Quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through ASA-GSH cycle modulating redox homeostasis of roots and ROS-mediated root-hair elongation

Abstract

Background Various environmental factors are capable of oxidative stress to result in limiting plant development and agricultural production. Fullerene-based carbon nanomaterials can enable radical scavenging and positively regulate plant growth. Even so, to date, our knowledge about the mechanism of fullerene-based carbon nanomaterials on plant growth and response to oxidative stress is still unclear. Results 20 or 50 mg/L quaternary ammonium iminofullerenes (IFQA) rescued the reduction in root lengths and root-hair densities and lengths of Arabidopsis and maize induced by accumulation of endogenous hydrogen peroxide (H2O2) under 3-amino-1,2,4-triazole or exogenous H2O2 treatment, as well as the root active absorption area and root activity under exogenous H2O2 treatment. Meanwhile, the downregulated contents of ascorbate acid (ASA) and glutathione (GSH) and the upregulated contents of dehydroascorbic acid (DHA), oxidized glutathione (GSSG), malondialdehyde (MDA), and H2O2 indicated that the exogenous H2O2 treatment induced oxidative stress of maize. Nonetheless, application of IFQA can increase the ratios of ASA/DHA and GSH/GSSG, as well as the activities of glutathione reductase, and ascorbate peroxidase, and decrease the contents of H2O2 and MDA. Moreover, the root lengths were inhibited by buthionine sulfoximine, a specific inhibitor of GSH biosynthesis, and subsequently rescued after addition of IFQA. The results suggested that IFQA could alleviate exogenous-H2O2-induced oxidative stress on maize by regulating the ASA-GSH cycle. Furthermore, IFQA reduced the excess accumulation of ROS in root hairs, as well as the NADPH oxidase activity under H2O2 treatment. The transcript levels of genes affecting ROS-mediated root-hair development, such as RBOH B, RBOH C, PFT1, and PRX59, were significantly induced by H2O2 treatment and then decreased after addition of IFQA. Conclusion The positive effect of fullerene-based carbon nanomaterials on maize-root-hair growth under the induced oxidative stress was discovered. Application IFQA can ameliorate oxidative stress to promote maize-root growth through decreasing NADPH-oxidase activity, improving the scavenging of ROS by ASA-GSH cycle, and regulating the expressions of genes affecting maize-root-hair development. It will enrich more understanding the actual mechanism of fullerene-based nanoelicitors responsible for plant growth promotion and protection from oxidative stress. Graphical Abstract

Root Hair Development and Adaptation to Abiotic Stress

“…This effect is because H 2 O 2 treatment increases expression of genes related to root hair development, such as RBOHB and RBOHC, but IFQA decreases the accumulation of oxidative stress-related ROS and thus the activity of NADPH oxidase. 180 ROS results in AF bundling. The der1-3 mutant of ACTIN2 showed shorter, thinner AFs.…”

“…Exogenous H 2 O 2 inhibits root hair density and mean root hair length in Arabidopsis , but this inhibition is alleviated by application of exogenous quaternary ammonium iminofullerenes (IFQA). This effect is because H 2 O 2 treatment increases expression of genes related to root hair development, such as RBOHB and RBOHC , but IFQA decreases the accumulation of oxidative stress-related ROS and thus the activity of NADPH oxidase …”

Influence of nanocompositions based on light fullerene derivatives on cultural plants under favorable and stress conditions of their habitat

“…The influence of fullerene derivatives like other nanomaterials is defined by their sizes, composition of functional groups, concentration, and species differences in plant response and environmental conditions [1,19,20]. Positive effect of the specified compounds on plants is probably associated with antioxidant activity, in particular with capability of binding reactive oxygen intermediates as was clearly shown on the barley plant example [21,22].…”

Physiological, biochemical, and metabolic changes in diploid and triploid watermelon leaves during flooding

“…Studies showed that APX is the most important scavenging enzyme ensuring the scavenging capability of reactive oxygen species ( Czarnocka and Karpiński, 2018 ). Furthermore, it has been previously reported that for mitigating and enhancing stress tolerance AsA/DHA ratios are far more important than AsA contents ( Szalai et al., 2009 ; Yu et al., 2021 ; Tai et al., 2022 ). Current results revealed lower AsA/DHA as well as GSH/GSSG ratios in 3X watermelon as compared to 2X.…”