Rhizosphere triangular warfare: mechanistic insights for plant- beneficial microbe- pathogen interactions

Abstract

The rhizosphere is a living physical space that is constantly evolving and is characterized by a complex interplay between beneficial microbes, pathogens, and plants, mediated by molecular and ecological interactions. These three-way relationships constitute a rhizosphere “triangular warfare system,” which controls plant health, nutrient uptake, disease resistance, and plant resilience. This review provides a mechanistic overview of the molecular, metabolic and ecological processes underlying these tripartite interactions. We discuss how plants integrate pattern-triggered immunity (PTI), effector-triggered immunity (ETI), microbiome exudation, and hormone signaling to select beneficial microbes to exclude pathogen entry. Beneficial microbes deploy volatile organic compounds, induction of systemic resistance (ISR), secretion systems, phytotoxins, siderophores, lytic enzymes, and microbiome-disrupting strategies to enhance plant fitness, whereas pathogens use virulence effectors, lytic enzymes, secretion systems, phytotoxins, siderophores, and microbiome-disrupting strategies to overcome host defenses and restructure rhizosphere communities. Recent advances in multi-omics have revealed the intricate signaling networks, metabolic interactions, and microbial competition shaping these relationships under various environmental conditions. We further explore emerging opportunities in microbiome engineering, synthetic microbial consortia and disease-suppressive soil management for sustainable crop protection. This review synthesizes existing mechanistic knowledge and introduces the concept of ‘rhizosphere triangular warfare’ as a stepping stone toward the next generation of microbiome-based agriculture and precision rhizosphere engineering under environmental changes.