Network mapping of root–microbe interactions in Arabidopsis thaliana

Abstract Understanding how plants interact with their colonizing microbiota to determine plant phenotypes is a fundamental question in modern plant science. Existing approaches for genome-wide association studies (GWAS) are often focused on the association analysis between host genes and the abundan...

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Main Authors: Xiaoqing He, Qi Zhang, Beibei Li, Yi Jin, Libo Jiang, Rongling Wu
Format: Article
Language:English
Published: Nature Publishing Group 2021-09-01
Series:npj Biofilms and Microbiomes
Online Access:https://doi.org/10.1038/s41522-021-00241-4
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spelling doaj-fb3f76463743455286087061a076e40c2021-09-12T11:27:58ZengNature Publishing Groupnpj Biofilms and Microbiomes2055-50082021-09-017111010.1038/s41522-021-00241-4Network mapping of root–microbe interactions in Arabidopsis thalianaXiaoqing He0Qi Zhang1Beibei Li2Yi Jin3Libo Jiang4Rongling Wu5Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry UniversityCenter for Computational Biology, College of Biological Sciences and Technology, Beijing Forestry UniversityCenter for Computational Biology, College of Biological Sciences and Technology, Beijing Forestry UniversityCenter for Computational Biology, College of Biological Sciences and Technology, Beijing Forestry UniversityBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry UniversityBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry UniversityAbstract Understanding how plants interact with their colonizing microbiota to determine plant phenotypes is a fundamental question in modern plant science. Existing approaches for genome-wide association studies (GWAS) are often focused on the association analysis between host genes and the abundance of individual microbes, failing to characterize the genetic bases of microbial interactions that are thought to be important for microbiota structure, organization, and function. Here, we implement a behavioral model to quantify various patterns of microbe-microbe interactions, i.e., mutualism, antagonism, aggression, and altruism, and map host genes that modulate microbial networks constituted by these interaction types. We reanalyze a root-microbiome data involving 179 accessions of Arabidopsis thaliana and find that the four networks differ structurally in the pattern of bacterial-fungal interactions and microbiome complexity. We identify several fungus and bacterial hubs that play a central role in mediating microbial community assembly surrounding A. thaliana root systems. We detect 1142 significant host genetic variants throughout the plant genome and then implement Bayesian networks (BN) to reconstruct epistatic networks involving all significant SNPs, of which 91 are identified as hub QTLs. Results from gene annotation analysis suggest that most of the hub QTLs detected are in proximity to candidate genes, executing a variety of biological functions in plant growth and development, resilience against pathogens, root development, and abiotic stress resistance. This study provides a new gateway to understand how genetic variation in host plants influences microbial communities and our results could help improve crops by harnessing soil microbes.https://doi.org/10.1038/s41522-021-00241-4
collection DOAJ
language English
format Article
sources DOAJ
author Xiaoqing He
Qi Zhang
Beibei Li
Yi Jin
Libo Jiang
Rongling Wu
spellingShingle Xiaoqing He
Qi Zhang
Beibei Li
Yi Jin
Libo Jiang
Rongling Wu
Network mapping of root–microbe interactions in Arabidopsis thaliana
npj Biofilms and Microbiomes
author_facet Xiaoqing He
Qi Zhang
Beibei Li
Yi Jin
Libo Jiang
Rongling Wu
author_sort Xiaoqing He
title Network mapping of root–microbe interactions in Arabidopsis thaliana
title_short Network mapping of root–microbe interactions in Arabidopsis thaliana
title_full Network mapping of root–microbe interactions in Arabidopsis thaliana
title_fullStr Network mapping of root–microbe interactions in Arabidopsis thaliana
title_full_unstemmed Network mapping of root–microbe interactions in Arabidopsis thaliana
title_sort network mapping of root–microbe interactions in arabidopsis thaliana
publisher Nature Publishing Group
series npj Biofilms and Microbiomes
issn 2055-5008
publishDate 2021-09-01
description Abstract Understanding how plants interact with their colonizing microbiota to determine plant phenotypes is a fundamental question in modern plant science. Existing approaches for genome-wide association studies (GWAS) are often focused on the association analysis between host genes and the abundance of individual microbes, failing to characterize the genetic bases of microbial interactions that are thought to be important for microbiota structure, organization, and function. Here, we implement a behavioral model to quantify various patterns of microbe-microbe interactions, i.e., mutualism, antagonism, aggression, and altruism, and map host genes that modulate microbial networks constituted by these interaction types. We reanalyze a root-microbiome data involving 179 accessions of Arabidopsis thaliana and find that the four networks differ structurally in the pattern of bacterial-fungal interactions and microbiome complexity. We identify several fungus and bacterial hubs that play a central role in mediating microbial community assembly surrounding A. thaliana root systems. We detect 1142 significant host genetic variants throughout the plant genome and then implement Bayesian networks (BN) to reconstruct epistatic networks involving all significant SNPs, of which 91 are identified as hub QTLs. Results from gene annotation analysis suggest that most of the hub QTLs detected are in proximity to candidate genes, executing a variety of biological functions in plant growth and development, resilience against pathogens, root development, and abiotic stress resistance. This study provides a new gateway to understand how genetic variation in host plants influences microbial communities and our results could help improve crops by harnessing soil microbes.
url https://doi.org/10.1038/s41522-021-00241-4
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AT yijin networkmappingofrootmicrobeinteractionsinarabidopsisthaliana
AT libojiang networkmappingofrootmicrobeinteractionsinarabidopsisthaliana
AT ronglingwu networkmappingofrootmicrobeinteractionsinarabidopsisthaliana
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