ROS and NO Regulation by Melatonin Under Abiotic Stress in Plants

Abstract

Abiotic stress in plants is an increasingly common problem in agriculture, and thus, studies on plant treatments with specific compounds that may help to mitigate these effects have increased in recent years. Melatonin (MET) application and its role in mitigating the negative effects of abiotic stress in plants have become important in the last few years. MET, a derivative of tryptophan, is an important plant-related response molecule involved in the growth, development, and reproduction of plants, and the induction of different stress factors. In addition, MET plays a protective role against different abiotic stresses such as salinity, high/low temperature, high light, waterlogging, nutrient deficiency and stress combination by regulating both the enzymatic and non-enzymatic antioxidant defense systems. Moreover, MET interacts with many signaling molecules, such as reactive oxygen species (ROS) and nitric oxide (NO), and participates in a wide variety of physiological reactions. It is well known that NO produces S-nitrosylation and NO₂-Tyr of important antioxidant-related proteins, with this being an important mechanism for maintaining the antioxidant capacity of the AsA/GSH cycle under nitro-oxidative conditions, as extensively reviewed here under different abiotic stress conditions. Lastly, in this review, we show the coordinated actions between NO and MET as a long-range signaling molecule, regulating many responses in plants, including plant growth and abiotic stress tolerance. Despite all the knowledge acquired over the years, there is still more to know about how MET and NO act on the tolerance of plants to abiotic stresses.

Keywords: NO; ROS; abiotic stress combination; drought; high light; high temperature; melatonin; post-translational modifications (PMTs), abiotic stress; salinity; waterlogging.

Figure 1

The four possible routes of melatonin (MET) biosynthesis. The enzymes that participate in the synthesis are: tryptophan decarboxylase (TDC), tryptophan hydroxylase (TPH), tryptamine 5-hydroxylase (T5H); serotonin N-acetyltransferase (SNAT); N-acetylserotonin methyltransferase (ASMT), and caffeic acid O-methyltransferase (COMT).

Figure 2

Interaction between melatonin (MET) and reactive oxygen species (ROS). ROS upregulates MET biosynthesis genes and enhances MET endogenous levels. MET can act as a ROS scavenger and controlled ROS levels through the melatonin-mediated induction of redox enzymes, such as SOD, CAT, POD, GPX and APX, and representative antioxidant representative non-enzymatic antioxidant compounds such as GSH and AsA (AsA-GSH cycle), osmoprotectants, and phenolic, flavonoid and carotenoid compounds. Similarly, the exogenous MET interacts with its receptor (CAND2/PMTR1), which appears to be melatonin-induced, resulting in the activation of responses against stressors are feed into a feedback mechanism with different regulating elements that belong to the redox network, such as ROS and RNS [42].

Figure 3

Nitric oxide (NO) synthesis in plants: (a) the non-enzymatically mechanism, under low pH or high reducing environments. (b) NO can be produced from nitrite through the action of the mitochondrial electron transport chain (mETC). (c) Nitrate reductase (NR) is responsible for the reduction of nitrate to nitrite using and then producing NO by Ni-NR activity. (d) NR can interact with the partner protein NOFNiR (nitric oxide-forming nitrite reductase) to produce NO from nitrite. (e) Arginine-dependent pathway in plants forms NO by NOS (nitric oxide synthase)-like activity.

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)-like since MET up-regulates the expression 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. As well, NOMET is 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 of the enzymes of the MET biosynthesis pathway) to increase MET levels.

Figure 5

Common MET functions in abiotic stress tolerance.