The rhizosphere nexus: Mechanistic foundations and engineering of plant-soil-microbe interactions for agricultural sustainability

Agricultural sustainability increasingly depends on optimizing the rhizosphere nexus, where plants, soil, and microorganisms interact to regulate nutrient cycling, stress resilience, and soil health. Traditional approaches favour single-strain inoculants, which frequently fail under field conditions owing to poor persistence, strong context dependency, and limited functional scope. This review critiques the limitations of reductionist inoculation paradigms and advances a shift toward engineering the rhizosphere by integrating plant traits, soil physicochemical constraints, and microbial functional diversity. We examined the fundamental tripartite interaction, emphasizing root architecture and exudation as heritable chemical blueprints that filter microbial recruitment, while soil properties serve as environmental constraints that govern microbial persistence and functional expression. Particular emphasis was placed on molecular communication networks, including cross-kingdom signalling among plants, bacteria, and fungi, and on how conventional agricultural inputs may disrupt these coordination processes. Beyond nutrient availability, we examined how microbial communities regulate the timing of macronutrient (N, P) and essential micronutrient (Fe, Mn, Zn) availability, and critically assessed the context-dependent trade-offs of arbuscular mycorrhizal fungi (AMF) under intensive management. The review further evaluates the role of the rhizosphere microbiome in enhancing resilience to abiotic stresses, such as drought, salinity, and heat, and in suppressing biotic stresses through induced systemic resistance and the development of disease-suppressive soils. Furthermore, we have highlighted emerging strategies for rhizosphere engineering, including microbiome-enabled breeding, synthetic microbial consortia, agronomic steering, and precision microbiome management. By integrating mechanistic insights with digital agriculture, metagenomics, and data-driven decision frameworks, this review reframes the farm as a dynamically regulated ecological system rather than a site for substituting chemical inputs, offering a pathway toward a more predictable and sustainable agricultural ecosystem.