Unravelling the Molecular Dialogue of Beneficial Microbe-Plant Interactions

Abstract

Plants are an intrinsic part of the soil community, which is comprised of a diverse range of organisms that interact in the rhizosphere through continuous molecular communications. The molecular dialogue within the plant microbiome involves a complex repertoire of primary and secondary metabolites that interact within different liquid matrices and biofilms. Communication functions are likely to involve membrane-less organelles formed by liquid-liquid phase separation of proteins and natural deep eutectic solvents that play a role as alternative media to water. We discuss the chemistry of inter-organism communication and signalling within the biosphere that allows plants to discriminate between harmful, benign and beneficial microorganisms. We summarize current information concerning the chemical repertoire that underpins plant-microbe communication and host-range specificity. We highlight how the regulated production, perception and processing of reactive oxygen species (ROS) is used in the communication between plants and microbes and within the communities that shape the soil microbiome.

Keywords: host‐range specificity; microbial transplantation; plant−microbe communication; reactive oxygen species; receptor−ligand signalling; root microbiome.

Figure 1

Microbiomes serve as the foundation for one health. The health of plants, humans and the environment are interconnected and rely on close association with microbial communities. The beneficial microbial microbes in the plant rhizosphere determine plant productivity by assisting in seed germination, foraging for nutrients under nutrient‐limiting conditions or nutrient recycling along with providing abiotic and biotic stress tolerance through production metabolites and modulating host immunity, respectively. In humans, the beneficial microbes introduced via direct consumption of plant products or indirect exposure through the environment contribute to overall health maintenance by boosting the immune system against pathogens, reducing the usage of antimicrobial compounds and providing some essential nutrients. The beneficial microbes can offer a sustainable solution for the conservation of nature by replacing chemical fertilizers and pesticides responsible for global warming and environmental pollution.

Figure 2

Mechanisms for plant−microbe interactions. Plant−microbe interactions occur in spermoshere, rhizosphere and phyllosphere. Microbes in the spermosphere aid seedling establishment by controlling germination and the secretion of compounds that inhibit competing pathogenic microbes. The plant−microbe chemical communication network involves primary and secondary metabolites that attract beneficial microbes and restrict pathogenic microbes. Beneficial microbes secret allelochemicals with biocontrol activity. Phytohormones including indole acetic acid (IAA), cytokinin (CK), gibberellic acid (GA), strigolactone (SL) and salicylic acid (SA) are secreted by both plants and microbes. Soil microbes not only enhance plant immunity by triggering systemic resistance responses via MAMP‐triggered immunity or effector‐triggered immunity, but they also directly inhibit invading pathogens. Beneficial microbes can successfully evade plant immune surveillance by deploying effector proteins to suppress plant immune response (A). The microbe‐derived PAMPs and MAMPs are perceived by PRRs that trigger signalling events, including Ca influx and activation of plasma membrane‐bound RBOH enzymes that produce reactive oxygen species (ROS burst). Oscillations in calcium concentrations (calcium spiking) and ROS waves act together with a network of signalling proteins as well as Ca‐dependent protein kinases (CDPKs, CCaMKs and CIPKs) to control transcriptional reprogramming, activation of defence‐related genes, secondary metabolite production and defence hormone synthesis. This system triggers an immune response throughout the plant resulting in systemic acquired resistance (B). Current concepts concerning this signalling cascade are described in detail in the accompanying text. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 3

Genetic approaches to broaden the host range of beneficial microbes. Microbe‐derived effector proteins can be engineered to block host defences and initiate symbiosis (A). Genetic engineering approach to recreate nodule organogenesis in nonlegume plants. The Myc‐receptor, which recognizes AMF‐produced Myc‐factors, has been engineered to perceive Nod factors by replacing the outer domain of the receptor. This induces the formation of nodule‐like structures by activating a common symbiotic signalling pathway (CSSP) (B). Another approach is to facilitate the association between nitrogen‐fixing microbes and cereals including rhizopine synthesis in plants such as wheat and rice. Rhizopine is sensed by nitrogen‐fixing bacteria via biosensor plasmids that encode rhizopine‐binding proteins and rhizopine‐dependent transcription factors (TF). These proteins drive the downstream expression of genes encoding proteins required for nitrogen fixation (C). Finally, the recruitment of root‐associated microbiota is dependent on host genetics. Genome‐wide association study mapping will identify novel host genetic loci that control microbial selection to facilitate breeding efforts to improve crop resilience (D). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 4

Holobiont approaches for next‐generation agriculture. Beneficial microbes can reduce the agricultural use of fertilizers and chemical pesticides, and contribute to rhizosphere carbon sink capacity (A). Rhizosphere microbiomes from plants inhabiting extreme environments or stress‐tolerant cultivars and can be transplanted can be used in phytoremediation and soil improvement approaches (B). Synthetic microbial communities (SynCom) can augment crop quality. High‐quality crop production systems can be used to source SynComs. High‐throughput sequencing and systems biology approaches can be used to identify appropriate SynCom systems. Network analysis provides information on core microbial taxa and hubs and facilitates the selection of best candidate microbes for further screening. The efficacy and ecological impacts of SynComs must be validated in field studies (C). Composites of the signalling chemicals found in root exudates, including flavonoids, γ‐aminobutyric acid, malate and citrate can be applied to soils to attract beneficial microbes (D). Nanomaterial‐based approaches are also an attractive approach for improving plant health by releasing trapped soil nutrients and modulating root exudates (E). [Color figure can be viewed at wileyonlinelibrary.com]