geographic distribution of these alleles may be structured by ecological and demographic pressures. Here we measure the variation in specialized metabolites across a population of 797 natural Arabidopsis thaliana accessions. We show a combination of geography, environmental parameters, demography, and different genetic processes all combine to influence the specific chemotypes and their distribution. This showed that causal loci in specialized metabolism contain frequent independently generated alleles with patterns suggesting potential within species convergence. This provides a new perspective about the complexity of the selective forces and mechanisms that shape the generation and distribution of allelic variation that may influence local adaptation.

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

Article and author information

Author details

  1. Ella Katz

    Plant Sciences, University of California, Davis, Davis, United States
    For correspondence
    elkatz@ucdavis.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1619-5597
  2. Jia-Jie Li

    Plant Sciences, University of California, Davis, Davis, United States
    Competing interests
    No competing interests declared.
  3. Benjamin Jaegle

    Vienna Biocenter (VBC), Gregor Mendel Institute, Austrian Academy of Sciences, Vienna, Austria
    Competing interests
    No competing interests declared.
  4. Haim Ashkenazy

    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5079-4684
  5. R Shawn Abrahams

    Division of Biological Sciences, Bond Life Sciences Center, University of Missouri, Columbia, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1749-2040
  6. Clement Bagaza

    Division of Biological Sciences, Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, United States
    Competing interests
    No competing interests declared.
  7. Samuel Holden

    Division of Biological Sciences, University of Missouri, Columbia, United States
    Competing interests
    No competing interests declared.
  8. J Chris Pires

    Division of Biological Sciences, University of Missouri, Columbia, United States
    Competing interests
    No competing interests declared.
  9. Ruthie Angelovici

    Division of Biological Sciences, University of Missouri, Columbia, United States
    Competing interests
    No competing interests declared.
  10. Daniel J Kliebenstein

    Department of Plant Sciences, University of California, Davis, Davis, United States
    Competing interests
    Daniel J Kliebenstein, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5759-3175

Funding

National Science Foundation (MCB 1906486)

  • Daniel J Kliebenstein

United States - Israel Binational Agricultural Research and Development Fund (FI-560-2017)

  • Ella Katz
  • Daniel J Kliebenstein

National Science Foundation (IOS 1655810)

  • Daniel J Kliebenstein

National Science Foundation (IOS 1754201)

  • Ruthie Angelovici

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

Reviewing Editor

  1. Meredith C Schuman, University of Zurich, Switzerland

Version history

  1. Received: February 23, 2021
  2. Accepted: May 2, 2021
  3. Accepted Manuscript published: May 5, 2021 (version 1)
  4. Version of Record published: June 15, 2021 (version 2)

Copyright

© 2021, Katz 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

  • 3,815
    views
  • 484
    downloads
  • 33
    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. Ella Katz
  2. Jia-Jie Li
  3. Benjamin Jaegle
  4. Haim Ashkenazy
  5. R Shawn Abrahams
  6. Clement Bagaza
  7. Samuel Holden
  8. J Chris Pires
  9. Ruthie Angelovici
  10. Daniel J Kliebenstein
(2021)
Genetic variation, environment and demography intersect to shape Arabidopsis defense metabolite variation across Europe
eLife 10:e67784.
https://doi.org/10.7554/eLife.67784

Share this article

https://doi.org/10.7554/eLife.67784

Further reading

    1. Ecology
    Hao Wang, Kai He ... Chaolun Li
    Research Article

    Bathymodioline mussels dominate deep-sea methane seep and hydrothermal vent habitats and obtain nutrients and energy primarily through chemosynthetic endosymbiotic bacteria in the bacteriocytes of their gill. However, the molecular mechanisms that orchestrate mussel host–symbiont interactions remain unclear. Here, we constructed a comprehensive cell atlas of the gill in the mussel Gigantidas platifrons from the South China Sea methane seeps (1100 m depth) using single-nucleus RNA-sequencing (snRNA-seq) and whole-mount in situ hybridisation. We identified 13 types of cells, including three previously unknown ones, and uncovered unknown tissue heterogeneity. Every cell type has a designated function in supporting the gill’s structure and function, creating an optimal environment for chemosynthesis, and effectively acquiring nutrients from the endosymbiotic bacteria. Analysis of snRNA-seq of in situ transplanted mussels clearly showed the shifts in cell state in response to environmental oscillations. Our findings provide insight into the principles of host–symbiont interaction and the bivalves' environmental adaption mechanisms.

    1. Ecology
    Kim Schalcher, Estelle Milliet ... Emily LC Shepard
    Research Article

    Predator-prey arms races have led to the evolution of finely tuned disguise strategies. While the theoretical benefits of predator camouflage are well established, no study has yet been able to quantify its consequences for hunting success in natural conditions. We used high-resolution movement data to quantify how barn owls (Tyto alba) conceal their approach when using a sit-and-wait strategy. We hypothesized that hunting barn owls would modulate their landing force, potentially reducing noise levels in the vicinity of prey. Analysing 87,957 landings by 163 individuals equipped with GPS tags and accelerometers, we show that barn owls reduce their landing force as they approach their prey, and that landing force predicts the success of the following hunting attempt. Landing force also varied with the substrate, being lowest on man-made poles in field boundaries. The physical environment, therefore, affects the capacity for sound camouflage, providing an unexpected link between predator-prey interactions and land use. Finally, hunting strike forces in barn owls were the highest recorded in any bird, relative to body mass, highlighting the range of selective pressures that act on landings and the capacity of these predators to modulate their landing force. Overall, our results provide the first measurements of landing force in a wild setting, revealing a new form of motion-induced sound camouflage and its link to hunting success.