Shoot-root hormonal coordination and cross-sphere microbiome assembly underpin nanomaterial-induced resistance to...

Mining-induced rare earth elements (REEs) pollution in agricultural soil threatens food security, necessitating effective remediation strategies. Foliar-applied nanoparticles (NPs) offer a promising approach, while their potential in alleviating REEs-induced stress in crops remains insufficiently understood, particularly the systemic phytohormone-mediated responses and associated microbiome assembly that are crucial for plant resilience. Here, we demonstrated that SiO₂-NPs and MnO₂-NPs (0.5 and 1.25 mg/day/plant) significantly promoted lettuce growth (up to 3.02-fold) and reduced REEs accumulation (up to 74.0%/91.2% in roots/shoots). Concurrently, plant nutritional status and photosynthesis activity were improved, with SiO₂-NPs specifically contributing to enhanced energy homeostasis. Gene set enrichment analysis (GSEA) revealed that NPs treatments activated plant resistance system, with SiO₂-NPs specifically promoting the biosynthesis of stress resistance-related compounds and MnO₂-NPs tending to regulate phytohormone signal transduction process. Crucially, these transcriptional responses were closely correlated to multiple phytohormones modulated by NPs in both shoots and roots, including auxin and jasmonates, as identified by weighted gene co-expression network analysis (WGCNA). Furthermore, NPs reshaped phyllosphere and rhizosphere microbiomes, such as Pseudomonadota, Cyanobacteriota and Bacillota. Notably, rhizosphere microbiome exhibited a strong correlation with phytohormone levels in shoots and roots, revealing the existence of a hormone-microbiome regulatory network that facilitates whole-plant adaptation to REEs stress. These findings underscore the pivotal role of NPs-induced phytohormonal signaling in coordinating shoot-root stress resistance and modulating microbiome composition under REEs contamination, providing mechanistic insights for developing NPs-based strategies to safeguard food production.