Coevolution of plant-microbe interactions, friend-foe continuum, and microbiome engineering for a sustainable future

The coevolution of plant-microbe (PM) associations over approximately 450 million years has been a fundamental driver of terrestrial life, giving rise to mutualistic, commensal, and pathogenic relationships along a dynamic friend-foe continuum. The need to adapt to the host environment has driven the convergent evolution of common strategies among mutualists and pathogens, enabling them to evade or modulate the plant immune system. This review synthesizes PM coevolution within a deep-time, three-pillar framework: organellogenesis, root evolution, and immune gatekeeping, linking ancient endosymbiotic events (mitochondria, chloroplasts, and nitroplasts) to contemporary holobiont-level phenotypes and biotechnological applications. We organize the friend-foe continuum around a coevolution-guided cost-benefit and tipping-point framework, using identified molecular switches and evolutionary constraints to derive actionable design rules for engineering PM associations. Moving beyond a descriptive toolbox of technologies, we integrate recent breakthroughs to analyze how four principal axes (host and microbial genetics, evolutionary dynamics, environmental and ecological conditions, and metabolic switches) define the thresholds that govern microbial lifestyle transitions. Finally, we propose specific, testable strategies for PM coevolution-informed crop improvement, distinguishing near-term feasible targets from long-term speculative goals in nitrogen utilization, synthetic microbial communities, immune receptor engineering, modulation of plant memory, and microbiome-integrated breeding through genome editing, synthetic biology, AI, and microbiome engineering. Together, these approaches extend existing syntheses into a predictive, evolution-informed framework that translates coevolutionary principles into a functional blueprint for sustainable, resilient agriculture.