Genomic basis for drought resistance in European beech forests threatened by climate change

  1. Markus Pfenninger  Is a corresponding author
  2. Friederike Reuss
  3. Angelika KIebler
  4. Philipp Schönnenbeck
  5. Cosima Caliendo
  6. Susanne Gerber
  7. Berardino Cocchiararo
  8. Sabrina Reuter
  9. Nico Blüthgen
  10. Karsten Mody
  11. Bagdevi Mishra
  12. Miklós Bálint
  13. Marco Thines
  14. Barbara Feldmeyer
  1. Senckenberg Biodiversity and Climate Research Centre, Germany
  2. Institute for Human Genetics, University Medical Center, Johannes Gutenberg University, Germany
  3. Senckenberg Research Institute and Natural History Museum, Germany
  4. Department of Biology, Technische Universität Darmstadt, Germany
  5. Hochschule Geisenheim University, Germany
  6. Biodiversity and Climate Research Centre, Germany
  7. LOEWE Centre for Translational Biodiversity Genomics, Germany
  8. Senckenberg Gesellschaft für Naturforschung, Germany

Abstract

In the course of global climate change, central Europe is experiencing more frequent and prolonged periods of drought. The drought years 2018 and 2019 affected European beeches (Fagus sylvatica L.) differently: even in the same stand, drought damaged trees neighboured healthy trees, suggesting that the genotype rather than the environment was responsible for this conspicuous pattern. We used this natural experiment to study the genomic basis of drought resistance with Pool-GWAS. Contrasting the extreme phenotypes identified 106 significantly associated SNPs throughout the genome. Most annotated genes with associated SNPs (>70%) were previously implicated in the drought reaction of plants. Non-synonymous substitutions led either to a functional amino acid exchange or premature termination. A SNP-assay with 70 loci allowed predicting drought phenotype in 98.6% of a validation sample of 92 trees. Drought resistance in European beech is a moderately polygenic trait that should respond well to natural selection, selective management, and breeding.

Data availability

Sequencing data have been deposited at ENA under project code PRJEB41889.The genome assembly including the annotation is available under the Access. No. PRJNA450822.

The following data sets were generated

Article and author information

Author details

  1. Markus Pfenninger

    Molecular Ecology, Senckenberg Biodiversity and Climate Research Centre, Frankfurt am Main, Germany
    For correspondence
    Markus.Pfenninger@senckenberg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1547-7245
  2. Friederike Reuss

    Molecular Ecology, Senckenberg Biodiversity and Climate Research Centre, Frankfurt am Main, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Angelika KIebler

    Molecular Ecology, Senckenberg Biodiversity and Climate Research Centre, Frankfurt am Main, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Philipp Schönnenbeck

    n/a, Institute for Human Genetics, University Medical Center, Johannes Gutenberg University, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Cosima Caliendo

    n/a, Institute for Human Genetics, University Medical Center, Johannes Gutenberg University, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Susanne Gerber

    n/a, Institute for Human Genetics, University Medical Center, Johannes Gutenberg University, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Berardino Cocchiararo

    Conservation Genetics Section, Senckenberg Research Institute and Natural History Museum, Gelnhausen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Sabrina Reuter

    Ecological Networks lab, Department of Biology, Technische Universität Darmstadt, Darmstadt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Nico Blüthgen

    Ecological Networks lab, Department of Biology, Technische Universität Darmstadt, Darmstadt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Karsten Mody

    Department of Applied Ecology, Hochschule Geisenheim University, Geisenheim, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Bagdevi Mishra

    n/a, Biodiversity and Climate Research Centre, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Miklós Bálint

    Functional Environmental Genomics, LOEWE Centre for Translational Biodiversity Genomics, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Marco Thines

    Biodiversity and Climate Research Centre, Senckenberg Gesellschaft für Naturforschung, Frankfurt (Main), Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Barbara Feldmeyer

    Molecular Ecology, Senckenberg Biodiversity and Climate Research Centre, Frankfurt am Main, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

There was no particular funding for this work; all work was financed by regular budgets

Copyright

© 2021, Pfenninger 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

  • 3,790
    views
  • 577
    downloads
  • 41
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

Share this article

https://doi.org/10.7554/eLife.65532

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Martina Rudgalvyte, Zehan Hu ... Dominique A Glauser
    Research Article

    Thermal nociception in Caenorhabditis elegans is regulated by the Ca²+/calmodulin-dependent protein kinase CMK-1, but its downstream effectors have remained unclear. Here, we combined in vitro kinase assays with mass-spectrometry-based phosphoproteomics to identify hundreds of CMK-1 substrates, including the calcineurin A subunit TAX-6, phosphorylated within its conserved regulatory domain. Genetic and pharmacological analyses reveal multiple antagonistic interactions between CMK-1 and calcineurin signaling in modulating both naive thermal responsiveness and adaptation to repeated noxious stimuli. Cell-specific manipulations indicate that CMK-1 acts in AFD and ASER thermo-sensory neurons, while TAX-6 functions in FLP thermo-sensory neurons and downstream interneurons. Since CMK-1 and TAX-6 act in distinct cell types, the phosphorylation observed in vitro might not directly underlie the behavioral phenotype. Instead, the opposing effects seem to arise from their distributed roles within the sensory circuit. Overall, our study provides (1) a resource of candidate CMK-1 targets for further dissecting CaM kinase signaling and (2) evidence of a previously unrecognized, circuit-level antagonism between CMK-1 and calcineurin pathways. These findings highlight a complex interplay of signaling modules that modulate thermal nociception and adaptation, offering new insights into potentially conserved mechanisms that shape nociceptive plasticity and pain (de)sensitization in more complex nervous systems.