Microbiome-mediated plant-soil feedbacks as a tool for resilient agriculture

Conventional agricultural intensification has eroded the biological foundations of productive soil by disrupting the reciprocal interactions, plant-soil feedback (PSF), through which plants actively shape and are continuously shaped by the soil microbiome. Although the molecular mechanisms governing PSF direction are increasingly well-characterized, deliberate PSF management as a practical tool for resilient crop production remains underdeveloped. This is largely because no integrative framework has translated these ecological insights into state-contingent, field-deployable decision rules. This review addresses that gap by first synthesizing the molecular basis of microbiome assembly, encompassing host genetic control of root exudate chemistry, receptor-mediated microbial recognition, and the bidirectional chemical dialogue between plant and rhizosphere. Building from this mechanistic foundation, we move beyond cataloging mechanisms to present a novel, integrative three-pillar management framework for actively steering PSF. This framework operationalizes PSF management by strategically combining: (i) engineering the plant partner (leveraging genetics to recruit beneficial microbiomes), (ii) managing the soil habitat (using agronomic practices to engineer suppressive ecological legacies), and (iii) deploying advanced microbial consortia. Critically, we argue that the recent meta-omics revolution, integrating metagenomics, metatranscriptomics, metaproteomics, and metabolomics, is the enabling technology that transforms this framework from a conceptual model into a quantifiable, diagnosable, and agriculturally deployable system. Multi-omics tools provide the empirical foundation for diagnosing soil feedback states, monitoring intervention outcomes, and building predictive models. By bridging the lab-field gap and evaluating key translational challenges, this review provides a coherent, actionable roadmap for harnessing PSF to achieve cultivated resilience in modern agriculture.