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

Version 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.

Metrics

  • 2,797
    views
  • 755
    downloads
  • 22
    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. 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

Share this article

https://doi.org/10.7554/eLife.75790

Further reading

    1. Genetics and Genomics
    Can Hu, Xue-Ting Zhu ... Jin-Qiu Zhou
    Research Article

    Telomeres, which are chromosomal end structures, play a crucial role in maintaining genome stability and integrity in eukaryotes. In the baker’s yeast Saccharomyces cerevisiae, the X- and Y’-elements are subtelomeric repetitive sequences found in all 32 and 17 telomeres, respectively. While the Y’-elements serve as a backup for telomere functions in cells lacking telomerase, the function of the X-elements remains unclear. This study utilized the S. cerevisiae strain SY12, which has three chromosomes and six telomeres, to investigate the role of X-elements (as well as Y’-elements) in telomere maintenance. Deletion of Y’-elements (SY12), X-elements (SY12XYΔ+Y), or both X- and Y’-elements (SY12XYΔ) did not impact the length of the terminal TG1-3 tracks or telomere silencing. However, inactivation of telomerase in SY12, SY12XYΔ+Y, and SY12XYΔ cells resulted in cellular senescence and the generation of survivors. These survivors either maintained their telomeres through homologous recombination-dependent TG1-3 track elongation or underwent microhomology-mediated intra-chromosomal end-to-end joining. Our findings indicate the non-essential role of subtelomeric X- and Y’-elements in telomere regulation in both telomerase-proficient and telomerase-null cells and suggest that these elements may represent remnants of S. cerevisiae genome evolution. Furthermore, strains with fewer or no subtelomeric elements exhibit more concise telomere structures and offer potential models for future studies in telomere biology.

    1. Genetics and Genomics
    2. Neuroscience
    Bohan Zhu, Richard I Ainsworth ... Javier González-Maeso
    Research Article

    Genome-wide association studies have revealed >270 loci associated with schizophrenia risk, yet these genetic factors do not seem to be sufficient to fully explain the molecular determinants behind this psychiatric condition. Epigenetic marks such as post-translational histone modifications remain largely plastic during development and adulthood, allowing a dynamic impact of environmental factors, including antipsychotic medications, on access to genes and regulatory elements. However, few studies so far have profiled cell-specific genome-wide histone modifications in postmortem brain samples from schizophrenia subjects, or the effect of antipsychotic treatment on such epigenetic marks. Here, we conducted ChIP-seq analyses focusing on histone marks indicative of active enhancers (H3K27ac) and active promoters (H3K4me3), alongside RNA-seq, using frontal cortex samples from antipsychotic-free (AF) and antipsychotic-treated (AT) individuals with schizophrenia, as well as individually matched controls (n=58). Schizophrenia subjects exhibited thousands of neuronal and non-neuronal epigenetic differences at regions that included several susceptibility genetic loci, such as NRG1, DISC1, and DRD3. By analyzing the AF and AT cohorts separately, we identified schizophrenia-associated alterations in specific transcription factors, their regulatees, and epigenomic and transcriptomic features that were reversed by antipsychotic treatment; as well as those that represented a consequence of antipsychotic medication rather than a hallmark of schizophrenia in postmortem human brain samples. Notably, we also found that the effect of age on epigenomic landscapes was more pronounced in frontal cortex of AT-schizophrenics, as compared to AF-schizophrenics and controls. Together, these data provide important evidence of epigenetic alterations in the frontal cortex of individuals with schizophrenia, and remark for the first time on the impact of age and antipsychotic treatment on chromatin organization.