Foliar Application of Zinc Oxide Nanoparticles Alleviates Phenanthrene and Cadmium-Induced Phytotoxicity in Lettuce: Regulation of Plant–Rhizosphere–Microbial Long Distance

Foliar application of beneficial nanoparticles exhibits potential in mitigating combined stresses from heavy metals and polycyclic aromatic hydrocarbons (PAHs) in crops, necessitating a comprehensive understanding of plant-rhizosphere-microbial processes to promote sustainable nanotechnology in agriculture. Herein, we investigated the mitigating mechanisms of foliar application of zinc oxide nanoparticles (<i>n</i>ZnO) on lettuce growth under phenanthrene (Phe) and cadmium (Cd) costress. Compared to Phe + Cd treatment, low (L-<i>n</i>ZnO) and high (H-<i>n</i>ZnO) concentration of <i>n</i>ZnO increased fresh biomass (27.2% and 8.42%) and root length (20.4% and 39.6%) and decreased MDA (35.0% and 40.0%) and H₂O₂ (29.0% and 15.6%) levels. L-<i>n</i>ZnO and H-<i>n</i>ZnO decreased Cd in roots (26.8% and 41.8%) and enhanced Zn in roots (19.9% and 107%), stems (221% and 2510%), and leaves (233% and 1500%), suggesting the long-distance migration of Zn from leaves to roots and subsequently regulating the metabolic pathways and microbial communities. Metabolomics revealed that <i>n</i>ZnO modulated leaf glycerophospholipid metabolism and amino acid pathways and promoted rhizosphere soil carbon and phosphorus metabolism. Additionally, <i>n</i>ZnO enriched the plant-growth-promoting, extreme, and stress-resistant bacteria in roots and leaves and heavy-metal-resistant and PAH-degrading bacteria in rhizosphere soil. These findings underscore the promising nanostrategy of <i>n</i>ZnO to benefit plant growth in soil cocontaminated with heavy metals and PAHs.