REVIEW Plant Signaling & Behavior 10:11, e1049788; November 2015; © 2015 Taylor and Francis Group, LLC
Regulatory roles of serotonin and melatonin in abiotic stress tolerance in plants Harmeet Kaur1, Soumya Mukherjee1, Frantisek Baluska2, and Satish C Bhatla1,* 1
Laboratory of Plant Physiology and Biochemistry; Department of Botany; University of Delhi; Delhi, India; 2Institute of Cellular and Molecular Botany; University of Bonn; Bonn, Germany
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.
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.
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 *Correspondence to: Satish C Bhatla; Email: [email protected] Submitted: 02/09/2015; Revised: 04/27/2015; Accepted: 05/06/2015 http://dx.doi.org/10.1080/15592324.2015.1049788
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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 mM) 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. 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
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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 Serotonin and melatoninmodulated 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 Figure 1. Biosynthetic pathway for the synthesis of indole-3-acetic acid, serotonin and melatonin from inhibition of auxin biosynthesis is likely a common precursor (tryptophan). to increase serotonin accumulation in plant tissues. Roots are the major sites biotic stress.78 Recent reports based on gene annotation and for serotonin and auxin biosynthesis. Recent report from the analysis of metabolic pathway network database (RiceCyc) in author’s laboratory has suggested NaCl stress-induced higher accurice have further shown that TDC1 and TDC3 are induced by mulation of serotonin in the vascular cells of the primary roots in abiotic and biotic stress factors.9 Melatonin biosynthesis and its sunflower seedlings and oil body containing cells of cotyledons.13 regulation involve the activity of enzymes downstream to seroto- Serotonin accumulation is regulated both by the age of seedlings nin biosynthesis, namely serotonin N-acetyltransferase (SNAT, and NaCl stress, with 6 day old seedling roots from controls E.C. Two.3.1.87) and hydroxyindole-O-methyltransferase exhibiting highest serotonin accumulation. Serotonin elicits tissue(HIOMT, E.C.2.1.1.4). HIOMT is a rate limiting enzyme, specific inhibitory effects on auxin responsive genes at the sites of thereby regulating the final step of melatonin biosynthesis from primary and adventitious roots and also in lateral root primordia.9 N-acetyl serotonin.10,11 Abiotic stress-induced regulation of It, thus, promotes root growth partially independent of auxin HIOMT is likely to affect the rate of melatonin biosynthesis activity. Effect of serotonin on lateral root induction has been (Fig. 2). Heat stress-induced elevation of SNAT and HIMOT found to be independent of the activity of AUX1 and AXR4 loci activities in rice seedlings leads to melatonin accumulation. but is dependent on AXR1 and AXR2 auxin related loci.9 Interestingly, the activities of these enzymes are elevated in Upregulation of melatonin biosynthesis is expected to occur dark.11 UV-B irradiation induces high melatonin biosynthesis under stress situations thus indicating the antistress properties of in Glycyrrhiza uralensis roots.12 Recent findings from the melatonin. Melatonin also elicits multiple physiological regulaauthor’s laboratory have shown NaCl¡stress induced 72% tory effects, thereby modulating abiotic stress tolerance in plants. increase in HIOMT activity in 2 day old, dark-grown sunflower Exogenously applied melatonin has significant effects on stress seedling cotyledons.13 Integrated bioinformatic analysis of data tolerance in plants due to its detoxification properties. Enhanced
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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 waterstressed 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 stressinduced lowering of auxin levels may affect plant growth, serotonin and melatonin partially ameliorate stressinduced 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 Figure 2. Abiotic stress-induced biochemical regulation of serotonin and melatonin biosynthesis. biotic stress even in the absence of melatonin.20 Exogenous melatonin treatment in cucumber seedlings induced down regulation of ABA serotonin under osmotic imbalance and quenching of excess biosynthetic genes whereas GA biosynthetic genes were upregu- ROS generated in plant cells.24,25 In plants facing stress (such as lated to provide necessary tolerance to NaCl stress.79 Thus, a hor- drought, salinity, chilling, metal toxicity, UV-B radiation, and monal crosstalk during abiotic stress appears to be regulated by pathogen attack), the equilibrium between ROS production and its quenching is perturbed and ROS generation is drastically melatonin. increased. Melatonin can detoxify the harmful effects of ROS by directly scavenging free radicals, and by the attenuation of radical Mechanism of quenching of ROS by melatonin Melatonin has greater antioxidative potential than serotonin. formation.26 It does not undergo redox cycling even under high Stress-induced serotonin accumulation and its association with physiological concentrations. These two properties make melatosenescence in rice plants has been attributed to reactive oxygen nin a unique antioxidant.27 It helps in the detoxification of sevspecies (ROS) scavenging.21 Estimation of serotonin and its eral ROS and RNS (reactive nitrogen species), such as the derivatives levels in safflower oil and Datura metel fruits has hydroxyl radical (OH¡) hydrogen peroxide (H2O2), peroxynihighlighted its antioxidative defensive role and protection of trite anion (ONOO¡), nitric oxide, peroxyl radical (LOO¡) and germ tissue against the adverse effects of environment-induced singlet oxygen (1O2).28-31 abiotic stress factors.22,23 Investigations on stress-associated seroMelatonin molecule consists of an electron-rich indole moiety tonin metabolism have provided clues for the protective role of and 2 side chain groups: 5-methoxy group and 3-amide group
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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 (AsAGSH) 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 nonenzymic antioxidants within the cell.42 The activities of these enzymes have often been reported to enhance under Figure 3. Structure of melatonin showing the sites of ROS quenching at the 2 side chains of the indole changing environmental conditions. heterocycle. Melatonin causes stimulation of electron transport chain and reduction in leakage of electrons. It thus limits O2¡ 43 (Fig. 3). The high resonance stability, electroreactivity and low formation. Melatonin helps in improving the redox state of cells activation energy barriers make melatonin a potent free radical by scavenging ROS and RNS.44 Majority of stress factors may alter scavenger.32,33 The side chains also have a significant contribu- the endogenous levels of melatonin. Endogenous levels of melatotion in the antioxidative properties of the molecule. Carbonyl nin have been reported to increase in response to various environmoiety present in the functional group (N CHO ) of C3 amide mental stresses. Melatonin upregulates the transcript levels and side chain has a key role in the quenching of more than one reac- stimulates the activities of several antioxidant enzymes.79 It also tive oxygen species. After the interaction of melatonin with ROS, regenerates some endogenous antioxidants, such as glutathione, to the nitrogen present in the carbonyl group of the melatonin mol- enhance cellular antioxidant system.45 Hung et al.46 reported the ecule leads to the formation of a new 5 membered ring. The sig- protective roles of exogenously applied melatonin during high temnificance of methoxy and acetyl groups of amide chain in the perature stress on seed germination of photosensitive and thermoantioxidative process has been confirmed by Tan et al.32 who sensitive Phacelia tanacetifolia Benth. seeds. Improved tolerance to observed that the OH¡ scavenging ability of a molecule lacking salt and drought stresses due to exogenous application of melatonin acetyl group of the amide chain is reduced by 50% as compared has also been reported in soybean.47 In this investigation, elevated to that of melatonin. A compound without both the groups acts antioxidant levels and increased activities of the ROS scavenging as a prooxidant. Analogs of melatonin devoid of methoxy group enzymes (superoxide dismutase, peroxidase, and catalase) were evipossess antioxidant properties but methoxy group does improve dent due to melatonin application coinciding with minimal the the efficiency of indole compounds as better antioxidants.32,34,35 adverse effects of stress. Melatonin is an important endogenous free radical scavenEnhanced antioxidant capacity is also evident from in vitro experiments by replacement of the methoxy group with a ger.32,48,49 It may directly scavenge H2O2 and help in the mainhydroxyl group but this, in turn, leads to a decrease in lipophilic- tenance of intracellular H2O2 concentration at steady state ity and a higher prooxidative potential of the modified mole- levels.28 This might be due to the inhibition of H2O2 accumulacule.36–39 Up to 4 or more reactive species can be scavenged by a tion and enhanced catalase and POD activities by endogenous single melatonin molecule making it an efficient antioxidant.12 melatonin supplementation. Pretreatment with 0.1 mM melatoThe mechanisms involved in the reaction of melatonin with the nin stimulates SOD and CAT activities along with increased surfree radicals includes processes such as electron donation to form vival rate in Rhodiola crenulata cells and callus.50 The melatoninyl cation radical, hydrogen donation from nitrogen upregulation of transcript levels of the genes encoding SOD, atom, nitrosation, addition reaction, substitution and nitrosa- APX, CT, and peroxidase by melatonin has been reported.51 It tion. Melatonin also shows damage repairing ability since it can has also been observed that melatonin treatment helps in mainrepair molecules that have been oxidized.33 taining the higher contents of ascorbic acid (AsA) and GSH.52
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Possible crosstalk among melatonin, nitric oxide and reactive A genomic, transcriptomic and metabolomic approach nitrogen species: A future perspective in understanding to understand the mechanism of melatonin-induced regulation nitrosative stress tolerance in plants of stress tolerance Nitric oxide (NO) is a highly diffusible, highly reactive, gasTranscriptomic analysis of melatonin-induced plant defense eous, free radical secondary messenger which elicits long distance genes in Arabidopsis has provided information on major classes signaling in plants. It is soluble both in water and lipid.53,54 At low of differentially expressed genes belonging to primary metaboconcentrations NO can regulate various biochemical and physio- lism and stress-associated responses.14,20 Further classification logical processes in plants, such as root organogenesis, hypocotyl has shown major genes to be expressed in the cytoplasm, nucleus growth, defense responses, stomatal movement, programmed cell and plasma membrane. Different set of genes are affected by death, hypersensitive responses, growth and development, and exogenous melatonin.20 Thus, melatonin treatment in bermuda phytoalaxin production.55-64 It can also activate some antioxidant grass (Cynodon dactylon L. Pers.) leads to overexpression of genes enzymes (SOD, CAT, APX) under normal conditions and thus associated with nitrogen and carbohydrate metabolism, horhelps in reducing the accumulation of reactive oxygen species.54 At monal pathway, redox signaling and secondary metabolism.14 high concentrations, NO can bring about nitrosation, nitration or Melatonin (1 mM) treatment in Arabidopsis alters the expression oxidation reactions.65 Plants subjected to abiotic stress frequently of 1308 genes (566 upregulated and 742 downregulated) associencounter a surge in RNS. Various reactive nitrogen species ated with plant defense mechanisms.20 Extensive transcriptomic (RNS), such as peroxynitrite (ONOO¡), nitrogen dioxide (NO2), analysis has shown upregulation of stress receptor kinases and dinitrogen trioxide (N2O3) and S-nitrosoglutathione (GSNO), stress associated calcium signaling components. Transcription regulate post-translational modifications (S-nitosylation) of pro- factors (TF) involved in the activation of stress responsive genes teins, and preferably cause modifications of several biomole- are significantly regulated by melatonin treatment. BASIC LEUcules.66,67 Salinity-induced nitrosative stress in olive leaves CINE ZIPPER PROTEINS, CBF/DREBs, MYB and zinc finger revealed an increment in Nitric Oxide Synthase (NOS)-dependent protein like TFs show more than fold16- accumulation due to NO liberation followed by accumulation of RNS in vascular bun- exogenous melatonin application under abiotic stress. Melatonin dles.68 Based on investigations in animal systems, it is evident that regulates the expression of novel transcriptionally active regions melatonin acts as a mediator of ROS and RNS crosstalk under mapped in Arabidopsis genome.20 Effect of melatonin in regulatnitrosative stress. Melatonin reacts with nitrogen centered radicals ing abiotic stress response is also operative through kinase activity 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, melatonininduced 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 Figure 4. Transcriptomic and metabolomic changes in response to exogenous melatonin and their roles to provide interesting mechanism of in abiotic stress tolerance (Data interpretation from Shi et al., 2014 and Weeda et al., 2014) crosstalk between NO and melatonin.
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events associated with abiotic stressinduced 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 Figure 5. Scheme depicting the signaling events during serotonin and melatonin-modulated abiotic endogenous levels of serotonin and melstress. atonin biosynthesis and their turnover in response to abiotic stress still require as a major component of stress signaling. Mitogen -activated pro- further attention. Plant root-soil interphase involves rapid signaltein kinases (MAPK) and calcium signaling kinases are also regu- ing events associated with absorption and exchange of various lated by exogenous melatonin. Effect of melatonin in delaying biomolecules. In this context, possibilities exist that melatonin is senescence is evident from the down regulation of chlorophyllase preferably absorbed from soil debris containing bacteria and (CLH1) expression, an enzyme responsible for chlorophyll degra- fungi.33 Fungi have been reported to possess high amount of dation. Li et al.76 reported melatonin-induced upregulation of melatonin. Tan et al.33 suggested the concept of melatonin recyNHX1 and AKT1 ion channel genes necessary for sodium ion cling in plants. Implications of mycorrhizal association in the regulation under salinity stress. GC-TOF-MS analysis of 54 amelioration of abiotic stress of plants can be investigated in the metabolites has revealed enhanced accumulation of amino acids, context of melatonin-induced defense responses. Characterizasugar alcohols and indoleamines by melatonin treatment under tion of receptors involved in serotonin and melatonin transport abiotic stress.20 These metabolites are independently regulated by and uptake in plants holds promise for deeper understanding of salt, drought or cold stress. A number of these metabolites are the stress tolerance mechanisms. associated with primary metabolic pathways (glycolysis, pentose phosphate pathway and tricarboxylic acid cycle). Melatonin treatDisclosure of Potential Conflicts of Interest ment induces high accumulation of compatible solutes, namely No potential conflicts of interest were disclosed. proline and carbohydrates (Fig. 4).14,20 Melatonin-induced abiotic stress tolerance in plants appears to be regulated at multiple Acknowledgments levels of receptor expression, transcriptional regulation of stress Authors are grateful to Alexander von Humboldt Foundation responsive genes, calcium-dependent kinase mediated signaling (Germany) for providing financial assistance in the form of events and accumulation of compatible solutes. In addition to Research Group Linkage Program between Frantisek Baluska these observations, ROS scavenging activity, antioxidant defense (IZMB, University of Bonn) and S.C. Bhatla (Department of systems and hormonal regulation are also subjected to alteration Botany, University of Delhi, India). Authors are also grateful to by melatonin under abiotic stress. Council of Scientific and Industrial Research (CSIR) and University Grants Commission (UGC) for providing research fellowships to Soumya Mukherjee and Harmeet Kaur, respectively. 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
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Funding
Financial support from Delhi University in the form of Research and Development Grant and Purse Grant are also gratefully acknowledged.
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47. Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS, et al. Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 2015; 66: 695-707; PMID:25297548; http://dx.doi.org/10.1093/jxb/ eru392 48. Tan DX, Manchester LC, Reiter RJ, Plummer BF, Hardies LJ, Weintraub ST, Vijayalaxmi S, Shepherd A M M. A novel melatonin metabolite, cyclic 3-hydroxymelatonin: a biomarker of in vivo hydroxyl radical generation. Biochem Biophys Res Commun 1998; 253:614-20; PMID:9918777; http://dx.doi.org/ 10.1006/bbrc.1998.9826 49. Reiter RJ, Tan DX, Terron MP, Flores LJ, Czarnocki Z. Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim Pol 2007; 54:1-9; PMID:17351668 50. Zhao Y, Qi L, Wang W, Saxena P, Liu C. Melatonin improves the survival of cryopreserved callus of Rhodiola crenulata. J Pineal Res 2011; 50:83-8; PMID:21073518; http://dx.doi.org/10.1111/j.1600079X.2010.00817.x 51. Rodriguez C, Mayo J, Sainz R, Antolin I, Herrera F, Martin V, Reiter RJ. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36:1-9; PMID:14675124; http://dx.doi.org/ 10.1046/j.1600-079X.2003.00092.x 52. Wang P, Yin L, Liang D, Li C, Ma F, Yue Z. Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate–glutathione cycle. J Pineal Res 2012; 53:11-20; PMID:21988707; http://dx.doi.org/10.1111/j.1600-079X.2011.00966.x 53. Davis KL, Martin E, Turko IV, Murad F. Novel effects of nitric oxide. Annu. Rev. Pharmacol. Toxicol 2001; 41:203-36; PMID:11264456 54. Hayat S, Hasan SA, Mori M, Fariduddin Q, Ahmad A. Nitric oxide : Chemistry, Biosynthesis and Physiological Role In Hayat S, Mori M, Pichtel J, Ahmad A, Nitric Oxide in Plant Physiology; Wiley-VCH Verlag GmbH and Co., Germany.2010. 1-16. 55. Neill SJ, Desikan R, Hancock JT. Nitric oxide signalling in plants. New Phytol 2003; 159:11-35; http://dx. doi.org/10.1046/j.1469-8137.2003.00804.x 56. Wendehenne D, Pugin A, Klessig DF, Durner J. Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plants Sci 2001; 6:177-83; PMID:11286923; http://dx.doi.org/10.1016/S13601385(01)01893-3 57. Pagnussat GC, Simontachi M, Puntarulo S, Lamattina L. Nitric oxide is required for root organogenesis. Plant Physiol 2002; 129:954-6; PMID:12114551; http://dx. doi.org/10.1104/pp.004036 58. Noritake T, Kawakita K, Doke N. Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol 1996; 37:113-6; http://dx.doi.org/ 10.1093/oxfordjournals.pcp.a028908
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59. Delledonne M, Xia Y, Dixon RA, Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature 1998; 394:585-8; PMID:9707120; http://dx. doi.org/10.1038/29087 60. Durner J, Wendehenne D, Klessig F. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 1998; 9:10328-33. 61. Kim OK, Murakami A, Nakamura Y, Ohigashi H. Screening of edible Japanese plants for nitric oxide generation inhibitory activities in RAW 264.7 cells. Cancer Lett 1998; 125:199-207; PMID:9566716; http://dx. doi.org/10.1016/S0304-3835(97)00513-2 62. Durner J, Klessig DF. Nitric oxide as a signal in plants. Curr Opin Plant Biol 1999; 2:369-74; PMID:10508751; http://dx.doi.org/10.1016/S13695266(99)00007-2 63. Magalhaes JR, Monte DC, Durzan D. Nitric oxide and ethylene emission in Arabidopsis thaliana. Physiol Mol Biol Plants 2000; 6:117-27. 64. Beligni MV, Lamattina L. Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 2000; 210:215-21; PMID:10664127; http://dx. doi.org/10.1007/PL00008128 65. Wink DA, Mitchell JB. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 1998; 25:434-56; PMID:9741580; http://dx.doi. org/10.1016/S0891-5849(98)00092-6 66. Astier J, Lindermayr C. Nitric oxide-dependent posttranslational modification in plants: an update. Int J Mol Sci 2012; 13:15193-208; PMID:23203119; http://dx.doi.org/10.3390/ijms131115193 67. Corpas FJ, Palma JM, >Del Rio LA, Barroso JB. Protein tyrosine nitration in higher plants grown under natural and stress conditions. Front Plant Sci 2013; 4:29; PMID:23444154; http://dx.doi.org/10.3389/ fpls.2013.00029 68. Valderrama R, Corpas FJ, Carreras A, FernandezOcana A, Chaki M, Luque F, Gomez-Rodrıguez MV, Colmenero-Varea P, del Rıo Luis A, Barrosoa JB. Nitrosative stress in plants. FEBS Letters 2007; 581:453-61; PMID:17240373; http://dx.doi.org/ 10.1016/j.febslet.2007.01.006 69. Turjanski AG, Chaia Z, Rosenstein RE, Estrin DA, Doctorovich F, Piro O. N-Nitrosomelatonin. Acta Crystallogr 2000; C56:682-3; PMID:10902020 70. Turjanski AG, Leonik F, Rosenstein RE, Estrin DA, Doctorovich F. Scavenging NO by melatonin. J Am Chem Soc 2000; 122:10468-9; http://dx.doi.org/ 10.1021/ja002006u 71. Manchester LC, Tan DX, Reiter RJ, Park W, Monis K, Qi W. High levels of melatonin in the seeds of edible plants: Possible function in germ tissue protection. Life
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Regulatory roles of serotonin and melatonin in abiotic stress tolerance in plants Harmeet Kaur1, Soumya Mukherjee1, Frantisek Baluska2, and Satish C Bhatla1,* 1
Laboratory of Plant Physiology and Biochemistry; Department of Botany; University of Delhi; Delhi, India; 2Institute of Cellular and Molecular Botany; University of Bonn; Bonn, Germany
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.
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.
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 *Correspondence to: Satish C Bhatla; Email: [email protected] Submitted: 02/09/2015; Revised: 04/27/2015; Accepted: 05/06/2015 http://dx.doi.org/10.1080/15592324.2015.1049788
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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 mM) 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. 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
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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 Serotonin and melatoninmodulated 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 Figure 1. Biosynthetic pathway for the synthesis of indole-3-acetic acid, serotonin and melatonin from inhibition of auxin biosynthesis is likely a common precursor (tryptophan). to increase serotonin accumulation in plant tissues. Roots are the major sites biotic stress.78 Recent reports based on gene annotation and for serotonin and auxin biosynthesis. Recent report from the analysis of metabolic pathway network database (RiceCyc) in author’s laboratory has suggested NaCl stress-induced higher accurice have further shown that TDC1 and TDC3 are induced by mulation of serotonin in the vascular cells of the primary roots in abiotic and biotic stress factors.9 Melatonin biosynthesis and its sunflower seedlings and oil body containing cells of cotyledons.13 regulation involve the activity of enzymes downstream to seroto- Serotonin accumulation is regulated both by the age of seedlings nin biosynthesis, namely serotonin N-acetyltransferase (SNAT, and NaCl stress, with 6 day old seedling roots from controls E.C. Two.3.1.87) and hydroxyindole-O-methyltransferase exhibiting highest serotonin accumulation. Serotonin elicits tissue(HIOMT, E.C.2.1.1.4). HIOMT is a rate limiting enzyme, specific inhibitory effects on auxin responsive genes at the sites of thereby regulating the final step of melatonin biosynthesis from primary and adventitious roots and also in lateral root primordia.9 N-acetyl serotonin.10,11 Abiotic stress-induced regulation of It, thus, promotes root growth partially independent of auxin HIOMT is likely to affect the rate of melatonin biosynthesis activity. Effect of serotonin on lateral root induction has been (Fig. 2). Heat stress-induced elevation of SNAT and HIMOT found to be independent of the activity of AUX1 and AXR4 loci activities in rice seedlings leads to melatonin accumulation. but is dependent on AXR1 and AXR2 auxin related loci.9 Interestingly, the activities of these enzymes are elevated in Upregulation of melatonin biosynthesis is expected to occur dark.11 UV-B irradiation induces high melatonin biosynthesis under stress situations thus indicating the antistress properties of in Glycyrrhiza uralensis roots.12 Recent findings from the melatonin. Melatonin also elicits multiple physiological regulaauthor’s laboratory have shown NaCl¡stress induced 72% tory effects, thereby modulating abiotic stress tolerance in plants. increase in HIOMT activity in 2 day old, dark-grown sunflower Exogenously applied melatonin has significant effects on stress seedling cotyledons.13 Integrated bioinformatic analysis of data tolerance in plants due to its detoxification properties. Enhanced
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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 waterstressed 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 stressinduced lowering of auxin levels may affect plant growth, serotonin and melatonin partially ameliorate stressinduced 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 Figure 2. Abiotic stress-induced biochemical regulation of serotonin and melatonin biosynthesis. biotic stress even in the absence of melatonin.20 Exogenous melatonin treatment in cucumber seedlings induced down regulation of ABA serotonin under osmotic imbalance and quenching of excess biosynthetic genes whereas GA biosynthetic genes were upregu- ROS generated in plant cells.24,25 In plants facing stress (such as lated to provide necessary tolerance to NaCl stress.79 Thus, a hor- drought, salinity, chilling, metal toxicity, UV-B radiation, and monal crosstalk during abiotic stress appears to be regulated by pathogen attack), the equilibrium between ROS production and its quenching is perturbed and ROS generation is drastically melatonin. increased. Melatonin can detoxify the harmful effects of ROS by directly scavenging free radicals, and by the attenuation of radical Mechanism of quenching of ROS by melatonin Melatonin has greater antioxidative potential than serotonin. formation.26 It does not undergo redox cycling even under high Stress-induced serotonin accumulation and its association with physiological concentrations. These two properties make melatosenescence in rice plants has been attributed to reactive oxygen nin a unique antioxidant.27 It helps in the detoxification of sevspecies (ROS) scavenging.21 Estimation of serotonin and its eral ROS and RNS (reactive nitrogen species), such as the derivatives levels in safflower oil and Datura metel fruits has hydroxyl radical (OH¡) hydrogen peroxide (H2O2), peroxynihighlighted its antioxidative defensive role and protection of trite anion (ONOO¡), nitric oxide, peroxyl radical (LOO¡) and germ tissue against the adverse effects of environment-induced singlet oxygen (1O2).28-31 abiotic stress factors.22,23 Investigations on stress-associated seroMelatonin molecule consists of an electron-rich indole moiety tonin metabolism have provided clues for the protective role of and 2 side chain groups: 5-methoxy group and 3-amide group
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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 (AsAGSH) 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 nonenzymic antioxidants within the cell.42 The activities of these enzymes have often been reported to enhance under Figure 3. Structure of melatonin showing the sites of ROS quenching at the 2 side chains of the indole changing environmental conditions. heterocycle. Melatonin causes stimulation of electron transport chain and reduction in leakage of electrons. It thus limits O2¡ 43 (Fig. 3). The high resonance stability, electroreactivity and low formation. Melatonin helps in improving the redox state of cells activation energy barriers make melatonin a potent free radical by scavenging ROS and RNS.44 Majority of stress factors may alter scavenger.32,33 The side chains also have a significant contribu- the endogenous levels of melatonin. Endogenous levels of melatotion in the antioxidative properties of the molecule. Carbonyl nin have been reported to increase in response to various environmoiety present in the functional group (N CHO ) of C3 amide mental stresses. Melatonin upregulates the transcript levels and side chain has a key role in the quenching of more than one reac- stimulates the activities of several antioxidant enzymes.79 It also tive oxygen species. After the interaction of melatonin with ROS, regenerates some endogenous antioxidants, such as glutathione, to the nitrogen present in the carbonyl group of the melatonin mol- enhance cellular antioxidant system.45 Hung et al.46 reported the ecule leads to the formation of a new 5 membered ring. The sig- protective roles of exogenously applied melatonin during high temnificance of methoxy and acetyl groups of amide chain in the perature stress on seed germination of photosensitive and thermoantioxidative process has been confirmed by Tan et al.32 who sensitive Phacelia tanacetifolia Benth. seeds. Improved tolerance to observed that the OH¡ scavenging ability of a molecule lacking salt and drought stresses due to exogenous application of melatonin acetyl group of the amide chain is reduced by 50% as compared has also been reported in soybean.47 In this investigation, elevated to that of melatonin. A compound without both the groups acts antioxidant levels and increased activities of the ROS scavenging as a prooxidant. Analogs of melatonin devoid of methoxy group enzymes (superoxide dismutase, peroxidase, and catalase) were evipossess antioxidant properties but methoxy group does improve dent due to melatonin application coinciding with minimal the the efficiency of indole compounds as better antioxidants.32,34,35 adverse effects of stress. Melatonin is an important endogenous free radical scavenEnhanced antioxidant capacity is also evident from in vitro experiments by replacement of the methoxy group with a ger.32,48,49 It may directly scavenge H2O2 and help in the mainhydroxyl group but this, in turn, leads to a decrease in lipophilic- tenance of intracellular H2O2 concentration at steady state ity and a higher prooxidative potential of the modified mole- levels.28 This might be due to the inhibition of H2O2 accumulacule.36–39 Up to 4 or more reactive species can be scavenged by a tion and enhanced catalase and POD activities by endogenous single melatonin molecule making it an efficient antioxidant.12 melatonin supplementation. Pretreatment with 0.1 mM melatoThe mechanisms involved in the reaction of melatonin with the nin stimulates SOD and CAT activities along with increased surfree radicals includes processes such as electron donation to form vival rate in Rhodiola crenulata cells and callus.50 The melatoninyl cation radical, hydrogen donation from nitrogen upregulation of transcript levels of the genes encoding SOD, atom, nitrosation, addition reaction, substitution and nitrosa- APX, CT, and peroxidase by melatonin has been reported.51 It tion. Melatonin also shows damage repairing ability since it can has also been observed that melatonin treatment helps in mainrepair molecules that have been oxidized.33 taining the higher contents of ascorbic acid (AsA) and GSH.52
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Possible crosstalk among melatonin, nitric oxide and reactive A genomic, transcriptomic and metabolomic approach nitrogen species: A future perspective in understanding to understand the mechanism of melatonin-induced regulation nitrosative stress tolerance in plants of stress tolerance Nitric oxide (NO) is a highly diffusible, highly reactive, gasTranscriptomic analysis of melatonin-induced plant defense eous, free radical secondary messenger which elicits long distance genes in Arabidopsis has provided information on major classes signaling in plants. It is soluble both in water and lipid.53,54 At low of differentially expressed genes belonging to primary metaboconcentrations NO can regulate various biochemical and physio- lism and stress-associated responses.14,20 Further classification logical processes in plants, such as root organogenesis, hypocotyl has shown major genes to be expressed in the cytoplasm, nucleus growth, defense responses, stomatal movement, programmed cell and plasma membrane. Different set of genes are affected by death, hypersensitive responses, growth and development, and exogenous melatonin.20 Thus, melatonin treatment in bermuda phytoalaxin production.55-64 It can also activate some antioxidant grass (Cynodon dactylon L. Pers.) leads to overexpression of genes enzymes (SOD, CAT, APX) under normal conditions and thus associated with nitrogen and carbohydrate metabolism, horhelps in reducing the accumulation of reactive oxygen species.54 At monal pathway, redox signaling and secondary metabolism.14 high concentrations, NO can bring about nitrosation, nitration or Melatonin (1 mM) treatment in Arabidopsis alters the expression oxidation reactions.65 Plants subjected to abiotic stress frequently of 1308 genes (566 upregulated and 742 downregulated) associencounter a surge in RNS. Various reactive nitrogen species ated with plant defense mechanisms.20 Extensive transcriptomic (RNS), such as peroxynitrite (ONOO¡), nitrogen dioxide (NO2), analysis has shown upregulation of stress receptor kinases and dinitrogen trioxide (N2O3) and S-nitrosoglutathione (GSNO), stress associated calcium signaling components. Transcription regulate post-translational modifications (S-nitosylation) of pro- factors (TF) involved in the activation of stress responsive genes teins, and preferably cause modifications of several biomole- are significantly regulated by melatonin treatment. BASIC LEUcules.66,67 Salinity-induced nitrosative stress in olive leaves CINE ZIPPER PROTEINS, CBF/DREBs, MYB and zinc finger revealed an increment in Nitric Oxide Synthase (NOS)-dependent protein like TFs show more than fold16- accumulation due to NO liberation followed by accumulation of RNS in vascular bun- exogenous melatonin application under abiotic stress. Melatonin dles.68 Based on investigations in animal systems, it is evident that regulates the expression of novel transcriptionally active regions melatonin acts as a mediator of ROS and RNS crosstalk under mapped in Arabidopsis genome.20 Effect of melatonin in regulatnitrosative stress. Melatonin reacts with nitrogen centered radicals ing abiotic stress response is also operative through kinase activity 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, melatonininduced 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 Figure 4. Transcriptomic and metabolomic changes in response to exogenous melatonin and their roles to provide interesting mechanism of in abiotic stress tolerance (Data interpretation from Shi et al., 2014 and Weeda et al., 2014) crosstalk between NO and melatonin.
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events associated with abiotic stressinduced 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 Figure 5. Scheme depicting the signaling events during serotonin and melatonin-modulated abiotic endogenous levels of serotonin and melstress. atonin biosynthesis and their turnover in response to abiotic stress still require as a major component of stress signaling. Mitogen -activated pro- further attention. Plant root-soil interphase involves rapid signaltein kinases (MAPK) and calcium signaling kinases are also regu- ing events associated with absorption and exchange of various lated by exogenous melatonin. Effect of melatonin in delaying biomolecules. In this context, possibilities exist that melatonin is senescence is evident from the down regulation of chlorophyllase preferably absorbed from soil debris containing bacteria and (CLH1) expression, an enzyme responsible for chlorophyll degra- fungi.33 Fungi have been reported to possess high amount of dation. Li et al.76 reported melatonin-induced upregulation of melatonin. Tan et al.33 suggested the concept of melatonin recyNHX1 and AKT1 ion channel genes necessary for sodium ion cling in plants. Implications of mycorrhizal association in the regulation under salinity stress. GC-TOF-MS analysis of 54 amelioration of abiotic stress of plants can be investigated in the metabolites has revealed enhanced accumulation of amino acids, context of melatonin-induced defense responses. Characterizasugar alcohols and indoleamines by melatonin treatment under tion of receptors involved in serotonin and melatonin transport abiotic stress.20 These metabolites are independently regulated by and uptake in plants holds promise for deeper understanding of salt, drought or cold stress. A number of these metabolites are the stress tolerance mechanisms. associated with primary metabolic pathways (glycolysis, pentose phosphate pathway and tricarboxylic acid cycle). Melatonin treatDisclosure of Potential Conflicts of Interest ment induces high accumulation of compatible solutes, namely No potential conflicts of interest were disclosed. proline and carbohydrates (Fig. 4).14,20 Melatonin-induced abiotic stress tolerance in plants appears to be regulated at multiple Acknowledgments levels of receptor expression, transcriptional regulation of stress Authors are grateful to Alexander von Humboldt Foundation responsive genes, calcium-dependent kinase mediated signaling (Germany) for providing financial assistance in the form of events and accumulation of compatible solutes. In addition to Research Group Linkage Program between Frantisek Baluska these observations, ROS scavenging activity, antioxidant defense (IZMB, University of Bonn) and S.C. Bhatla (Department of systems and hormonal regulation are also subjected to alteration Botany, University of Delhi, India). Authors are also grateful to by melatonin under abiotic stress. Council of Scientific and Industrial Research (CSIR) and University Grants Commission (UGC) for providing research fellowships to Soumya Mukherjee and Harmeet Kaur, respectively. 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
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Funding
Financial support from Delhi University in the form of Research and Development Grant and Purse Grant are also gratefully acknowledged.
Plant Signaling & Behavior
Volume 10 Issue 11
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