Network mapping of root-microbe interactions inArabidopsis 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 based on the association analysis between host genes and the abundance of individual microbes, failing to characterize the genetic architecture of microbial interactions that are thought to a determinant of 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 and find 91 hub QTLs. Gene annotation shows that a number of the hub genes detected are biologically relevant, playing roles in plant growth and development, resilience against pathogens, root development, and improving resistance against abiotic stress conditions. The new model allows us to better understand the underlying mechanisms that govern the relationships between plants and their entire microbiota and harness soil microbes for plant production.

The root microbiome: Community assembly and its contributions to plant fitness

“…These QTL are involved in cell‐wall integrity, plant immunity, and root and root hair development (Bergelson et al, 2019). By reanalyzing the same dataset, He et al (2021) identified hub fungi and bacteria that are critical for assembling the microbial community. Likewise, they identified 91 hub host QTL involved in plant growth and development, root growth, pathogen resistance, and abiotic stress resistance (He et al, 2021).…”

“…By reanalyzing the same dataset, He et al (2021) identified hub fungi and bacteria that are critical for assembling the microbial community. Likewise, they identified 91 hub host QTL involved in plant growth and development, root growth, pathogen resistance, and abiotic stress resistance (He et al, 2021). A recent study suggests that FERONIA (FER), a cell membrane receptor protein kinase, is involved in regulating microbiota structure.…”

Disentangling leaf-microbiome interactions in Arabidopsis thaliana by network mapping

“…We calculate the degree of each node in a network. To reduce the bias, we statistically identify the hub taxa with the highest degree and closeness centrality [13,37]. Meanwhile, six network indices, including connectivity (Con), closeness (C(u)), betweenness(B(u)), eccentricity (E(u)), eigencentrality (G(u)), and Pagerank (P(u)) are calculated, as described previously [35].…”

“…Thus, we can map host genes for the topological architecture of microbe-microbe interactions and interdependence. Second, it has been increasingly clear that microbial traits are not only determined by key host QTLs, but also through their epistatic networks [37]. Network mapping can draw the host genetic landscape of microbial interactions.…”

Gnotobiotic Plant Systems for Reconstitution and Functional Studies of the Root Microbiota

“…Surveys with field‐collected samples are limited in their ability to draw conclusions about the biological function(s) of the root microbiota. This is due to the numerous interactions between and within the different microbial classes of the root microbiota, interactions with the plant host, and the influence of edaphic and other environmental parameters on microbial community composition and activity (Bulgarelli et al., 2013; Duran et al., 2018; He et al., 2021; Thiergart et al., 2020). This makes it almost impossible to disentangle these interactions and assign particular plant phenotypes to microbial services.…”