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Soil contamination with indium (In) oxide nanoparticles (In2O3-NPs) threatens plant growth and development. However, their toxicity in plants under ambient (aCO(2)) and elevated (eCO(2)) conditions is scarcely studied. To this end, this study was conducted to investigate In2O3-NPs toxicity in the young and old leaves of C3 (barley) and C4 (maize) plants and to understand the mechanisms underlying the stress mitigating impact of eCO(2). Treatment of C3 and C4 plants with In2O3-NPs significantly reduced growth and photosynthesis, induced oxidative damage (H2O2, lipid peroxidation), and impaired P and Fe homeostasis, particularly in the young leaves of C4 plants. On the other hand, this phytotoxic hazard was mitigated by eCO(2) which improved both C3 and C4 growth, decreased In accumulation and increased phosphorus (P) and iron (Fe) uptake, particularly in the young leaves of C4 plants. Moreover, the improved photosynthesis by eCO(2) accordingly enhanced carbon availability under the challenge of In2O3-NPs that were directed to the elevated production of metabolites involved in antioxidant and detoxification systems. Our physiological and biochemical analyses implicated the role of the antioxidant defenses, including superoxide dismutase (SOD) in stress mitigation under eCO(2). This was validated by studying the effect of In2O3-stress on a transgenic maize line (TG) constitutively overexpressing the AtFeSOD gene and its wild type (WT). Although it did not alter In accumulation, the TG plants showed improved growth and photosynthesis and reduced oxidative damage. Overall, this work demonstrated that C3 was more sensitive to In2O3-NPs stress; however, C4 plants were more responsive to eCO(2). Moreover, it demonstrated the role of SOD in determining the hazardous effect of In2O3-NPs.

Soil contamination with indium oxide nanoparticles (In2O3-NPs) is a challenge for plant growth and productivity. Despite In2O3-NPs toxicity, their effects on plant growth and metabolism are largely unknown, particularly under future climate CO2 (eCO(2)). Therefore, the In2O3-NPs toxicity and stress mitigating impact of eCO(2) in the young and old leaves of C3 (wheat) and C4 (sorghum) plants were investigated. Overall, In2O3-NPs significantly retard the biomass and photosynthetic machinery of all tested crops, particularly the young leaves of C3 plants. Consequently, In2O3-NPs altered C and N metabolism in C3 and C4 plants. On the other hand, eCO(2) contrarily alleviated the hazardous effects of In2O3-NPs on growth and photosynthesis, especially in the young leaves of C4 plants. Increased photosynthesis consequently enhanced the soluble sugars' accumulation and metabolism (e.g., sucrose P synthase, cytosolic, and vacuolar invertase) in all stressed plants, but to a greater extent in C4 young leaves. High sugar availability also induced TCA organic and fatty acids' accumulation. This also provided a route for amino acids and polyamines biosynthesis, where a clear increase in proline biosynthetic enzymes [e.g., pyrroline-5-carboxylate synthetase (P5CS), ornithine aminotransferase (OAT), Pyrroline-5-carboxylate reductase (P5CR), pyrroline-5-carboxylate dehydrogenase (P5CDH), and proline dehydrogenase (PRODH)] and polyamine metabolic enzymes (e.g., spermine and spermidine synthases, ornithine decarboxylase, and adenosyl methionine decarboxylase) were mainly recorded in C4 young leaves. The observed increases in these metabolites involved in osmo- and redox-regulation to reduce In2O3-NPs induced oxidative damage. Overall, our study, for the first time, shed light on how eCO(2) differentially mitigated In2O3-NPs stress in old and young leaves of different species groups under the threat of In2O3-NPs contamination.