Physiological, transcriptomic and metabolomic analyses reveal the mechanism of CuO and silicon nanoparticles involved in Polygonatum kingianum response to root rot

Copper oxide nanoparticles (CuNPs) and silicon nanoparticles (SiNPs) play a crucial role in enhancing plant growth and development under stress conditions, making them valuable tools in sustainable agriculture. However, the mechanisms by which CuNPs and SiNPs influence plant responses to root rot remain poorly understood. This study integrated physiological, transcriptomic, and metabolomic analyses to elucidate the potential mechanisms of Polygonatum kingianum, a well-known medicinal plant, in response to root rot induced by Fusarium oxysporum. The results demonstrated that F. oxysporum inoculation severely induced root rot in P. kingianum, leading to rhizome decay, reduced root biomass, and impaired leaf photosynthetic capacity. In contrast, foliar application of CuNPs and SiNPs significantly enhanced P. kingianum against rhizome rot, with relative therapeutic effects increasing by 48.68% and 50.31%, respectively, thereby showing an increment in the growth of the seedling. In addition, these nanoparticles modulated the balance of ROS and antioxidant abundance, improved mineral element content, and thereby enhanced photosynthetic ability under root rot conditions. CuNPs and SiNPs reprogrammed differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) involved in photosynthesis, carbon fixation via the Calvin cycle, glycolysis/gluconeogenesis, starch and sucrose metabolism, the TCA cycle, glutathione metabolism, flavonoid metabolism, and phenylpropanoid metabolism, thus modulating P. kingianum against rhizome rot through primary and secondary metabolic pathways. Combined KEGG enrichment analysis of DEGs and DAMs revealed that cysteine and methionine metabolism, ABC transporters, flavonoid biosynthesis, purine metabolism, and plant hormone signal transduction were enriched upon CuNPs treatment, whereas cysteine and methionine metabolism, pyruvate metabolism, and galactose metabolism were significantly enriched upon SiNPs treatment. A Pearson coefficient analysis showed that 22 genes were positively correlated with the disease index under CuNP treatment, while 27 genes were positively correlated under SiNP treatment. Furthermore, 27 common DAMs related to flavonoid metabolism, isoflavonoid metabolism, and amino acid metabolism were identified in seedlings treated with both CuNPs and SiNPs. CuNPs or SiNPs enhanced the resistance of P. kingianum to root rot through the regulation of osmoprotectant and ROS homeostasis, modulation of mineral element accumulation, and reprogramming of key transcriptional and metabolic pathways, highlighting the potential of NPs in preventing root diseases in medicinal plants.