Plant Growth-Promoting Microorganisms Mediate Plant Metabolic Reprogramming to Manage the Rhizospheric Microbiome.

The microbial community surrounding plant roots plays a vital role in plant growth, nutrient uptake, stress resilience and other potential functions. This review synthesizes available evidence that plant growth-promoting microorganisms (PGPMs) not only directly benefit the plant but also modulate the rhizospheric microbiome by mediating metabolic reprogramming of the host plant. PGPMs modify the composition of root exudates through the regulation of phytohormone signaling and transcriptional networks, thereby promoting beneficial microbes and suppressing disease. Key mechanisms involve the jasmonate, ethylene, and strigolactones signaling pathways. Transcription factors MYB72, ERF1 regulate biosynthesis and secretion of metabolites like organic acids and coumarins. The exudates serve as specific signals for microbial community assembly and as enhancers of feedback loops that reinforce plant-microbe mutualism. We examine the ecological and agricultural significance of PGPM-induced metabolic reprogramming of the host due to PGPMs that enhances disease suppression, abiotic stress tolerance, and nutrient use efficiency. Lastly, we address advanced methods and strategies for transferring these biological pathways to the agricultural realm and on to a more sustainable agricultural practice with emphasis on the need to integrate multi-omics (whole genomics, transcriptomics, and metabolomics), synthetic microbial communities and plant genetic engineering for microbiome-assisted agriculture. This synthesis reveals that PGPM-induced metabolic reprogramming operates through an integrated cross-scale framework linking microbial perception, phytohormone signaling, transcriptional regulators, and transporter-mediated exudate efflux, with root exudates functioning as plant-controlled ecological filters that selectively shape the rhizosphere microbiome. We further identify key translational challenges, including context-dependent efficacy and the lab-to-field gap, and propose a roadmap combining multi-omics, synthetic communities, and genome editing to realize the potential of microbiome-assisted sustainable agriculture.