Unmasking Spatial Heterogeneity in Phytotoxicology Mechanisms Induced by Carbamazepine by Mass Spectrometry Imaging and Multiomics Analyses

Previous
studies have highlighted the toxicity of pharmaceuticals
and personal care products (PPCPs) in plants, yet understanding their
spatial distribution within plant tissues and specific toxic effects
remains limited. This study investigates the spatial-specific toxic
effects of carbamazepine (CBZ), a prevalent PPCP, in plants. Utilizing
desorption electrospray ionization mass spectrometry imaging (DESI-MSI),
CBZ and its transformation products were observed predominantly at
the leaf edges, with 2.3-fold higher concentrations than inner regions,
which was confirmed by LC–MS. Transcriptomic and metabolic
analyses revealed significant differences in gene expression and metabolite
levels between the inner and outer leaf regions, emphasizing the spatial
location’s role in CBZ response. Notably, photosynthesis-related
genes were markedly downregulated, and photosynthetic efficiency was
reduced at leaf edges. Additionally, elevated oxidative stress at
leaf edges was indicated by higher antioxidant enzyme activity, cell
membrane impairment, and increased free fatty acids. Given the increased
oxidative stress at the leaf margins, the study suggests using in situ Raman spectroscopy for early detection of CBZ-induced
damage by monitoring reactive oxygen species levels. These findings
provide crucial insights into the spatial toxicological mechanisms
of CBZ in plants, forming a basis for future spatial toxicology research
of PPCPs.