Coordinated Actions of Glyoxalase and Antioxidant Defense Systems in Conferring Abiotic Stress Tolerance in Plants

Abstract

Being sessile organisms, plants are frequently exposed to various environmental stresses that cause several physiological disorders and even death. Oxidative stress is one of the common consequences of abiotic stress in plants, which is caused by excess generation of reactive oxygen species (ROS). Sometimes ROS production exceeds the capacity of antioxidant defense systems, which leads to oxidative stress. In line with ROS, plants also produce a high amount of methylglyoxal (MG), which is an α-oxoaldehyde compound, highly reactive, cytotoxic, and produced via different enzymatic and non-enzymatic reactions. This MG can impair cells or cell components and can even destroy DNA or cause mutation. Under stress conditions, MG concentration in plants can be increased 2- to 6-fold compared with normal conditions depending on the plant species. However, plants have a system developed to detoxify this MG consisting of two major enzymes: glyoxalase I (Gly I) and glyoxalase II (Gly II), and hence known as the glyoxalase system. Recently, a novel glyoxalase enzyme, named glyoxalase III (Gly III), has been detected in plants, providing a shorter pathway for MG detoxification, which is also a signpost in the research of abiotic stress tolerance. Glutathione (GSH) acts as a co-factor for this system. Therefore, this system not only detoxifies MG but also plays a role in maintaining GSH homeostasis and subsequent ROS detoxification. Upregulation of both Gly I and Gly II as well as their overexpression in plant species showed enhanced tolerance to various abiotic stresses including salinity, drought, metal toxicity, and extreme temperature. In the past few decades, a considerable amount of reports have indicated that both antioxidant defense and glyoxalase systems have strong interactions in conferring abiotic stress tolerance in plants through the detoxification of ROS and MG. In this review, we will focus on the mechanisms of these interactions and the coordinated action of these systems towards stress tolerance.

Keywords: abiotic stress; antioxidant defense; glutathione; methylglyoxal; oxidative stress; reactive oxygen species.

Figure 1

Generation of oxidative stress due to the consequences of abiotic stress (ROS, reactive oxygen species; ¹O₂, singlet oxygen; O₂^•−, superoxide anion; H₂O₂, hydrogen peroxide; OH^•, hydroxyl radical; MG, methylglyoxal; AOX, antioxidants).

Figure 2

Methylglyoxal biosynthesis, damaging effects, and its detoxification through the glyoxalase system (modified from Kalapos [56] and Kaur et al. [48]) (G-6P, glucose 6-phosphate; F-6P, fructose 6-phosphate; F-1,6P2, fructose 1,6-bisphosphate; GA-3P, glyceraldehyde 3-phosphate; DHAP, dihydroxyacetone-phosphate; GSH, glutathione; Gly I, Glyoxalase I; Gly II, Glyoxalase II; Gly III, Glyoxalase III; AGEs, advanced glycation end products).

Figure 3

Coordinated actions of antioxidant defense and glyoxalase systems in eliminating the toxic ROS and MG under abiotic stress. Dotted lines denote non-enzymatic conversions. R may be an aliphatic, aromatic, or heterocyclic group; X may be a sulfate, nitrite, or halide group. (Ascorbic acid, AsA; glutathione, GSH; glutathione dissulfide, GSSG; superoxide dismutase, SOD; catalase, CAT; ascorbate peroxidase, APX; MDHA, monodehydroascorbate; monodehydroascorbate reductase, MDHAR; DHA, dehydroascorbate; dehydroascorbate reductase, DHAR; glutathione reductase, GR; glutathione peroxidase, GPX; glutathione S-transferase, GST; NADP, nicotinamide adenine dinucleotide phosphate; Gly I, glyoxalase I; Gly II, glyoxalase II; SLG, S-D-lactoylglutathione). (Adapted from Hasanuzzaman et al. [4].) Solid arrows indicate enzymatic reactions while dotted arrows indicate non-enzymatic reactions.

Figure 4

MG signaling pathways in plants (Modified from Hoque et al. [49] and Kaur et al. [40,41]) (ROS_ext, extracellular ROS; ROS_int, Intracellular ROS; [Ca²⁺]_cyt, cytosolic Ca²⁺).