Route-Specific Phytotoxicity: Foliar Polystyrene Nanoplastics Inhibit Rice Photosynthesis

We examine the effects of polystyrene (PS) NPs at 5.4 ± 1.0 nm on rice (Oryza sativa L.) under two scenarios: a comparative 14-day hydroponic exposure (3.6–35.7 μg PS plant–1 d–1) of root vs foliar exposure and a 30-day soil-based foliar exposure (5.3–73.4 μg PS plant–1 d–1) from heading to maturity. PS NPs exhibit route-specific phytotoxicity: while only high-dose root exposure inhibits photosynthesis, foliar exposure causes sustained inhibition. Importantly, soil-based foliar exposure also inhibits photosynthesis without the PS NP translocation to grains. This foliar-specific inhibition correlates directly with PS accumulation in leaves and is mechanistically attributed to its colocalization with chloroplasts (Pearson’s r = 0.592), as confirmed by confocal imaging in high-dose (35.7 μg PS plant–1 d–1) exposed leaf. The colocalization impairs both the light-dependent reactions and carbon fixation during photosynthesis, as evidenced by significant reductions in photosynthetic pigments (54.4–61.0%), Hill reaction activity (49.9–70.2%), ATP production (22.1–24.3%), net photosynthetic rate (84.5–89.0%), Rubisco activity (84.6–87.5%), stomatal conductance (47.9–69.5%), and transpiration rate (47.4–48.9%). Transcriptomic analysis identifies the genetic basis of this inhibition, showing significant downregulation of the core photosynthesis pathway and key genes for photosynthetic-antenna proteins, carbon fixation, and carotenoid/porphyrin metabolism. These findings provide mechanistic insights into PS NP-induced photosynthesis inhibition and underscore atmospheric NPs as an emerging threat to global food security.