Clonal integration orchestrates a plant-microbe alliance for systemic resilience to copper-based nanopesticides

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Engineered nanomaterials particularly copper oxide nanoparticles (CuO NPs) are being rapidly integrated into modern agriculture as highly efficient and multifunctional nanoagrochemicals to enhance crop management and sustainability. However, their ecological risk assessments remain fundamentally constrained by conventional single-plant toxicity assays, which critically overlook the trans-ramet consequences and microbial crosstalk central to clonally propagating crops. This study reveals how clonal strawberry plants ( Fragaria × ananassa ) leverage physiological integration to orchestrate a synergistic plant-microbe defense network against CuO NP stress. Using a split-pot system, we demonstrate that stolon-mediated connectivity enables parent plants to not only resist toxicity but also transform mild stress into a growth advantage (19.44%-22.82% biomass), while fully protecting offspring ramets from oxidative damage. This systemic clonal resilience is underpinned by a coordinated strategy of acropetal NP translocation and selective microbiome assembly. Parents enrich and vertically transmit key beneficial symbionts (e.g., Rhizomicrobium and Pseudolabrys ) carrying metal-resistance genes ( cusA, cusB and cueR ), a process driven by root exudate reprogramming. The recruited microbiome functions simultaneously in metal immobilization and nutrient acquisition, sustaining offspring fitness. Crucially, this system maintains offspring levels of proteins, vitamins, and starch while activating specialized defense pathways, including flavonoid biosynthesis and phytohormonal signaling. Our findings illuminate a cooperative defense mechanism, orchestrated through clonal integration, that converts nanomaterial exposure into a systemic adaptive advantage. This work provides critical insights into the ecological risk assessment of NPs specifically within stoloniferous clonal agroecosystems, and offers a novel framework for leveraging plant-microbe interactions in sustainable agriculture.

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