Arabidopsis Iron Superoxide Dismutase FSD1 Protects Against Methyl Viologen-Induced Oxidative Stress in a Copper-Dependent Manner

Abstract

Iron superoxide dismutase 1 (FSD1) was recently characterized as a plastidial, cytoplasmic, and nuclear enzyme with osmoprotective and antioxidant functions. However, the current knowledge on its role in oxidative stress tolerance is ambiguous. Here, we characterized the role of FSD1 in response to methyl viologen (MV)-induced oxidative stress in Arabidopsis thaliana. In accordance with the known regulation of FSD1 expression, abundance, and activity, the findings demonstrated that the antioxidant function of FSD1 depends on the availability of Cu2+ in growth media. Arabidopsis fsd1 mutants showed lower capacity to decompose superoxide at low Cu2+ concentrations in the medium. Prolonged exposure to MV led to reduced ascorbate levels and higher protein carbonylation in fsd1 mutants and transgenic plants lacking a plastid FSD1 pool as compared to the wild type. MV induced a rapid increase in FSD1 activity, followed by a decrease after 4 h long exposure. Genetic disruption of FSD1 negatively affected the hydrogen peroxide-decomposing ascorbate peroxidase in fsd1 mutants. Chloroplastic localization of FSD1 is crucial to maintain redox homeostasis. Proteomic analysis showed that the sensitivity of fsd1 mutants to MV coincided with decreased abundances of ferredoxin and photosystem II light-harvesting complex proteins. These mutants have higher levels of chloroplastic proteases indicating an altered protein turnover in chloroplasts. Moreover, FSD1 disruption affects the abundance of proteins involved in the defense response. Collectively, the study provides evidence for the conditional antioxidative function of FSD1 and its possible role in signaling.

Genetic Mechanism of Non-Targeted-Site Resistance to Diquat in Spirodela polyrhiza

“…From a physiological point of view, the increased diquat resistance of SP050 was characterized by an increased SOD activity and stable antioxidant ratios under diquat exposure compared to susceptible genotypes. Such genotypic-specific changes in AsA/DHA ratios were previously related to differences in SOD activity [ 35 ]. Since the GSH/GSSG ratio and diquat tissue concentration were significantly correlated after 24h of diquat exposure, some of the observed differences in antioxidant ratios might be influenced by diquat uptake kinetics as well.…”

“…The quenching process of ROS occurs through the synergistic action of several enzymes, including the superoxide dismutase (SOD) via the conversion of the reductive metabolites AsA and GSH to their oxidized counterparts ( Figure 3 A), dehydroascorbate (DHA) and oxidized glutathione (GSSG), respectively. Therefore, we used the activity of SOD together with the ratios of AsA/DHA and GSH/GSSG as proxies to estimate antioxidant stress responses to diquat [ 23 , 24 , 34 , 35 ]. Diquat exposure decreased the GSH/GSSG and AsA/DHA levels in SP011 but not in SP050 ( Figure 3 B,C).…”

Co-regulation of mitochondrial and chloroplast function: Molecular components and mechanisms

“…Its localization in cytosol, chloroplasts, and mitochondria was observed in a variety of genetic mutants with disrupted mitochondrial complex I biogenesis and activity ( Wang et al., 2016 ). Depletion of At12Cys protein not only affects biogenesis/activity of the mitochondrial respiratory chain but also increases the protein abundance of Fe superoxide dismutase 1 ( Wang et al., 2016 ), a chloroplastic, cytoplasmic, and nuclear enzyme that performs an antioxidant function in a copper-dependent manner ( Dvořák et al., 2020 ; Melicher et al., 2022 ). These findings indicate that At12Cys protein not only affects respiratory chain biogenesis in mitochondria but also may impact ROS homeostasis in the chloroplasts, cytoplasm, and nucleus by affecting the abundance of Fe superoxide dismutase 1.…”

Protein-protein interactions in plant antioxidant defense

“…SODs respond to changes in external conditions via transcriptional, posttranscriptional and posttranslational regulation ( Dvořák et al., 2021b ). One of the major factors affecting expression of FSD1 and CSD genes is the availability of Cu 2+ ( Yamasaki et al., 2009 ; Yan et al., 2017 ; Melicher et al., 2022 ). Furthermore, expression of SOD genes also depends on diverse transcription factors under changing external conditions ( Dvořák et al., 2021b ).…”

“…Interestingly, AtCDC48A controls the degradation of intrachloroplastic proteins during oxidative stress and is vital for methyl viologen-induced oxidative stress tolerance ( Li et al., 2022 ). Indeed, abundances of cytosolic, stromal and thylakoid APX are hypersensitive to highly oxidative conditions induced by prolonged exposure to methyl viologen ( Melicher et al., 2022 ). Thus, CDC48 may govern APX, SOD and CAT degradation to modulate plant antioxidant defense and may play a key role as a regulator of the cellular redox status.…”