Nanoplastic toxicity induces metabolic shifts in Populus × euramericana cv. '74/76' revealed by multi-omics analysis

• Published in: Journal of hazardous materials 2024-05, Vol.470, p.134148, Article 134148
• Main Authors: Xu, Liren, Liu, Chong, Ren, Yachao, Huang, Yinran, Liu, Yichao, Feng, Shuxiang, Zhong, Xinyu, Fu, Donglin, Zhou, Xiaohong, Wang, Jinmao, Liu, Yujun, Yang, Minsheng
• Format: Article
• Language: English
• Subjects: Chlorophyll - metabolism; Metabolomics; Multiomics; Nanoparticles - toxicity; Oxidative Stress - drug effects; Photosynthesis - drug effects; Plant Leaves - drug effects; Plant Leaves - metabolism; Plant Roots - drug effects; Plant Roots - metabolism; Polystyrenes - toxicity; Populus - drug effects; Populus - genetics; Populus - metabolism; Populus × euramericana cv. ‘74/76’; PS-NPs; Toxic effects; Transcriptomics
• ISSN: 0304-3894; 1873-3336; 1873-3336
• DOI: 10.1016/j.jhazmat.2024.134148

There is increasing global concern regarding the pervasive issue of plastic pollution. We investigated the response of Populus × euramericana cv. ‘74/76’ to nanoplastic toxicity via phenotypic, microanatomical, physiological, transcriptomic, and metabolomic approaches. Polystyrene nanoplastics (PS-NPs) were distributed throughout the test plants after the application of PS-NPs. Nanoplastics principally accumulated in the roots; minimal fractions were translocated to the leaves. In leaves, however, PS-NPs easily penetrated membranes and became concentrated in chloroplasts, causing thylakoid disintegration and chlorophyll degradation. Finally, oxidant damage from the influx of PS-NPs led to diminished photosynthesis, stunted growth, and etiolation and/or wilting. By integrating dual-omics data, we found that plants could counteract mild PS-NP-induced oxidative stress through the antioxidant enzyme system without initiating secondary metabolic defense mechanisms. In contrast, severe PS-NP treatments promoted a shift in metabolic pattern from primary metabolism to secondary metabolic defense mechanisms, an effect that was particularly pronounced during the upregulation of flavonoid biosynthesis. Our findings provide a useful framework from which to further clarify the roles of key biochemical pathways in plant responses to nanoplastic toxicity. Our work also supports the development of effective strategies to mitigate the environmental risks of nanoplastics by biologically immobilizing them in contaminated lands. [Display omitted] •Polystyrene nanoplastics (PS-NPs) are toxic to the woody model plant Poplar.•PS-NPs accumulated mainly in roots, with minimal amounts reaching leaves.•PS-NPs easily penetrated membranes systems, causing thylakoid disintegration.•PS-NPs caused shifts in metabolic patterns in a dose-dependent manner.•Flavonoids are crucial for defending poplar against a severe PS-NPs toxicity.