Organ-specific secondary metabolism under elevated CO2 enhances gadolinium detoxification in tomato (Solanum lycopersicum)

Rare earth elements are emerging environmental pollutants, and gadolinium (Gd) contamination poses a potential risk to global plant production. This study investigated how future climate conditions influence Gd toxicity in tomatoes ( Solanum lycopersicum ) using a two-factor design combining soil Gd contamination (150 mg/kg) and elevated CO₂ (eCO₂; 620 ppm). High Gd exposure severely impaired plant growth, reducing shoot and root biomass, increasing hydrogen peroxide (H₂O₂) levels in tomato shoots (82%) and roots (36%), and causing mineral deficiencies. eCO₂ partially buffered these effects, enhancing baseline root DW by 150% and 120%, respectively and improving nutrient balance in Gd-stressed plants. eCO₂ induced detoxification responses were organ-specific, with roots primarily accumulating phytochelatins (76%), while shoots synthesized metallothioneins (124%). Antioxidant defenses were spatially differentiated: shoots relied primarily on ascorbate peroxidase (APX), whereas roots used both non-enzymatic antioxidants (phenols, tocopherols, ascorbate) and enzymatic defenses (catalase (CAT) and glutathione reductase). Consistently, the expression of these key enzymes (e.g., APX, CAT) were also upregulated. Importantly, eCO₂ alleviated reduced oxidative damage and induced antioxidant defense including anthocyanin biosynthetic pathway, a key defense against metal-induced oxidative stress. eCO₂ enhanced phenylpropanoid flux by increasing the availability of phenylalanine, cinnamic acid, and naringenin, along with higher activities of phenylalanine ammonia-lyase (PAL) and chalcone synthase (CHS). This metabolic shift suggests that eCO₂ strengthens the biochemical defense of tomato against Gd toxicity, potentially mitigating the agricultural risks associated with rare earth element pollution.