From the shoot to the rhizosphere

Author(s)
Oussama Bouaicha, Fabio Trevisan, Raphael Tiziani, Martin Brenner, Wolfram Weckwerth, Elisabetta Onelli, Alessandra Moscatelli, Tanja Mimmo, Luigimaria Borruso
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.

Organisation(s)
Functional and Evolutionary Ecology
External organisation(s)
Free University of Bozen-Bolzano, Università degli Studi di Milano-Bicocca
Journal
Environmental and Experimental Botany
Volume
237
ISSN
0098-8472
DOI
https://doi.org/10.1016/j.envexpbot.2025.106222
Publication date
09-2025
Peer reviewed
Yes
Austrian Fields of Science 2012
106031 Plant physiology
Keywords
ASJC Scopus subject areas
Ecology, Evolution, Behavior and Systematics, Agronomy and Crop Science, Plant Science
Portal url
https://ucrisportal.univie.ac.at/en/publications/be46bc6f-e486-4880-8ad0-f1f056acbc6e