Compartment-specific importance of glutathione during abiotic and biotic stress

Abstract

The tripeptide thiol glutathione (γ-L-glutamyl-L-cysteinyl-glycine) is the most important sulfur containing antioxidant in plants and essential for plant defense against abiotic and biotic stress conditions. It is involved in the detoxification of reactive oxygen species (ROS), redox signaling, the modulation of defense gene expression, and the regulation of enzymatic activities. Even though changes in glutathione contents are well documented in plants and its roles in plant defense are well established, still too little is known about its compartment-specific importance during abiotic and biotic stress conditions. Due to technical advances in the visualization of glutathione and the redox state through microscopical methods some progress was made in the last few years in studying the importance of subcellular glutathione contents during stress conditions in plants. This review summarizes the data available on compartment-specific importance of glutathione in the protection against abiotic and biotic stress conditions such as high light stress, exposure to cadmium, drought, and pathogen attack (Pseudomonas, Botrytis, tobacco mosaic virus). The data will be discussed in connection with the subcellular accumulation of ROS during these conditions and glutathione synthesis which are both highly compartment specific (e.g., glutathione synthesis takes place in chloroplasts and the cytosol). Thus this review will reveal the compartment-specific importance of glutathione during abiotic and biotic stress conditions.

Keywords: abiotic stress; biotic stress; chloroplasts; drought; glutathione; mitochondria; nuclei; peroxisomes.

FIGURE 1

The ascorbate–glutathione cycle in plants. Hydrogen peroxide (H₂O₂) within the plant cell can be detoxified by ascorbate peroxidase (APX). In this reaction, the reduced form of ascorbate (Asc) is oxidized to monodehydroascorbate (MDHA). MDHA is then either reduced by monodehydroascorbate reductase (MDHAR) to Asc or, since very unstable, reacts to dehydroascorbate (DHA). DHA is reduced by dehydroascorbate reductase (DHAR) to Asc. In this reaction, the reduced form of glutathione (GSH) is oxidized to glutathione disulfide (GSSG). GSSG is then reduced by glutathione reductase (GR) to GSH. The electron acceptor NADP is regenerated during the reduction of MDHA and GSSG by the respective enzymes. Asc and GSH are additional able to detoxify reactive oxygen species by direct chemical interaction. Thus, besides the total ascorbate and glutathione level their redox state (reduced vs. oxidized state) which depends on the activity of the described enzymes (gray boxes) is also very important for successful plant protection.

FIGURE 2

Compartment-specific production of reactive oxygen species (ROS) induced by different stress conditions and possible detoxification and signaling pathways involving ascorbate (Asc) and glutathione (GSH) and ROS. C, chloroplast; M, mitochondrium; N, nucleus; Px, peroxisome; V, vacuole.

FIGURE 3

Images show the typical distribution of glutathione. (A) Monochlorobimane staining in guard cells of the upper epidermis of tobacco cells in the light microscope. Fluorescence was observed in cytosol and nuclei (N) but not in vacuoles (V) and cell walls (arrowhead). Additionally, no fluorescence could be observed in chloroplasts (arrows in A and B) which can be best identified when comparing the autofluorescence of chloroplast (B) with monochlorobimane staining (A). Transmission electron micrographs show the subcellular distribution of glutathione (C,D) in mesophyll cells of leaves from Arabidopsis Col-0 plants. Glutathione-specific labeling could be observed in different concentrations in mitochondria (M), chloroplasts (C), peroxisomes (Px) but not in vacuoles (V) and cell walls (CW). Glutathione-specific labeling was observed in the stroma as well as inside the thylakoid lumen (arrowheads) when plants were exposed to high light intensities of 700 µmol m^-2 s^-1. Bars in (A,B) = 10 µm, (C,D) = 0.5 µm.