Multitrophic rhizosphere-phyllosphere signaling networks regulating plant physiological adaptation and stress resilience

Plants operate as metaorganisms, depending on the coordinated signalling between the microbiomes of the roots (rhizosphere) and leaves (phyllosphere). This review covers recent studies that have identified rhizosphere-phyllosphere cross-talk as a crucial determinant of systemic stress resilience. Microbial metabolites, phytohormones, volatile organic compounds (VOCs), extracellular vesicles (EVs), and short RNAs (sRNAs) coordinate subterranean responses via vascular, gaseous, and molecular routes. Beneficial root-associated microbes modulate plant ethylene levels and antioxidant defense system in leaves through production of indole-3-acetic acid (IAA) and ACC deaminase activity. This causes the leaves to hold more water and chlorophyll when it is dry. In contrast, phyllosphere methylotrophs control root exudation through cytokinin-linked feedback which maintains metabolic balance. The identification of EV-encapsulated sRNAs and microbial lipopeptides as mobile nano-messengers paves way for a novel epoch in plant-microbe communication. Fungi, mycorrhizal association, and polyphagous insects are important in the regulation of nutrient fluxes and mediation of the trade-offs between nutrient acquisition and plant defense. Integrative multi-omics, isotope tracking, and synthetic community (SynCom) reconstructions now enable causal mapping of these systemic linkages. Understanding the cross-talk between different parts of the microbiome can help develop climate-resilient crops and provide a mechanistic basis for sustainable agriculture.