Network mapping of root–microbe interactions in Arabidopsis thaliana

Abstract

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.