Hidden conversations beneath the soil: microRNA and hormone control of root symbioses

Plants are found in dynamic soil ecosystems, which are highly enriched with microorganisms that have significant impacts on the health and productivity of plants. Promotion of nutrient uptake, fixation of nitrogen, and tolerance to stress by arbuscular mycorrhizal fungi (AMF) and plant growth-promoting rhizobacteria occur via complex molecular communication with plant roots. Post-transcriptional gene silencing is mediated by MicroRNAs (miRNAs)-small non-coding RNAs that control gene networks in symbiosis and stress responses. Concurrently, phytohormones (auxin, cytokinin, ethylene, jasmonates, salicylic acid, abscisic acid, strigolactones, gibberellins, and brassinosteroids) control root development, defence, and microbial recruitment. Their combined regulatory functions in the establishment of root symbiosis are yet to be fully appreciated, although the integrated regulatory functions of miRNAs and phytohormones in regulating root symbiotic assembly have increasingly been recognised. The paper is a synthesis of the existing knowledge on root-associated beneficial symbioses and a critical assessment of the new roles of plant miRNAs and phytohormonal pathways in the establishment and maintenance of nodulation and arbuscular mycorrhizal associations. We suggest that miRNAs and phytohormones are linked in a complex regulatory network in which miRNAs can regulate hormone pathways and vice versa. We have also demonstrated crucial knowledge gaps by identifying molecular crosstalk between plants and their microbiota, functional validation of miRNA-target pairs, cross-kingdom small RNA trafficking and systemic shoot-root signalling that future studies can use to harness the full potential of plant-microbe interaction for achieving sustainable agriculture.