Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maize

Abstract

The root-associated microbiome (rhizobiome) affects plant health, stress tolerance, and nutrient use efficiency. However, it remains unclear to what extent the composition of the rhizobiome is governed by intraspecific variation in host plant genetics in the field and the degree to which host plant selection can reshape the composition of the rhizobiome. Here we quantify the rhizosphere microbial communities associated with a replicated diversity panel of 230 maize (Zea mays L.) genotypes grown in agronomically relevant conditions under high N (+N) and low N (-N) treatments. We analyze the maize rhizobiome in terms of 150 abundant and consistently reproducible microbial groups and we show that the abundance of many root-associated microbes is explainable by natural genetic variation in the host plant, with a greater proportion of microbial variance attributable to plant genetic variation in -N conditions. Population genetic approaches identify signatures of purifying selection in the maize genome associated with the abundance of several groups of microbes in the maize rhizobiome. Genome-wide association study was conducted using the abundance of microbial groups as rhizobiome traits, and identified n = 622 plant loci that are linked to the abundance of n = 104 microbial groups in the maize rhizosphere. In 62/104 cases, which is more than expected by chance, the abundance of these same microbial groups was correlated with variation in plant vigor indicators derived from high throughput phenotyping of the same field experiment. We provide comprehensive datasets about the three-way interaction of host genetics, microbe abundance, and plant performance under two N treatments to facilitate targeted experiments towards harnessing the full potential of root-associated microbial symbionts in maize production.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Michael A Meier

    Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Gen Xu

    Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Martha G Lopez-Guerrero

    Department of Biochemistry, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Guangyong Li

    Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Christine Smith

    Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Brandi Sigmon

    Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Joshua R Herr

    Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3425-292X
  8. James R Alfano

    Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Yufeng Ge

    Department of Biological Systems Engineering, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. James C Schnable

    Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States
    For correspondence
    schnable@unl.edu
    Competing interests
    The authors declare that no competing interests exist.
  11. Jinliang Yang

    Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States
    For correspondence
    jinliang.yang@unl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0999-3518

Funding

National Science Foundation (Cooperative Agreement OIA-1557417)

  • Jinliang Yang

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

Reviewing Editor

  1. Rebecca Bart, The Donald Danforth Plant Science Center, United States

Publication history

  1. Preprint posted: November 2, 2021 (view preprint)
  2. Received: November 23, 2021
  3. Accepted: July 25, 2022
  4. Accepted Manuscript published: July 27, 2022 (version 1)
  5. Version of Record published: September 13, 2022 (version 2)

Copyright

© 2022, Meier 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. Michael A Meier
  2. Gen Xu
  3. Martha G Lopez-Guerrero
  4. Guangyong Li
  5. Christine Smith
  6. Brandi Sigmon
  7. Joshua R Herr
  8. James R Alfano
  9. Yufeng Ge
  10. James C Schnable
  11. Jinliang Yang
(2022)
Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maize
eLife 11:e75790.
https://doi.org/10.7554/eLife.75790

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    Funding: The Natural Science Fund for Distinguished Young Scholars of Zhejiang Province; National Natural Science Foundation of China; Key Project of Research and Development Plan of Hunan Province; the Swedish Heart Lung Foundation; the Swedish Research Council; the Swedish Cancer Society.