Coumarin Communication Along the Microbiome–Root–Shoot Axis

Bidirectional signaling occurs along the microbiome–root–shoot axis in plants much akin to that along the human microbiome–gut–brain axis. Production of plant secondary metabolites elicited by rhizosphere microbiota, such as coumarins, can directly impact the composition and activity of the microbial community. Microbially elicited production of secondary metabolites in the roots can act as intertissue messengers in plants. Coumarins are the ‘new kids on the block’ in the chemical communication along the microbiome–root–shoot axis. Plants shape their rhizosphere microbiome by secreting root exudates into the soil environment. Recently, root-exuded coumarins were identified as novel players in plant–microbiome communication. Beneficial members of the root-associated microbiome stimulate coumarin biosynthesis in roots and their excretion into the rhizosphere. The iron-mobilizing activity of coumarins facilitates iron uptake from the soil environment, while their selective antimicrobial activity shapes the root microbiome, resulting in promotion of plant growth and health. Evidence is accumulating that, in analogy to strigolactones and flavonoids, coumarins may act in microbiome-to-root-to-shoot signaling events. Here, we review this multifaceted role of coumarins in bidirectional chemical communication along the microbiome–root–shoot axis. Plants shape their rhizosphere microbiome by secreting root exudates into the soil environment. Recently, root-exuded coumarins were identified as novel players in plant–microbiome communication. Beneficial members of the root-associated microbiome stimulate coumarin biosynthesis in roots and their excretion into the rhizosphere. The iron-mobilizing activity of coumarins facilitates iron uptake from the soil environment, while their selective antimicrobial activity shapes the root microbiome, resulting in promotion of plant growth and health. Evidence is accumulating that, in analogy to strigolactones and flavonoids, coumarins may act in microbiome-to-root-to-shoot signaling events. Here, we review this multifaceted role of coumarins in bidirectional chemical communication along the microbiome–root–shoot axis. a molecular signaling pathway that is essential for plants to associate with AM fungi and for legumes specifically to engage in symbiosis with nitrogen-fixing rhizobacteria. This signaling pathway contains a set of conserved genes that are shared by the rhizobial and mycorrhizal associations. Upon perception of a microbial signal at the plasma membrane, a series of signal transduction cascades is activated involving the production of calcium oscillations, which are perceived by Ca+/calmodulin-dependent protein kinase (CCaMK). After this, there is transcriptional regulation of transcription factors and genes that coordinate the formation of symbiosis. a physiological state of the plant following root colonization by selected beneficial microbes or treatment with natural/synthetic compounds characterized by the launching of a faster and stronger defense response, resulting in enhanced resistance against future pathogen or insect attack or enhanced tolerance to abiotic stresses. the totality of microbial genomes and the functional traits of the microbiota present in a specific host tissue. the bidirectional communication between the gastrointestinal microbiota, the gut, and the central nervous system (brain) involving signals from the neuron system, immune system, and endocrine system that affect gut behavior, and the emotional status and fitness of the host. concept describing the bidirectional communication between rhizosphere microbiota, the plant root, and the aerial shoot tissue involving plant- or microbe-derived signals that affect plant growth, nutrition, and health. the combined population of all commensal, symbiotic, and pathogenic microbial organisms (including archaea, bacteria, fungi, and protists) that live in or on a host, such as the rhizosphere microbiota or gut microbiota. a secondary metabolite biosynthesis pathway in plants that generates a range of aromatic metabolites. Products of this pathway have roles in the resistance of plants to (a)biotic stresses, and in plant structural support and stress adaptation. Phenylpropanoid compounds are derived from the amino acid phenylalanine, the end-product of the shikimate pathway, through deamination by phenylalanine ammonia lyase (PAL). Phenylpropanoid natural compounds include hydroxycinnamic acid, flavonoid/isoflavonoids, lignans/lignin, coumarins, and stilbenes.