Under a changing climate, cultivating climate-resilient
crops will
be critical to maintaining food security. Here, we propose the application
of reactive oxygen species (ROS)-generating nanoparticles as nanobiostimulants
to trigger stress/immune responses and subsequently increase the stress
resilience of plants. We established three regimens of silver nanoparticles
(AgNPs)-based “stress training”: seed training (ST),
leaf training (LT), and combined seed and leaf training (SLT). Trained
rice seedlings were then exposed to either rice blast fungus (Magnaporthe oryzae) or chilling stress (10 °C). The
results show that all “stress training” regimes, particularly
SLT, significantly enhanced the resistance of rice against the fungal
pathogen (lesion size reduced by 82% relative to untrained control).
SLT also significantly enhanced rice tolerance to cold stress. The
mechanisms for the enhanced resilience were investigated with metabolomics
and transcriptomics, which show that “stress training”
induced considerable metabolic and transcriptional reprogramming in
rice leaves. AgNPs boosted ROS-activated stress signaling pathways
by oxidative post-translational modifications of stress-related kinases,
hormones, and transcriptional factors (TFs). These signaling pathways
subsequently modulated the expression of defense genes, including
specialized metabolites (SMs) biosynthesis genes, cell membrane lipid
metabolism genes, and pathogen–plant interaction genes. Importantly,
results showed that the “stress memory” can be transferred
transgenerationally, conferring offspring seeds with improved seed
germination and seedling vigor. This may provide an epigenetic breeding
strategy to fortify stress resilience of crops. This nanobiostimulant-based
stress training strategy will increase yield vigor against a changing
climate and will contribute to sustainable agriculture by reducing
agrochemical use.