Abstract
We hypothesized that foliar exposure to polyethylene microspheres (PEMS) in tomato plants (Solanum lycopersicum L.) triggers a cascade of physiological responses in leaves that ultimately reshape the root metabolome and exudate composition, thereby modulating the root-associated microbiome. Tomato plants were grown in soil and hydroponics. Leaves were sprayed with PEMS (10–100–1000 mg L−1) or water (Control), avoiding direct contact with the growing media. After 31 days, biomass, SPAD, root metabolome, and rhizosphere microbial communities in soil-grown plants and exudome in hydroponic were assessed; root metabolome and exudates were analyzed via GC-MS, and rhizosphere communities via DNA metabarcoding. Additionally, shoots and roots were examined using transmission electron microscopy. Foliar PEMS exposure increased shoot and root biomass and SPAD index in the early days post-treatments, while reducing shoot water content, likely due to PEMS-induced ultrastructural cellular damage. In roots, PEMS significantly reduced the concentrations of several key metabolites, including serine, tryptophan, 5,6-dihydrouracil, lactic acid, tartaric acid, palmitic acid, and stearic acid. Root exudates also showed declines in isoleucine, malic, succinic, citric, aspartic, gluconic, and threonic acids. These changes significantly altered rhizobacterial alpha and beta diversity, notably enriching taxa linked to plant growth-promoting rhizobacteria (PGPR) functions. In contrast, fungal communities were unaffected, indicating lower responsiveness to short-term root exudate shifts. This underscores the short-term substantial impact of airborne microplastics on plant–rhizosphere system functioning. Overall, the aerial microplastics rapidly propagate effects from foliage to roots, altering belowground chemistry and selectively reshaping microbial communities, with potential consequences for nutrient cycling, plant health, and ecosystem resilience.