Chemical Communication Between Plant and Microbe in the Phyllosphere

The phyllosphere encompasses all above-ground plant parts, covering ~10⁹ km² and hosting as many as 10²⁶ microbial cells, yet its chemical ecology remains understudied compared to the rhizosphere. This review synthesizes recent advances in metabolite-mediated communication orchestrating phyllosphere microbiome assembly, function and host feedback. Leaf structural traits, host immune genes, developmental stage, and fluctuating environmental drivers create spatiotemporal chemical niches that filter incoming microbes. We then examine four major classes of plant-derived signals, including primary metabolites, secondary metabolites and phytohormones, with an emphasis on their dual functionality. Microbial feedback occurs through phytohormone synthesis/catabolism, volatile and soluble effectors and antimicrobial metabolites that collectively modulate plant immunity, growth and stress tolerance while structuring inter-microbial competition. These bidirectional exchanges form a dynamic network where plants and microbes continuously negotiate cooperation and conflict under diurnal and seasonal oscillations. We outline translational prospects, including probiotic foliar applications, metabolite priming and breeding for beneficial consortia, while identifying key challenges in signal attribution, microbiota stabilization and deciphering community-level crosstalk dynamics for sustainable crop protection.