"Nanophytovirology" is a potential management approach to combat plant viral diseases. Herein, the impact of foliar application of CeO nanoparticles (CeO-NPs) on the growth, plant cell ultrastructure, and physiology of alfalfa mosaic virus (AMV)-infected alfalfa seedlings was explored at different concentrations and application strategies. In a solar greenhouse, 20 mL of CeO-NP suspensions of 50, 100, 200, and 500 mg/L was sprayed onto the plant surface every other day for 9 days. As a result, the total volume applied per pot was 100 mL. It showed that the beneficial effects of CeO-NPs on infected alfalfa seedlings were dependent on the concentration and application period. Compared to the infected control, foliar application with 100 mg/L CeO-NPs before AMV infection (CeO-NPs-BVI) showed the greatest virus suppression efficacy; significantly reduced the disease indices by 58.87%; improved growth, yield, and nutritional quality; and significantly increased plant height, plant dry biomass, crude protein, and crude fat contents and relative feeding value by 15.17, 37.12, 18.77, 71.19, and 10.09%, respectively. Moreover, CeO-NPs-BVI maintained the chloroplast quantity and structure of leaf cells and significantly enhanced the chlorophyll content and photosynthesis rate of alfalfa leaves by 36.14 and 40.13%, respectively, as compared to infected control. Mechanistically, cell ultrastructure, physiology, and transcriptomic analyses revealed that (1) CeO-NPs effectively mitigated AMV-induced chloroplast structure damage, subsequently enhancing photosynthesis and carbon fixation in photosynthetic organisms, providing sufficient energy and antiviral activities for maintaining plant growth and development; (2) CeO-NPs reduced the AMV's ability to bind to host receptors and evade host immune recognition, significantly activating and boosting plant systemic immunity by down-regulating ABA and ETH levels and upregulating SA, IAA, and BR levels; (3) CeO-NPs activated the plant antioxidative systems to eliminate excess reactive oxygen species. These findings provide significant insight into the potential of CeO-NPs as highly efficient antiviral agent.
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