Determining the scale at which variation in a single gene changes population yields

  1. Erica McGale
  2. Henrique Valim
  3. Deepika Mittal
  4. Jesús Morales Jimenez
  5. Rayko Halitschke
  6. Meredith C Schuman
  7. Ian T Baldwin  Is a corresponding author
  1. Max Planck Institute for Chemical Ecology, Germany
  2. National Institute of Plant Genome Research, India
  3. Instituto Potosino de Investigación Científica y Tecnológica A C, Mexico
  4. University of Zurich, Switzerland

Abstract

Plant trait diversity is known to influence population yield, but the scale at which this happens remains unknown: divergent individuals might change yields of immediate neighbors (neighbor scale) or of plants across a population (population scale). We use Nicotiana attenuata plants silenced in mitogen-activated protein kinase 4 (irMPK4) – with low water-use efficiency (WUE) – to study the scale at which water-use traits alter intraspecific population yields. In the field and glasshouse, we observed overyielding in populations with low percentages of irMPK4 plants, unrelated to water-use phenotypes. Paired-plant experiments excluded the occurrence of overyielding effects at the neighbor scale. Experimentally altering field arbuscular mycorrhizal fungal associations by silencing the Sym-pathway gene NaCCaMK did not affect reproductive overyielding, implicating an effect independent of belowground AMF interactions. Additionally, micro-grafting experiments revealed dependence on shoot-expressed MPK4 for N. attenuata to vary its yield per neighbor presence. We find that variation in a single-gene, MPK4, is responsible for population overyielding through a mechanism, independent of irMPK4's WUE phenotype, at the aboveground, population scale.

Data availability

The datasets used in the final fittings of our linear (LM), generlized least-squares (GLS), or linear mixed effects (LME/R) models, from which statistical significances were extracted, are included as "Source Data" files in our submission. Each Source Data file refers to the figure in which the corresponding data/results are displayed.

Article and author information

Author details

  1. Erica McGale

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5996-4213
  2. Henrique Valim

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  3. Deepika Mittal

    Plant-pathogen Interactions, National Institute of Plant Genome Research, New Delhi, India
    Competing interests
    No competing interests declared.
  4. Jesús Morales Jimenez

    CONACYT-Consorcio de Investigación Innovación y Desarrollo para las Zonas Áridas (CIIDZA), Instituto Potosino de Investigación Científica y Tecnológica A C, San Luis Potosí, Mexico
    Competing interests
    No competing interests declared.
  5. Rayko Halitschke

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1109-8782
  6. Meredith C Schuman

    University of Zurich, Zürich, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3159-3534
  7. Ian T Baldwin

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    For correspondence
    baldwin@ice.mpg.de
    Competing interests
    Ian T Baldwin, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5371-2974

Funding

Max-Planck-Gesellschaft

  • Erica McGale
  • Henrique Valim
  • Deepika Mittal
  • Jesús Morales Jimenez
  • Rayko Halitschke
  • Meredith C Schuman
  • Ian T Baldwin

European Research Council (Advanced Grant 293926)

  • Henrique Valim
  • Meredith C Schuman
  • Ian T Baldwin

iDiv

  • Erica McGale
  • Henrique Valim
  • Meredith C Schuman

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

Reviewing Editor

  1. Bernhard Schmid, University of Zurich, Switzerland

Publication history

  1. Received: November 11, 2019
  2. Accepted: February 13, 2020
  3. Accepted Manuscript published: February 14, 2020 (version 1)
  4. Version of Record published: April 6, 2020 (version 2)

Copyright

© 2020, McGale 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. Erica McGale
  2. Henrique Valim
  3. Deepika Mittal
  4. Jesús Morales Jimenez
  5. Rayko Halitschke
  6. Meredith C Schuman
  7. Ian T Baldwin
(2020)
Determining the scale at which variation in a single gene changes population yields
eLife 9:e53517.
https://doi.org/10.7554/eLife.53517
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