Melatonin: Awakening the Defense Mechanisms during Plant Oxidative Stress

Abstract

Melatonin is a multifunctional signaling molecule that is ubiquitously distributed in different parts of a plant and responsible for stimulating several physio-chemical responses to adverse environmental conditions. In this review, we show that, although plants are able to biosynthesize melatonin, the exogenous application of melatonin to various crops can improve plant growth and development in response to various abiotic and biotic stresses (e.g., drought, unfavorable temperatures, high salinity, heavy metal contamination, acid rain, and combined stresses) by regulating antioxidant machinery of plants. Current knowledge suggests that exogenously applied melatonin can enhance the stress tolerance of plants by regulating both the enzymatic and non-enzymatic antioxidant defense systems. Enzymic antioxidants upregulated by exogenous melatonin include superoxide dismutase, catalase, glutathione peroxidase, and enzymes involved in the ascorbate-glutathione cycle (ascorbate peroxidase, monodehydroascorbate reductase, dehydroascorbate reductase, and glutathione reductase), whereas levels of non-enzymatic antioxidants such as ascorbate, reduced glutathione, carotenoids, tocopherols, and phenolics are also higher under stress conditions. The enhanced antioxidant system consequently exhibits lower lipid peroxidation and greater plasma membrane integrity when under stress. However, these responses vary greatly from crop to crop and depend on the intensity and type of stress, and most studies to date have been conducted under controlled conditions. This means that a wider range of crop field trials and detailed transcriptomic analysis are required to reveal the gene regulatory networks involved in the between melatonin, antioxidants, and abiotic stress.

Keywords: ROS; antioxidant; ascorbate-glutathione cycle; melatonin.

Figure 1

Biosynthetic pathway for melatonin in plants. The following enzymes are involved in this pathway: tryptophan decarboxylase (TDC), tryptamine 5-hydroxylase (T5H), arylalkylamine N-acetyltransferase (AANAT), serotonin-N-acetyltransferase (SNAT), N-acetylserotonin methyltransferase (ASMT), aromatic-L-amino-acid decarboxylase (AADC), hydroxyindole-O-methyltransferase (HIOMT), tryptophan hydroxylase (TPH), N-acetylserotonin deacetylase (ASDAC), and indole-3-acetic acid (IAA).

Figure 2

Effect of exogenous melatonin on the ascorbate–glutathione (AsA-GCH) cycle in plants. In this reaction, AsA in its reduced form is oxidized to monodehydroascorbate (MDHA). MDHA is then either reduced by monodehydroascorbate reductase (MDHAR) to AsA or, because it is very unstable, reacts to form dehydroascorbate (DHA). DHA is reduced by dehydroascorbate reductase (DHAR) to AsA. 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 nicotinamide adenine dinucleotide phosphate (NADP) is regenerated during the reduction of MDHA and GSSG by the respective enzymes. AsA and GSH are also able to detoxify reactive oxygen species via direct chemical interaction. Thus, in addition to the total AsA and GSH levels, their redox state (i.e., reduced vs. oxidized), which depends on the activity of the four enzymes (gray boxes), is also very important for successful plant responses to stress. The blue arrows indicate that the exogenous application of melatonin increases the activity of these enzymes, whereas the red arrows indicate the opposite.