Functional interaction of melatonin with gasotransmitters and ROS in plant adaptation to abiotic stresses

Abstract

Melatonin is considered a multifunctional stress metabolite and a novel plant hormone affecting seed germination, root architecture, circadian rhythms, leaf senescence, and fruit ripening. Melatonin functions related to plant adaptation to stress stimuli of various natures are considered especially important. One of the key components of melatonin's stress-protective action is its ability to neutralise reactive oxygen species (ROS) and reactive nitrogen species directly. However, many of its effects are related to its involvement in the signalling network of plant cells and its influence on the expression of a large number of genes important for adaptation to adverse factors. Insights into the functional relationships of melatonin with gasotransmitters (GT) - gaseous molecules performing signalling functions - are still emerging. This review has analysed and summarised the experimental data that testify to the participation of the main GTs - nitric oxide, hydrogen sulfide, and carbon monoxide - in the implementation of the protective effect of melatonin when plants are exposed to abiotic stimuli of various nature. In addition, modulation by melatonin of one of the most important components in the action of GTs and ROS - post-translational modifications of proteins and the influence of ROS and GTs on melatonin synthesis in plants under stress conditions and the specific physiological effects of exogenous melatonin and GTs have been reviewed. Finally, the prospects of the GTs' practical application to achieve synergistic stress-protective effects on plants have been considered.

Keywords: ROS; abiotic stress; carbon monoxide; cell signalling; hydrogen sulfide; melatonin; nitric oxide; protein post-translational modifications.

Figure 1

Melatonin synthesis in plants. 5-HT – 5-hydroxytryptamine (serotonin); 5-MT – 5-methoxytryptamine; AADC – aromatic amino acid decarboxylase; AANAT – arylalkylamine N-acetyltransferase (arylamine N-acetyltransferase); aHT – N-acetyl 5-hydroxytryptamine; ASMT – N-acetylserotonin O-methyltransferase; COMT – caffeic acid O-methyltransferase; HIOMT – hydroxyindole O-methyltransferase (N-acetylserotonin O-methyltransferase); SNAT – serotonin N-acetyltransferase; T5H – tryptamine 5-hydroxylase; TDC – tryptophan decarboxylase; TPH – tryptophan hydroxylase. Red arrows indicate melatonin synthesis pathways that are activated under stressful conditions. Other explanations in the text.

Figure 2

Direct interaction of melatonin with ROS and RNS. 2-OHM, 2-hydroxymelatonin; 3-OHM, 3-hydroxymelatonin; AFMK , cyclic N1-acetyl-N 2-formyl-5-methoxykynuramine; AMK , N1-acetyl-5-methoxykynuramine; AMMC , acetamidomethyl-6-methoxycinnolinone; AMNK , N1-acetyl-5-methoxy-3-nitrokynuramine; IDO , indoleamine 2,3-dioxygenase; M2H , melatonin 2-hydroxylase; M3H , melatonin 3-hydroxylase; NOMela , N-nitrosomelatonin; ROS , reactive oxygen species; RNS , reactive nitrogen species. Other explanations in the text.

Figure 3

Functional interaction of melatonin with ROS in plant cells. 2-OHM – 2-hydroxymelatonin; CPKs, Ca²⁺-dependent protein kinases; CCaMK, Ca²⁺/calmodulin-dependent protein kinase; ROS, reactive oxygen species. The dashed arrow with blunt end indicates the possible inhibitory effect of melatonin on the expression of genes encoding certain molecular forms of NADPH oxidase. Other explanations in the text.

Figure 4

Involvement of NO in the activation of stress protection systems in plant cells under the action of melatonin. cGMP – cyclic guanosine monophosphate; COMT – caffeic acid O-methyltransferase; GC – guanylate cyclase; MAPK3/6 – mitogen activated protein kinases 3/6; NOMela – N-nitrosomelatonin; NOS – NO synthase; NR1 – nitrate reductase 1; ROS – reactive oxygen species; SNAT – serotonin N-acetyltransferase; T5H – tryptamine 5-hydroxylase; TDC – tryptophan decarboxylase. Dashed arrows indicate connections between signalling mediators without clear experimental evidence; blunt-ended arrows indicate antagonistic interactions between signalling mediators. Other explanations in the text.

Figure 5

Relationship between melatonin and hydrogen sulfide during activation of plant cell stress defence systems. ASMT, N-acetylserotonin O-methyltransferase; DES1, cysteine synthase-like desulfhydrase 1; LCD, L-cysteine desulfhydrase; MAPK, mitogen activated protein kinases; SNAT, serotonin N-acetyltransferase. Dashed arrows indicate connections between signalling mediators without clear experimental evidence. Other explanations in the text.

Figure 6

Possible effect of melatonin on the processes of post-translational modification of proteins by gasotransmitters and ROS. Mel, melatonin; NOMela, N-nitrosomelatonin; ROS, reactive oxygen species. Other explanations in the text.