ROS and NO Phytomelatonin-Induced Signaling Mechanisms under Metal Toxicity in Plants: A Review

Abstract

Metal toxicity in soils, along with water runoff, are increasing environmental problems that affect agriculture directly and, in turn, human health. In light of finding a suitable and urgent solution, research on plant treatments with specific compounds that can help mitigate these effects has increased, and thus the exogenous application of melatonin (MET) and its role in alleviating the negative effects of metal toxicity in plants, have become more important in the last few years. MET is an important plant-related response molecule involved in growth, development, and reproduction, and in the induction of different stress-related key factors in plants. It has been shown that MET plays a protective role against the toxic effects induced by different metals (Pb, Cd, Cu, Zn, B, Al, V, Ni, La, As, and Cr) by regulating both the enzymatic and non-enzymatic antioxidant plant defense systems. In addition, MET interacts with many other signaling molecules, such as reactive oxygen species (ROS) and nitric oxide (NO) and participates in a wide variety of physiological reactions. Furthermore, MET treatment enhances osmoregulation and photosynthetic efficiency, and increases the concentration of other important antioxidants such as phenolic compounds, flavonoids, polyamines (PAs), and carotenoid compounds. Some recent studies have shown that MET appeared to be involved in the regulation of metal transport in plants, and lastly, various studies have confirmed that MET significantly upregulated stress tolerance-related genes. Despite all the knowledge acquired over the years, there is still more to know about how MET is involved in the metal toxicity tolerance of plants.

Keywords: NO; ROS; heavy metals; metal toxicity; phytomelatonin.

Figure 1

Common MET functions in metal toxicity tolerance. Reactive oxygen species (ROS), reactive nitrogen species (RNS), ascorbic acid (AsA), glutathione (GSH), catalase (CAT), superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxide (APX), and glutathione reductase (GR), nitric oxide (NO), polyamines (PAs), malondialdehyde (MDA).

Figure 2

Regulation of metal transport by MET. Treatment of MET decreased Pb, Cd, V and Al transfer from root to aerial parts of the plant. In addition, exogenous MET was related to the thickened root cuticle and epidermis.

Figure 3

Interaction between melatonin (MET) and reactive oxygen species (ROS). ROS upregulate MET biosynthesis genes and enhance MET endogenous levels. MET can act as a ROS scavenger and control ROS levels through the melatonin-mediated induction of redox enzymes, such as CAT, SOD, POD, GPX and APX, as well as non-enzymatic antioxidant compounds, such as GSH and AsA (AsA-GSH cycle), osmoprotectants, and phenolic, flavonoid and carotenoid compounds.

Figure 4

Interaction between melatonin (MET) and nitric oxide (NO). MET promotes the accumulation of NO by increasing the activity of NOS (nitric oxide synthase) by MET-mediated up-regulation of related genes. MET scavenges excess NO, as it produces oxidative injury (red arrow). In the presence of oxygen, MET can be easily converted to N-Nitrosomelatonin (NOMET) by NO nitrosation under different pH conditions, being NOMET an effective NO donor in cell cultures under the presence of serotonin and its derivatives. On the other hand, through a cyclic guanosine monophosphate (cGMP)-dependent pathway, NO induces the expression of TDC, T5H, SNAT and COMT genes that codify for the MET biosynthesis pathway enzymes to increase MET levels (these two process has not been described in plants grown under metal toxicity, although something similar was shown under other abiotic stresses). Abbreviations: Tryptophan decarboxylase (TDC), tryptamine5-hydroxylase (T5H), serotonin N-acetyltransferase (SNAT), and caffeic acid O-methyltransferase (COMT). Modified figure from our previous article [16].