Nanoparticle-Elicited Eustress Intensifies Cucumber Plant Adaptation to Water Deficit

Under changing climates, engineering drought-resistant crops is critical for reducing food insecurity. Here, we leverage plant "stress memory" and ROS-generating silica nanoparticles (NPs) to enhance the drought tolerance of cucumber plants. Under PEG-mimicking drought conditions, cucumber seeds primed with fumed silica NPs (40 mg/L, 4 h) exhibited an increased seed germination rate (from 66.7 to 80.0%), enhanced seedling vigor (59.3%), and improved root and shoot length (24.4 and 74.1%, respectively) compared to seeds primed with water. In contrast, silicic acid and traditional silicon fertilizers at the same dose did not show priming effects, indicating that the released Si did not contribute to the observed outcomes. Metabolomics reveals that silica seed priming accelerated the mobilization of seed-stored reserves. Vegetative tissues also exhibit enhanced drought resistance, and metabolomics analysis reveals that the drought resistance strategy involves the upregulation of sugars (glucose, sucrose, trehalose, maltose; 34.7-74.8%), amino acids (methionine, 6-fold), signaling molecules (salicylic acid, 2.5-fold), and antioxidants (ascorbic acid, 2-hydroxycinnamic acid, ferulic acid, P-coumaric acid; 16.0-83.8%). Transcriptomics analysis reveals that several drought- and even desiccation-tolerant associated genes exert more pronounced transcript changes in silica-primed leaves. The life cycle study shows that silica seed priming does not generate any yield penalty or compromise the nutritional quality of the fruits. Importantly, offspring seeds exhibit enhanced vigor and drought tolerance, indicating the transgenerational transmission of the acquired drought resilience. The findings of this study provide a promising approach for engineering crops that are resilient to climate change.