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

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...

Full description

Bibliographic Details
Main Authors: Michael A Meier, Gen Xu, Martha G Lopez-Guerrero, Guangyong Li, Christine Smith, Brandi Sigmon, Joshua R Herr, James R Alfano, Yufeng Ge, James C Schnable, Jinliang Yang
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/75790
_version_ 1811181658531954688
author Michael A Meier
Gen Xu
Martha G Lopez-Guerrero
Guangyong Li
Christine Smith
Brandi Sigmon
Joshua R Herr
James R Alfano
Yufeng Ge
James C Schnable
Jinliang Yang
author_facet Michael A Meier
Gen Xu
Martha G Lopez-Guerrero
Guangyong Li
Christine Smith
Brandi Sigmon
Joshua R Herr
James R Alfano
Yufeng Ge
James C Schnable
Jinliang Yang
author_sort Michael A Meier
collection DOAJ
description 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 n=622 plant loci were identified 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 toward harnessing the full potential of root-associated microbial symbionts in maize production.
first_indexed 2024-04-11T09:21:20Z
format Article
id doaj.art-4985814c06ed441898567b4a80352b89
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-11T09:21:20Z
publishDate 2022-07-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-4985814c06ed441898567b4a80352b892022-12-22T04:32:12ZengeLife Sciences Publications LtdeLife2050-084X2022-07-011110.7554/eLife.75790Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maizeMichael A Meier0https://orcid.org/0000-0002-7727-6561Gen Xu1Martha G Lopez-Guerrero2Guangyong Li3Christine Smith4Brandi Sigmon5Joshua R Herr6https://orcid.org/0000-0003-3425-292XJames R Alfano7Yufeng Ge8James C Schnable9Jinliang Yang10https://orcid.org/0000-0002-0999-3518Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States; Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United StatesDepartment of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States; Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United StatesDepartment of Biochemistry, University of Nebraska-Lincoln, Lincoln, United StatesDepartment of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States; Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United StatesCenter for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United StatesDepartment of Plant Pathology, University of Nebraska-Lincoln, Lincoln, United StatesCenter for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United States; Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, United StatesCenter for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United States; Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, United StatesBiological Systems Engineering Department, University of Nebraska-Lincoln, Lincoln, United StatesDepartment of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States; Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United StatesDepartment of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, United States; Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, United StatesThe 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 n=622 plant loci were identified 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 toward harnessing the full potential of root-associated microbial symbionts in maize production.https://elifesciences.org/articles/75790microbiomerhizobiomeGWAShost-microbe interactionpopulation geneticsnitrogen
spellingShingle Michael A Meier
Gen Xu
Martha G Lopez-Guerrero
Guangyong Li
Christine Smith
Brandi Sigmon
Joshua R Herr
James R Alfano
Yufeng Ge
James C Schnable
Jinliang Yang
Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maize
eLife
microbiome
rhizobiome
GWAS
host-microbe interaction
population genetics
nitrogen
title Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maize
title_full Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maize
title_fullStr Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maize
title_full_unstemmed Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maize
title_short Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maize
title_sort association analyses of host genetics root colonizing microbes and plant phenotypes under different nitrogen conditions in maize
topic microbiome
rhizobiome
GWAS
host-microbe interaction
population genetics
nitrogen
url https://elifesciences.org/articles/75790
work_keys_str_mv AT michaelameier associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT genxu associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT marthaglopezguerrero associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT guangyongli associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT christinesmith associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT brandisigmon associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT joshuarherr associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT jamesralfano associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT yufengge associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT jamescschnable associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize
AT jinliangyang associationanalysesofhostgeneticsrootcolonizingmicrobesandplantphenotypesunderdifferentnitrogenconditionsinmaize