Metal and non-metal nanoparticles differentially regulate flavonoid accumulation in Cyclocarya paliurus: A multi-omics analysis

Abstract

Nanotechnology offers emerging tools for elevating metabolites levels in agricultural and medicinal crops, yet its regulatory effects on woody species remains underexplored. Cyclocarya paliurus, a precious tree species with flavonoid-linked antioxidant and hypoglycemic properties, was foliar-applied with nanoparticles (NPs) of ZnO, MnO₂, and SiO₂ to investigate their elicitation potential under field-simulated conditions. Compared with the control, applications of MnO₂- and SiO₂-NPs markedly increased total flavonoid content (TFC) in C. paliurus leaves by 21.26–49.99 %, and enhanced per-plant flavonoid accumulation by 40.70–50.06 %. Conversely, applications of high-dose ZnO-NPs induced oxidative imbalance, resulting in a 30.25 % and 43.84 % decline in TFC and flavonoid accumulation respectively. Multi-omics profiling revealed that both MnO₂- NPs and SiO₂-NPs activated ROS-dependent pathways involving MAPK and glutathione signaling, while SiO₂-NPs may also promote flavonoid biosynthesis via enhancing carbon fixation and primary metabolism. The MYB-bHLH-WD40 complex (including MYB113, bHLH42, and TTG1) was identified as a central regulatory node, ranking among the top 10 contributors in O2PLS analysis and exhibiting strong correlations (cor > 0.95) with flavonoid metabolites. Collectively, we propose a model wherein ROS signaling induced by NPs interacts with transcriptional networks to modulate flavonoid accumulation. This work provides a nano-enabled strategy to boost health-promoting compounds in the woody plants.