Influences of sulfonated graphene oxide on gas exchange performance, antioxidant systems and redox states of ascorbate and glutathione in nitrate and/or ammonium stressed-wheat (Triticum aestivum L.)

Abstract

Graphene oxide has unique physiochemical properties and a large surface area. After functionalization, its shape, surface, adsorption capacity, and toxicity levels can change. The potential impacts of sulfonated graphene oxide (SGO, modified with the sulfonic group) on metabolic processes and biological pathways are unanswered questions concerning NO₃⁻ or NH₄⁺ toxicity. To fill this gap of knowledge, in the present study, SGO (50–250–500 mg L⁻¹) was applied to Triticum aestivum cv. Ekiz with/without 140 mM nitrate (NS stress) and 5 mM ammonium (AS stress). Both stress treatments suppressed the growth, water content, osmotic potential, and photosynthetic capacity, as detected by a decrease in the carbon assimilation rate (A), stomatal conductance (g_s), intercellular CO₂ concentration (C_i), and transpiration rate (E), and an increase in stomatal limitation. After stress exposure, SGO provided positive responses to these parameters. There were different responses in the antioxidant system under stress: superoxide dismutase (SOD) and peroxidase (POX) under NS stress; SOD, catalase (CAT) and POX under AS and NS + AS stresses. However, hydrogen peroxide (H₂O₂) and lipid peroxidation increased because lack of effective antioxidant activation. In response to NS or AS, SGO successfully regulated SOD, CAT, glutathione peroxidase (GPX) and the enzyme/non-enzymes related to the AsA–GSH cycle, attenuating the high levels of H₂O₂, lipoxygenase (LOX) and TBARS-based damage. Along with the antioxidant system, SGO controlled the contents of NO₃⁻ or NH₄⁺ by regulation of NPF6.3 and AMT1.2 genes. Interestingly, under NS plus AS, the alleviation action of SGO varied in a concentration-dependent manner: (i) low SGO concentration (50 mg L⁻¹) protected the regeneration of ascorbate (AsA) and glutathione (GSH) and the high activities of GST and GPX; (ii) 250 mg L⁻¹ SGO maintained the GSH redox state and the induced activity of glutathione S-transferase (GST); (iii) the highest SGO concentration (500 mg L⁻¹) did not eliminate H₂O₂ accumulation, which coincided with the increased levels of TBARS and LOX. The toxicity of the high SGO concentration was further increased in wheat with non-stress or NS plus AS stresses. Our findings specified that the damage stimulated by NS and/or AS stress was removed by SGO applications through the increased antioxidant activity and gas exchange parameters, resulting in the protection of the redox state.