Abstract
The present study introduces metabolic modeling as a new tool to analyze the network of redox reactions composing the superoxide dismutase-ascorbate (Asc)-glutathione (GSH) cycle. Based on previously determined concentrations of antioxidants and defense enzymes in chloroplasts, kinetic properties of antioxidative enzymes, and nonenzymatic rate constants of antioxidants with reactive oxygen, models were constructed to simulate oxidative stress and calculate changes in concentrations and fluxes of oxidants and antioxidants. Simulated oxidative stress in chloroplasts did not result in a significant accumulation of O2*- and H2O2 when the supply with reductant was sufficient. Model results suggest that the coupling between Asc- and GSH-related redox systems was weak because monodehydroascorbate radical reductase prevented dehydroascorbate (DHA) formation efficiently. DHA reductase activity was dispensable. Glutathione reductase was mainly required for the recycling of GSH oxidized in nonenzymatic reactions. In the absence of monodehydroascorbate radical reductase and DHA reductase, glutathione reductase and GSH were capable to maintain the Asc pool more than 99% reduced. This suggests that measured DHA/Asc ratios do not reflect a redox balance related to the Asc-GSH-cycle. Decreases in Asc peroxidase resulted in marked H2O2 accumulation without significant effects on the redox balance of Asc/DHA or GSH/GSSG. Simulated loss of SOD resulted in higher H2O2 production rates, thereby affecting all subsequent steps of the Asc-GSH-cycle. In conclusion, modeling approaches contribute to the theoretical understanding of the functioning of antioxidant systems by pointing out questions that need to be validated and provide additional information that is useful to develop breeding strategies for higher stress resistance in plants.
Highlights
The present study introduces metabolic modeling as a new tool to analyze the network of redox reactions composing the superoxide dismutase-ascorbate (Asc)-glutathione (GSH) cycle
Simulated oxidative stress in chloroplasts did not result in a significant accumulation of O2.Ϫ and H2O2 when the supply with reductant was sufficient
Model results suggest that the coupling between Asc- and GSH-related redox systems was weak because monodehydroascorbate radical reductase prevented dehydroascorbate (DHA) formation efficiently
Summary
MDA can be reduced by ferredoxin (Miyake and Asada, 1994) or by NAD(P)H in a reaction catalyzed by MDA reductase (MDAR, EC 1.1.5.4; Hossain and Asada, 1985) These mechanisms efficiently recycle Asc, it is inevitable that dehydroascorbate (DHA) is formed to some extent because of spontaneous disproportionation of MDA radicals to Asc and DHA (Fig. 1). By simple analysis of concentrations of antioxidants and activities of defense enzymes in plant tissues, it will not be possible to understand the regulation in the network of interacting redox reactions In this respect, a theoretical and quantitative understanding of functioning of the cycle will be necessary, which requires knowledge about the fluxes of oxidants and antioxidants. Metabolic Modeling of Antioxidative Systems enzymatic versus enzyme-catalyzed redox reactions for oxidant detoxification, (b) to estimate the relative contribution of different defense enzymes to the recycling of antioxidants, and (c) to explore the limits of the SOD-Asc-GSH cycle for stress compensation
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