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. 2015 Dec 2;10(11):e1049788. doi: 10.1080/15592324.2015.1049788

Regulatory roles of serotonin and melatonin in abiotic stress tolerance in plants

Harmeet Kaur 1, Soumya Mukherjee 1, Frantisek Baluska 2, Satish C Bhatla 1,*
PMCID: PMC4883943  PMID: 26633566

Abstract

Understanding the physiological and biochemical basis of abiotic stress tolerance in plants has always been one of the major aspects of research aiming to enhance plant productivity in arid and semi-arid cultivated lands all over the world. Growth of stress-tolerant transgenic crops and associated agricultural benefits through increased productivity, and related ethical issues, are also the major concerns of current research in various laboratories. Interesting data on the regulation of abiotic stress tolerance in plants by serotonin and melatonin has accumulated in the recent past. These two indoleamines possess antioxidative and growth-inducing properties, thus proving beneficial for stress acclimatization. Present review shall focus on the modes of serotonin and melatonin-induced regulation of abiotic stress tolerance in plants. Complex molecular interactions of serotonin and auxin-responsive genes have suggested their antagonistic nature. Data from genomic and metabolomic analyses of melatonin-induced abiotic stress signaling have lead to an understanding of the regulation of stress tolerance through the modulation of transcription factors, enzymes and various signaling molecules. Melatonin, nitric oxide (NO) and calmodulin interactions have provided new avenues for research on the molecular aspects of stress physiology in plants. Investigations on the characterization of receptors associated with serotonin and melatonin responses, are yet to be undertaken in plants. Patenting of biotechnological inventions pertaining to serotonin and melatonin formulations (through soil application or foliar spray) are expected to be some of the possible ways to regulate abiotic stress tolerance in plants. The present review, thus, summarizes the regulatory roles of serotonin and melatonin in modulating the signaling events accompanying abiotic stress in plants.

Keywords: abiotic stress, melatonin, nitric oxide, reactive oxygen species, serotonin

Abbreviations

ACC synthase

aminocyclopropane-1-carboxylic acid synthase

APX

ascorbate peroxidase

AsA

ascorbate

AsA-GSH

ascorbate-glutathione

CAT

catalase

DHAR

dehydroascorbate reductase

GPX

guaiacol peroxidase

GR

glutathione reductase

GSH

glutathione

IAA

indole-3-acetic acid

MAPK

mitogen activated protein kinases

MDHAR

monodehydroascorbate reductase

NO

nitric oxide

ROS

reactive oxygen species

SOD

superoxide dismutase.

Abiotic stress-induced serotonin and melatonin biosyntheses are positively regulated by a surge in tryptophan levels

Serotonin and melatonin are 2 major indoleamines derived from tryptophan. A precise regulation of auxin and serotonin biosynthesis through the modulation of tryptophan levels seems to be associated with stress signals.77 Analysis of 14C-tryptophan metabolism has shown that serotonin and melatonin biosynthesis in plants is initiated from tryptophan.1 Root tips and stele, which are major sites for auxin and serotonin biosynthesis, exhibit tissue-specific differential expression of tryptophan biosynthesis genes in rice. The pathway of serotonin biosynthesis in higher plants is mediated by tryptamine formation, which is catalyzed by 2-tryptophan decarboxylase (TDC; EC 4.1.1.28), and its further catalysis by tryptamine 5-hydroxylase (T5H) leads to the synthesis of serotonin (Fig. 1).2,3 Characterization of TDC and biochemical analysis of its overexpression in transgenic lines in rice has revealed 7–25 fold increase in serotonin accumulation in the transgenic seeds in comparison with the wild type, thus implying its regulatory role in serotonin biosynthesis.4 Furthermore, overexpression of TDC-1 and TDC-3 genes in transgenic rice resulted in high accumulation of serotonin and its subsequent effect on morphological changes lead to stunted growth, poor fertility and dark brown pigmentation of leaves.80 TDC appears to be the rate limiting enzyme of the pathway, having a high Km value (690 µM) for tryptophan.5 Enzyme downstream to TDC in the serotonin biosynthesis pathway, namely tryptamine 5-hydroxylase (T5H), however, has a low Km value. Thus, regulation of serotonin biosynthesis and the formation of its derivatives is initiated in the presence of higher levels of tryptophan in plant organs.

Figure 1.

Figure 1.

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Biosynthetic pathway for the synthesis of indole-3-acetic acid, serotonin and melatonin from a common precursor (tryptophan).

Mechanism of abiotic stress-induced alteration in the extent of tryptophan biosynthesis has been elucidated at transcriptional level in Arabidopsis.6 Tryptophan is known to initiate the formation of various secondary growth metabolites, namely phytoalexins, indole glucosinolates, alkaloids and serotonin. Plant defense and acclimatization to abiotic stress are related to the spatial and temporal distribuion of these metabolites. Rice and Arabidopsis exhibit abiotic stress-induced regulation of the enzymes of tryptophan biosynthesis pathway, namely anthranilate synthase (EC: 4.1.3.27) and tryptophan synthase (EC: 4.2.1.20).7,8 A surge in the activity of anthranilate synthase (EC: 4.1.3.27) and accumulation of tryptophan-derived metabolites (including serotonin) has been observed in the leaves of rice plants in response to biotic stress.78 Recent reports based on gene annotation and analysis of metabolic pathway network database (RiceCyc) in rice have further shown that TDC1 and TDC3 are induced by abiotic and biotic stress factors.9 Melatonin biosynthesis and its regulation involve the activity of enzymes downstream to serotonin biosynthesis, namely serotonin N-acetyltransferase (SNAT, E.C. Two.3.1.87) and hydroxyindole-O-methyltransferase (HIOMT, E.C.2.1.1.4). HIOMT is a rate limiting enzyme, thereby regulating the final step of melatonin biosynthesis from N-acetyl serotonin.10,11 Abiotic stress-induced regulation of HIOMT is likely to affect the rate of melatonin biosynthesis (Fig. 2). Heat stress-induced elevation of SNAT and HIMOT activities in rice seedlings leads to melatonin accumulation. Interestingly, the activities of these enzymes are elevated in dark.11 UV-B irradiation induces high melatonin biosynthesis in Glycyrrhiza uralensis roots.12 Recent findings from the author's laboratory have shown NaCl−stress induced 72% increase in HIOMT activity in 2 day old, dark-grown sunflower seedling cotyledons.13 Integrated bioinformatic analysis of data sets has also been established with the purpose of developing a metabolic network of rice. Gene family members of the tryptophan biosynthetic pathway in rice show coordination with the genes responsible for serotonin and auxin biosynthesis under abiotic and biotic stress.9 Stress-induced regulation of tryptophan biosynthesis in rice is, thus, speculated to be crucial for an accumulation of secondary metabolites.9

Figure 2.

Figure 2.

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Abiotic stress-induced biochemical regulation of serotonin and melatonin biosynthesis.

Serotonin and melatonin-modulated hormonal crosstalk in plants: An upcoming idea for abiotic stress tolerance

Serotonin and melatonin regulate abiotic stress-induced plant growth inhibition possibly by altering hormonal metabolism induced by stress signals.13,14,81 Among the major plant hormones, indole-3-acetic acid (IAA) is structurally similar to the 2 indoleamines - serotonin and melatonin.15 Serotonin, a tryptophan-derived conserved signaling molecule, regulates gene expression associated with auxin responsive pathways. Auxin transport and its spatio-temporal distribution in plant tissues regulate polarity, growth and gravitropism. Auxin efflux and its threshold levels are also altered by NaCl stress.16,17 Abiotic stress-induced inhibition of auxin biosynthesis is likely to increase serotonin accumulation in plant tissues. Roots are the major sites for serotonin and auxin biosynthesis. Recent report from the author's laboratory has suggested NaCl stress-induced higher accumulation of serotonin in the vascular cells of the primary roots in sunflower seedlings and oil body containing cells of cotyledons.13 Serotonin accumulation is regulated both by the age of seedlings and NaCl stress, with 6 day old seedling roots from controls exhibiting highest serotonin accumulation. Serotonin elicits tissue-specific inhibitory effects on auxin responsive genes at the sites of primary and adventitious roots and also in lateral root primordia.9 It, thus, promotes root growth partially independent of auxin activity. Effect of serotonin on lateral root induction has been found to be independent of the activity of AUX1 and AXR4 loci but is dependent on AXR1 and AXR2 auxin related loci.9

Upregulation of melatonin biosynthesis is expected to occur under stress situations thus indicating the antistress properties of melatonin. Melatonin also elicits multiple physiological regulatory effects, thereby modulating abiotic stress tolerance in plants. Exogenously applied melatonin has significant effects on stress tolerance in plants due to its detoxification properties. Enhanced stress tolerance due to the addition of melatonin to the soil has been observed in pea plants treated with high levels of copper in the soil.18 Zhang et al.19 investigated the response of water-stressed Cucumis sativus L. plants due to melatonin treatment and observed better proliferation of roots, thus indicating melatonin-induced drought tolerance. Transcriptomic analysis in Arabidopsis has shown 183 genes to be associated with melatonin-induced changes in hormonal signaling.20 Auxin responsive genes exhibit both up and down regulation in response to melatonin. Auxin transport and homeostasis are, thus, under the precise regulation by melatonin though it does not seem to affect the expression of auxin biosynthetic genes.20 Although abiotic stress-induced lowering of auxin levels may affect plant growth, serotonin and melatonin partially ameliorate stress-induced inhibitory effects. Ethylene and abscisic acid biosynthetic pathway genes also seem to be regulated by melatonin availability in Arabidopsis. Upregulation of 2 ACC synthase genes in response to melatonin suggests its role in the induction of ethylene biosynthesis.20 Melatonin-induced upregulation of abscisic acid, salicylic acid, jasmonic acid and ethylene biosynthetic pathway genes modulates several hormonal responses, thereby affecting plant defense processes. These hormone biosynthetic genes modulate their expression in response to abiotic and biotic stress even in the absence of melatonin.20 Exogenous melatonin treatment in cucumber seedlings induced down regulation of ABA biosynthetic genes whereas GA biosynthetic genes were upregulated to provide necessary tolerance to NaCl stress.79 Thus, a hormonal crosstalk during abiotic stress appears to be regulated by melatonin.

Mechanism of quenching of ROS by melatonin

Melatonin has greater antioxidative potential than serotonin. Stress-induced serotonin accumulation and its association with senescence in rice plants has been attributed to reactive oxygen species (ROS) scavenging.21 Estimation of serotonin and its derivatives levels in safflower oil and Datura metel fruits has highlighted its antioxidative defensive role and protection of germ tissue against the adverse effects of environment-induced abiotic stress factors.22,23 Investigations on stress-associated serotonin metabolism have provided clues for the protective role of serotonin under osmotic imbalance and quenching of excess ROS generated in plant cells.24,25 In plants facing stress (such as drought, salinity, chilling, metal toxicity, UV-B radiation, and pathogen attack), the equilibrium between ROS production and its quenching is perturbed and ROS generation is drastically increased. Melatonin can detoxify the harmful effects of ROS by directly scavenging free radicals, and by the attenuation of radical formation.26 It does not undergo redox cycling even under high physiological concentrations. These two properties make melatonin a unique antioxidant.27 It helps in the detoxification of several ROS and RNS (reactive nitrogen species), such as the hydroxyl radical (OH−) hydrogen peroxide (H2O2), peroxynitrite anion (ONOO−), nitric oxide, peroxyl radical (LOO−) and singlet oxygen (1O2).28-31

Melatonin molecule consists of an electron-rich indole moiety and 2 side chain groups: 5-methoxy group and 3-amide group (Fig. 3). The high resonance stability, electroreactivity and low activation energy barriers make melatonin a potent free radical scavenger.32,33 The side chains also have a significant contribution in the antioxidative properties of the molecule. Carbonyl moiety present in the functional group (N‒C˭O ) of C3 amide side chain has a key role in the quenching of more than one reactive oxygen species. After the interaction of melatonin with ROS, the nitrogen present in the carbonyl group of the melatonin molecule leads to the formation of a new 5 membered ring. The significance of methoxy and acetyl groups of amide chain in the antioxidative process has been confirmed by Tan et al.32 who observed that the OH− scavenging ability of a molecule lacking acetyl group of the amide chain is reduced by 50% as compared to that of melatonin. A compound without both the groups acts as a prooxidant. Analogs of melatonin devoid of methoxy group possess antioxidant properties but methoxy group does improve the efficiency of indole compounds as better antioxidants.32,34,35 Enhanced antioxidant capacity is also evident from in vitro experiments by replacement of the methoxy group with a hydroxyl group but this, in turn, leads to a decrease in lipophilicity and a higher prooxidative potential of the modified molecule.36–39 Up to 4 or more reactive species can be scavenged by a single melatonin molecule making it an efficient antioxidant.12 The mechanisms involved in the reaction of melatonin with the free radicals includes processes such as electron donation to form melatoninyl cation radical, hydrogen donation from nitrogen atom, nitrosation, addition reaction, substitution and nitrosation. Melatonin also shows damage repairing ability since it can repair molecules that have been oxidized.33

Figure 3.

Figure 3.

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Structure of melatonin showing the sites of ROS quenching at the 2 side chains of the indole heterocycle.

At low concentrations ROS function as secondary messengers in signal transduction and are required for growth, but at high endogenous concentrations they can be detrimental to plants due to oxidative burst.40,41 In order to protect themselves from the adverse effects of ROS, plant cells have a non-enzymatic and enzymatic detoxification system.42 The enzymic antioxidants include superoxide dismutase (SOD), catalase (CT), guaiacol peroxidase (GPX), enzymes of ascorbate glutahione (AsA-GSH) cycle, such as ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR) and glutathione reductase (GR). Ascorbate (AsA), glutathione (GSH), carotenoids, tocopherols, and phenolics serve as potent non-enzymic antioxidants within the cell.42 The activities of these enzymes have often been reported to enhance under changing environmental conditions. Melatonin causes stimulation of electron transport chain and reduction in leakage of electrons. It thus limits O2− formation.43 Melatonin helps in improving the redox state of cells by scavenging ROS and RNS.44 Majority of stress factors may alter the endogenous levels of melatonin. Endogenous levels of melatonin have been reported to increase in response to various environmental stresses. Melatonin upregulates the transcript levels and stimulates the activities of several antioxidant enzymes.79 It also regenerates some endogenous antioxidants, such as glutathione, to enhance cellular antioxidant system.45 Hung et al.46 reported the protective roles of exogenously applied melatonin during high temperature stress on seed germination of photosensitive and thermosensitive Phacelia tanacetifolia Benth. seeds. Improved tolerance to salt and drought stresses due to exogenous application of melatonin has also been reported in soybean.47 In this investigation, elevated antioxidant levels and increased activities of the ROS scavenging enzymes (superoxide dismutase, peroxidase, and catalase) were evident due to melatonin application coinciding with minimal the adverse effects of stress.

Melatonin is an important endogenous free radical scavenger.32,48,49 It may directly scavenge H2O2 and help in the maintenance of intracellular H2O2 concentration at steady state levels.28 This might be due to the inhibition of H2O2 accumulation and enhanced catalase and POD activities by endogenous melatonin supplementation. Pretreatment with 0.1 μM melatonin stimulates SOD and CAT activities along with increased survival rate in Rhodiola crenulata cells and callus.50 The upregulation of transcript levels of the genes encoding SOD, APX, CT, and peroxidase by melatonin has been reported.51 It has also been observed that melatonin treatment helps in maintaining the higher contents of ascorbic acid (AsA) and GSH.52

Possible crosstalk among melatonin, nitric oxide and reactive nitrogen species: A future perspective in understanding nitrosative stress tolerance in plants

Nitric oxide (NO) is a highly diffusible, highly reactive, gaseous, free radical secondary messenger which elicits long distance signaling in plants. It is soluble both in water and lipid.53,54 At low concentrations NO can regulate various biochemical and physiological processes in plants, such as root organogenesis, hypocotyl growth, defense responses, stomatal movement, programmed cell death, hypersensitive responses, growth and development, and phytoalaxin production.55-64 It can also activate some antioxidant enzymes (SOD, CAT, APX) under normal conditions and thus helps in reducing the accumulation of reactive oxygen species.54 At high concentrations, NO can bring about nitrosation, nitration or oxidation reactions.65 Plants subjected to abiotic stress frequently encounter a surge in RNS. Various reactive nitrogen species (RNS), such as peroxynitrite (ONOO−), nitrogen dioxide (NO2), dinitrogen trioxide (N2O3) and S-nitrosoglutathione (GSNO), regulate post-translational modifications (S-nitosylation) of proteins, and preferably cause modifications of several biomolecules.66,67 Salinity-induced nitrosative stress in olive leaves revealed an increment in Nitric Oxide Synthase (NOS)-dependent NO liberation followed by accumulation of RNS in vascular bundles.68 Based on investigations in animal systems, it is evident that melatonin acts as a mediator of ROS and RNS crosstalk under nitrosative stress. Melatonin reacts with nitrogen centered radicals to produce nitrosated products such as N-nitrosomelatonin, which is formed due to reaction of NO with melatonin.69,70 It can also help in maintaining the levels of NO by inhibiting the activity of prooxidative enzyme-nitric oxide synthase.71 However, melatonin-induced modulation of putative NOS in plants still remains to be demonstrated. Peroxynitrite anion (ONOO−), formed due to interaction of NO and O2−, is a toxic molecule.72,73 Melatonin can scavenge peroxynitrite anions or peroxynitrous acid by their interaction with the indole moiety present in melatonin. At physiological pH, it can react only with ONOOH or its activated form (ONOOH*)74,75. The mechanism of melatonin action needs further investigations. Investigations on melatonin and its effect on nitrosative stress shall provide new information on the regulation of abiotic stress tolerance in plants. Investigations on melatonin-induced modulation of protein tyrosine nitration and alteration of nitrosative stress induced biomarkers in plants are likely to provide interesting mechanism of crosstalk between NO and melatonin.

A genomic, transcriptomic and metabolomic approach to understand the mechanism of melatonin-induced regulation of stress tolerance

Transcriptomic analysis of melatonin-induced plant defense genes in Arabidopsis has provided information on major classes of differentially expressed genes belonging to primary metabolism and stress-associated responses.14,20 Further classification has shown major genes to be expressed in the cytoplasm, nucleus and plasma membrane. Different set of genes are affected by exogenous melatonin.20 Thus, melatonin treatment in bermuda grass (Cynodon dactylon L. Pers.) leads to overexpression of genes associated with nitrogen and carbohydrate metabolism, hormonal pathway, redox signaling and secondary metabolism.14 Melatonin (1 mM) treatment in Arabidopsis alters the expression of 1308 genes (566 upregulated and 742 downregulated) associated with plant defense mechanisms.20 Extensive transcriptomic analysis has shown upregulation of stress receptor kinases and stress associated calcium signaling components. Transcription factors (TF) involved in the activation of stress responsive genes are significantly regulated by melatonin treatment. BASIC LEUCINE ZIPPER PROTEINS, CBF/DREBs, MYB and zinc finger protein like TFs show more than fold16- accumulation due to exogenous melatonin application under abiotic stress. Melatonin regulates the expression of novel transcriptionally active regions mapped in Arabidopsis genome.20 Effect of melatonin in regulating abiotic stress response is also operative through kinase activity as a major component of stress signaling. Mitogen -activated protein kinases (MAPK) and calcium signaling kinases are also regulated by exogenous melatonin. Effect of melatonin in delaying senescence is evident from the down regulation of chlorophyllase (CLH1) expression, an enzyme responsible for chlorophyll degradation. Li et al.76 reported melatonin-induced upregulation of NHX1 and AKT1 ion channel genes necessary for sodium ion regulation under salinity stress. GC-TOF-MS analysis of 54 metabolites has revealed enhanced accumulation of amino acids, sugar alcohols and indoleamines by melatonin treatment under abiotic stress.20 These metabolites are independently regulated by salt, drought or cold stress. A number of these metabolites are associated with primary metabolic pathways (glycolysis, pentose phosphate pathway and tricarboxylic acid cycle). Melatonin treatment induces high accumulation of compatible solutes, namely proline and carbohydrates (Fig. 4).14,20 Melatonin-induced abiotic stress tolerance in plants appears to be regulated at multiple levels of receptor expression, transcriptional regulation of stress responsive genes, calcium-dependent kinase mediated signaling events and accumulation of compatible solutes. In addition to these observations, ROS scavenging activity, antioxidant defense systems and hormonal regulation are also subjected to alteration by melatonin under abiotic stress.

Figure 4.

Figure 4.

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Transcriptomic and metabolomic changes in response to exogenous melatonin and their roles in abiotic stress tolerance (Data interpretation from Shi et al., 2014 and Weeda et al., 2014)

Future perspectives

Investigations on serotonin and melatonin induced regulation of abiotic stress tolerance in plants have provided significant information on several physiological aspects associated with growth and defense mechanisms in plants. Various signaling events associated with abiotic stress-induced modulation of serotonin and melatonin biosynthesis and their interactions with other biomolecules shall provide new avenues for research (Fig. 5). Serotonin-induced alteration in plant growth regulation under abiotic stress has fewer reports to date. Melatonin has been reported to be associated with calcium-mediated signaling response in plants.20 Melatonin–calmodulin interactions in plants still remain elusive. Melatonin-induced regulation of calcium-dependent signaling is expected to be operative under abiotic stress in plants. Investigations on exogenous melatonin treatment under abiotic stress have provided significant information on genomic and transcriptomic regulation of pathways associated with hormonal metabolism and other signaling events. However, alteration in endogenous levels of serotonin and melatonin biosynthesis and their turnover in response to abiotic stress still require further attention. Plant root-soil interphase involves rapid signaling events associated with absorption and exchange of various biomolecules. In this context, possibilities exist that melatonin is preferably absorbed from soil debris containing bacteria and fungi.33 Fungi have been reported to possess high amount of melatonin. Tan et al.33 suggested the concept of melatonin recycling in plants. Implications of mycorrhizal association in the amelioration of abiotic stress of plants can be investigated in the context of melatonin-induced defense responses. Characterization of receptors involved in serotonin and melatonin transport and uptake in plants holds promise for deeper understanding of the stress tolerance mechanisms.

Figure 5.

Figure 5.

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Scheme depicting the signaling events during serotonin and melatonin-modulated abiotic stress.

Funding

Financial support from Delhi University in the form of Research and Development Grant and Purse Grant are also gratefully acknowledged.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Acknowledgments

Authors are grateful to Alexander von Humboldt Foundation (Germany) for providing financial assistance in the form of Research Group Linkage Program between Frantisek Baluska (IZMB, University of Bonn) and S.C. Bhatla (Department of Botany, University of Delhi, India). Authors are also grateful to Council of Scientific and Industrial Research (CSIR) and University Grants Commission (UGC) for providing research fellowships to Soumya Mukherjee and Harmeet Kaur, respectively.

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