The impact of engineered nickel oxide nanoparticles on ascorbate glutathione cycle in Allium cepa L

Abstract

Engineered nickel oxide nanoparticle (NiO-NP) can inflict significant damages on exposed plants, even though very little is known about the modus operandi. The present study investigated effects of NiO-NP on the crucial stress alleviation mechanism Ascorbate-Glutathione Cycle (Asa-GSH cycle) in the model plant Allium cepa. Cellular contents of reduced glutathione (GSH) and oxidised glutathione (GSSG), was disturbed upon NiO-NP exposure. The ratio of GSH to GSSG changed from 20:1 in NC to 4:1 in roots exposed to 125 mg L^-1 NiO-NP. Even the lowest treatments of NiO-NP (10 mg L^-1) increased ascorbic acid (2.9-folds) and cysteine contents (1.6-folds). Enzymes like glutathione reductase, ascorbate peroxidase, glutathione peroxidase and glutathione-S-transferase also showed altered activities in the affected tissues. Further, intracellular methylglyoxal, a harbinger of ROS (Reactive oxygen species), increased significantly (~ 26 to 65-fold) across different concentrations NiO-NP. Intracellular H₂O₂ (hydrogen peroxide) and ROS levels increased with NiO-NP doses, as did electrolytic leakage from damaged cells. The present work indicated that multiple pathways were compromised in NiO-NP affected plants and this information can bolster our general understanding of the actual mechanism of its toxicity on living cells, and help formulate strategies to thwart ecological pollution.

Supplementary information: The online version contains supplementary material available at 10.1007/s12298-023-01314-8.

Keywords: Antioxidants; Engineered nanoparticle hazard; Environmental pollutant; GSH:GSSG ratio; Methylglyoxal; ROS; Reduced glutathione.

Fig. 1

Generalized view of ascorbate-glutathione (Asa-GSH) cycle (modified from Noctor et al. ; without using any original image or idea subjected to copyright; ASC-Ascorbate; MDHA-Monodehydroascorbaste; DHA-Dehydroascorbate; MDHAR-Monodehydroascorbate reductase; APX-Ascorbate peroxidase; DHAR-Dehydroascorbate reductase; GRX-Glutaredoxins; NAD(P)⁺/NAD(P)H-Nicotinamide-adenine dinucleotide phosphate

Fig. 2

Relative electrolyte leakage in Allium cepa roots on NiO-NP exposure; At least 5 data sets were used for statistical analyses; Different letters at the top of the bars represent significant differences (p < 0.005) between the treatments after performing One-way ANOVA

Fig. 3

a-f Effect of increasing NiO-NP concentration on integrity of cellular membrane in experimental samples detected through SEM imaging (a-negative control, b-10, c-50, d-125, e-250, f-500 mg L⁻¹ of NiO-NP respectively; magnification ~ 400X

Fig. 4

a Reduced glutathione (GSH) content in Allium cepa roots on NiO-NP exposure; b Oxidised glutathione (GSSG) content in Allium cepa roots on NiO-NP exposure; At least 5 data sets were used for statistical analyses; Different letters at the top of the bars represent significant differences (p < 0.005) between the treatments after performing One-way ANOVA

Fig. 5

a-f Effect of increasing NiO-NP concentration on reduced glutathione (GSH) content in the treated samples following monochlorobimane staining documented through LSCM (a-negative control, b-25, c-50, d-125, e-250 and f-500 mg L⁻¹ of NiO-NP respectively; bar represented 130 μm)

Fig. 6

a Methylglyoxal content; b Cysteine content in Allium cepa roots on NiO-NP exposure; At least 5 data sets were used for statistical analyses; Different letters at the top of the bars represent significant differences (p < 0.005) between the treatments after performing One-way ANOVA

Fig. 7

Ascorbate content in Allium cepa roots on NiO-NP exposure; At least 5 data sets were used for statistical analyses; Different letters at the top of the bars represent significant differences (p < 0.005) between the treatments after performing One-way ANOVA

Fig. 8

Effect of NiO-NP exposure on enzyme activities in Allium cepa roots. a Glutathione reductase (GR) activity; b Ascorbate peroxidase (APX) activity; c Glutathione peroxidase (GPx) activity; d Glutathione transferase (GST); At least 5 data sets were used for statistical analyses; Different letters at the top of the bars represent significant differences (p < 0.005) between the treatments after performing One-way ANOVA

Fig. 9

Schematic presentation of possible mechanism of NiO-NP affected Asa-GSH cycle and cell cycle in A. cepa roots (Prepared by the authors without using any copyrighted images/objects)