Modulation of the Root Microbiome by Plant Molecules: The Basis for Targeted Disease Suppression and Plant Growth Promotion

Abstract

Plants host a mesmerizing diversity of microbes inside and around their roots, known as the microbiome. The microbiome is composed mostly of fungi, bacteria, oomycetes, and archaea that can be either pathogenic or beneficial for plant health and fitness. To grow healthy, plants need to surveil soil niches around the roots for the detection of pathogenic microbes, and in parallel maximize the services of beneficial microbes in nutrients uptake and growth promotion. Plants employ a palette of mechanisms to modulate their microbiome including structural modifications, the exudation of secondary metabolites and the coordinated action of different defence responses. Here, we review the current understanding on the composition and activity of the root microbiome and how different plant molecules can shape the structure of the root-associated microbial communities. Examples are given on interactions that occur in the rhizosphere between plants and soilborne fungi. We also present some well-established examples of microbiome harnessing to highlight how plants can maximize their fitness by selecting their microbiome. Understanding how plants manipulate their microbiome can aid in the design of next-generation microbial inoculants for targeted disease suppression and enhanced plant growth.

Keywords: disease suppression; microbial inoculants; microbiota; plant defense; plant growth promotion; plant molecules; root exudation; root microbiome.

Figure 1

Plants respond to different environmental stresses and modulate their microbiome. (A) Plants not experiencing any biotic stress and having access to nutrients (green pentagons), release constitutively exudates (red arrows) that allow them to sustain a balance in the rhizosphere between pathogenic and beneficial microbes. (B) Upon infection by a pathogen (red microbe), the exudation profile of roots changes and stress-induced exudates (blue arrows) aid the plants in inhibiting pathogenic growth in the rhizosphere, while selecting at the same time for beneficial microbes. Some of these beneficial microbes when they establish themselves in the rhizosphere, can trigger ISR that can help plants deal with pathogenic infections in the leaves. (C) In the case of soil suppressiveness or “cry-for-help” conditions, there is establishment of beneficial rhizosphere communities that are further supported by the release of stress-induced exudates. Under these conditions, soilborne and foliar pathogens fail to cause disease. (D) Plants experiencing nutrient deficiencies (e.g. iron, nitrogen, phosphate) change the metabolomic profile of their roots to either make nutrients more available and soluble or to attract beneficial microbes (e.g. rhizobia, AMF, PGPR) that can help them deal with the nutrient deficiency. Font size indicates the abundance of beneficial or pathogenic subsets of the microbiota under different conditions. The figure was designed with Biorender (https://biorender.com).

Figure 2

Integration of modern technologies to engineer microbial inoculants that boost plant growth and suppress pathogens. Plants respond to stresses and change their exudation. To unravel how changes in exudation affect microbiome composition and functions, we need to couple advance metabolomic techniques with metagenomics sequencing (A) and culture-based methodologies (B). At the same time, there is promise for the use of exometabolomics methodologies and spatial metabolomics that can help in finding where specific exudates are produced and how the microbes around the exudation site are affected (C). Analysis of the generated data in depth will allow the characterization of the microbial communities that respond to exudates and the identification of networks that will reveal how microbes interact and contribute in the microbiome assembly (A). The parallel isolation of a representative fraction of the root microbiome (B) will allow to link descriptive data with the isolated microbes and will guide the design of synthetic communities (D). Testing of these synthetic communities with different hosts under different conditions (e.g. biotic/abiotic stress/in vitro/in soil/in field) will facilitate the selection of synthetic communities that can promote plant growth (E) and suppress pathogens (F) in a consistent and reproducible manner. The figure was designed with Biorender (https://biorender.com/).