Metabolomics Reveals How Cucumber (Cucumis sativus) Reprograms Metabolites To Cope with Silver Ions and Silver Nanoparticle-Induced Oxidative Stress

Abstract

Due to their well-known antifungal activity, the intentional use of silver nanoparticles (AgNPs) as sustainable nanofungicides is expected to increase in agriculture. However, the impacts of AgNPs on plants must be critically evaluated to guarantee their safe use in food production. In this study, 4-week-old cucumber (Cucumis sativus) plants received a foliar application of AgNPs (4 or 40 mg/plant) or Ag⁺ (0.04 or 0.4 mg/plant) for 7 days. Gas chromatography–mass spectrometry (GC-MS)=based nontarget metabolomics enabled the identification and quantification of 268 metabolites in cucumber leaves. Multivariate analysis revealed that all the treatments significantly altered the metabolite profile. Exposure to AgNPs resulted in metabolic reprogramming, including activation of antioxidant defense systems (upregulation of phenolic compounds) and downregulation of photosynthesis (upregulation of phytol). Additionally, AgNPs enhanced respiration (upregulation of tricarboxylic acid cycle intermediates), inhibited photorespiration (downregulation of glycine/serine ratio), altered membrane properties (upregulation of pentadecanoic and arachidonic acids, downregulation of linoleic and linolenic acids), and reduced inorganic nitrogen fixation (downregulation of glutamine and asparagine). Although Ag ions induced some of the same metabolic changes, alterations in the levels of carbazole, lactulose, raffinose, citraconic acid, lactamide, acetanilide, and p-benzoquinone were AgNP-specific. The results of this study offer new insight into the molecular mechanisms by which cucumber responds to AgNP exposure and provide important information to support the sustainable use of AgNPs in agriculture.