Root architecture and the rhizosphere microbiome: Shaping sustainable agriculture

Understanding root architecture and exudation is fundamental for enhancing crop productivity and promoting sustainable agriculture. Historically, plant researchers have focused on above-ground traits to increase yield and reduce input dependence. However, below-ground traits, especially those related to the root system, are equally critical yet often overlooked due to phenotyping challenges. Root architecture, including some root traits, i.e., lateral root density, root hair abundance, and root tip number, plays central roles in plant establishment, stress tolerance, and the recruitment of beneficial microbes in the rhizosphere. Root exudates, a complex array of chemical compounds released by roots, vary with plant species, developmental stage, and environmental conditions. These compounds act as signals and nutrients, shaping the composition and function of rhizosphere microbial communities. In turn, the microbiome of rhizosphere contributes to plant health by facilitating nutrient uptake, enhancing stress resilience, and providing defense against pathogens. Integrating root traits into breeding programs offers promising opportunities to select for genotypes that are more efficient in recruiting beneficial microbes. Heritable root traits, such as increased branching, finer roots, and higher exudation capacity, can enhance microbiome assembly and stability. The assessment of genes can also regulate of these traits and represent targets for genomics-assisted selection. Some strategies, such as microbiome engineering, particularly through the design of synthetic microbial communities (SynComs), can be used to modulate root architecture and optimize plant-microbe interactions. Despite these promising outcomes, challenges remain in translating SynCom applications to the field due to environmental variability, native microbial competition, and limited understanding of host genetic controls. This review discusses how root architecture shapes the rhizosphere microbiome and explores strategies, such as trait-based breeding and microbiome engineering, for advancing sustainable crop production.