Novel Perspectives on the Molecular Crosstalk Mechanisms of Serotonin and Melatonin in Plants T

Plant Physiology and Biochemistry 132 (2018) 33–45

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Plant Physiology and Biochemistry

journal homepage: www.elsevier.com/locate/plaphy

Review Novel perspectives on the molecular crosstalk mechanisms of serotonin and melatonin in plants T

Soumya Mukherjee

Department of Botany, Jangipur College, University of Kalyani, West Bengal, 742213, India

ARTICLE INFO ABSTRACT

Keywords: Current review focuses on the signiﬁcant role of serotonin and melatonin in various molecular crosstalk me- Auxin chanisms in plants. In this context phytohormones (like auxin, gibberellins, ethylene or abscisic acid), plant Brassinosteroids growth regulators, and associated biomolecules like reactive oxygen species, nitric oxide, brassinosteroids and Jasmonates hydrogen sulphide have been discussed in a wider context. Long distance signaling responses of serotonin in Melatonin association with auxin, jasmonic acid, salicylic acid and ABA have been critically reviewed. Auxin-serotonin Nitric oxide crosstalk in relation to PIN protein functioning and root growth regulation appears to be a major advancement in Reactive oxygen species Serotonin the context of phytoserotonin signaling in plants. Auxin and serotonin share structural similarities which bring possibilities of auxin receptors being surrogated for serotonin transport in plants. The modulation of root apex architecture is highly regulative in terms of serotonin-jasmonic acid crosstalk. Reactive oxygen species (ROS) appears to be a primary mediator of serotonin mediated root growth response. Serotonin induced signaling therefore involve ROS, auxin, JA and ethylene action. Although there exists handful of critical reviews on the role of phytomelatonin in plants, recent advancements on its regulatory role in modulating plant hormones, ROS scavenging enzymes, ROS/RNS and glutathione levels need attention. Melatonin signaling associated with nitrogen metabolism and nitrosative stress are recent developments in plants. Interesting relationship between nitric oxide and melatonin has been established in relation with biotic and abiotic stress tolerance in plants. Developments in hydrogen sulphide-melatonin signaling in plants are still at its nascent stage but exhibits promising scopes for future.

1. Introduction alleviation mechanisms of serotonin and melatonin in plants (Burkhardt et al., 2001; Manchester et al., 2000; Mukherjee et al., 2014). However, Investigations of plant signaling responses have succeeded through the lacuna in summarising the critical aspects of crosstalk mechanisms various attempts of physiological, biochemical and molecular analysis. associated with serotonin and melatonin requires to be filled with more Recent advancements on the molecular mechanisms of crosstalk events investigations of all previously framed hypotheses. The biosynthetic associated with serotonin and melatonin provide insights into their pathway of these two indoleamines initiates from common precursor efficacy as potent morphogens. The intricacies lie in the fact that varied tryptophan. Auxin biosynthesis associates with the accumulation of responses have been obtained for exogenous or endogenous levels of these two indoleamines in plants (Dharmawardhana et al., 2013). these amines in plants. Serotonin and melatonin have been associated Melatonin by virtue of its structural features possesses free radical with various physiological responses in different plant organs in- scavenging activities during various oxidative environments (Tan et al., vestigated across wide families of angiosperms (Odjakova and 1993). Serotonin appears to be less dynamic in eliciting a wide range of Hadjiivanova, 1997; Paredes et al., 2008; Park and Back, 2012; Pelagio- physiological responses in comparison with melatonin. This difference Flores et al. 2011, 2012). Lower plant groups have also been reported to in the activity pertains to the intermediate position of serotonin in respond to diurnal fluctuations as a response to these biomolecules melatonin biosynthesis pathway. Serotonin has also been reported to (Beilby et al., 2015). The appreciation for these two molecules as mere possess various derivatives in plant tissues (Hotta et al., 2002; Murch morphogens is, however, not of sole interest in the current scenario of et al., 2009). Transcriptomic and metabolomic analysis have provided research. Various attempts have been made to understand the stress sequential cues to the crosstalk of phytohormones and other signaling

Abbreviations: ABA, Abscisic acid; ASMT, n-acetyl serotonin methyl transferase; BR, Brassinosteroids; CK, Cytokinin; ET, Ethylene; GA, Gibberellic acid; JA, Jasmonates; NO, Nitric oxide; RNS, reactive nitrogen species; ROS, Reactive oxygen species E-mail address: [email protected]. https://doi.org/10.1016/j.plaphy.2018.08.031 Received 5 July 2018; Received in revised form 14 August 2018; Accepted 24 August 2018 Available online 27 August 2018 0981-9428/ © 2018 Elsevier Masson SAS. All rights reserved. S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45 molecules associated with these indoleamines (Weeda et al., 2014). acetylserotonin O-methyltransferase (ASMT) has been reported in These include primary phytohormones such as auxin, cytokinin, gib- Arabidopsis (Byeon et al., 2016). This enzyme catalyzes the final step of berellins, ethylene or ABA and other signaling molecules like reactive melatonin biosynthesis from N-acetylserotonin. The enzyme was re- oxygen species, nitric oxide, brassinosteroids and hydrogen sulphide. ported to exhibit cytoplasmic localization. Caffeic acid O-methyl Long distance signaling response of these indoleamines in association transferase (COMT) in Arabidopsis exhibits methylation activity to- with nitric oxide, jasmonic acid or salicylic acid has also been reported wards the substrate N-acetyl serotonin (Byeon et al., 2014). Km and in various plant systems (Qian et al., 2015; Shi et al., 2015a; Zhu and Vmax values for in vivo ASMT activity were found to be lower than that Lee, 2015). Auxin-serotonin crosstalk in response to various environ- of COMT activity. Interestingly the two pathways of melatonin bio- mental cues requires to be further investigated. Investigations are re- synthesis in plants (via N-acetyl serotonin and via 5-methoxy trypta- quired to decipher the metabolic regulations of tryptophan pathway mine) have been reported to be operative during normal and senes- and associated auxin and serotonin biosynthesis. In this context the cence conditions respectively (Back et al., 2016). During senescence the regulatory genes for auxin and serotonin biosynthesis pathway should organs are likely to produce higher amount of serotonin which triggers be analyzed. The action of melatonin in relation to other phyto- formation of 5-methoxytryptamine followed by melatonin. Thus suffi- hormones provides precise insights on its long and short distance sig- cient insights have been obtained in regard to the metabolic association naling in plants (Li et al., 2017). Understanding the nature of com- of serotonin and melatonin in various plant systems. This is largely munication among the target molecules is crucial for classifying the regulated by types of plant organ, age of tissue, photomodulatory effect signaling mechanisms. Exogenous melatonin induced changes in gene and other environmental cues. expression of various phytohormones have been reported in plants (Weeda et al., 2014; Wei et al., 2016; Zhang et al., 2017a). Melatonin is 3. Serotonin signaling in plants a potent regulator of various antioxidative enzymes, ROS/RNS and glutathione levels (Arora and Bhatla, 2017; Kaur and Bhatla, 2016; Liu 3.1. Significance of serotonin biosynthesis and its derivatization in plants et al. 2015a, 2015b). Interestingly nitric oxide and melatonin crosstalk has been established in relation with biotic and abiotic stress in plants Serotonin and auxin biosynthesis in plants initiates from the (Liu et al., 2015a; Shi et al., 2015a). Earlier investigations and reviews common precursor tryptophan. The main rate limiting enzyme of ser- from the author and co-workers have revealed salt-stress induced sig- otonin biosynthesis appears to be TDC (tryptophan decarboxylase) naling of serotonin and melatonin and their roles in abiotic stress tol- Kang et al., 2008. Tryptophan is one of the least abundant aminoacids erance (Kaur et al., 2015; Mukherjee et al., 2014, 2016). present in plant cells (Hildebrandt et al., 2015). This is due to the fact that it acts as a precursor of various secondary metabolites like indole 2. Metabolic association of serotonin and melatonin in plants glucosinolates, phytoalexins and alkaloids. The diverse class of secondary metabolites impart plant immunity against pathogen attack and The biosynthetic pathway of serotonin and melatonin initiates from biotic stress. In this context serotonin plays an important role as anti- their common precursor L-tryptophan. The pathway operative in plants oxidant and free radical homoeostasis in cells (Dharmawardhana et al., is similar to that in mammals and bacteria in terms of enzyme activity 2013; Mukherjee et al., 2014). Various enzymes associated with tryp- and turnover of various metabolic intermediates. L-tryptophan is the tophan biosynthesis are anthranilate synthase (E.C.4.1.3.27) and tryp- common precursor for auxin and serotonin in plants. According to tophan synthase (E.C.4.2.1.20) (Kanno et al., 2004; Zhao and Last, Murch and Saxena (2002) auxin and serotonin biosynthesis initiates 1996). The regulation of tryptophan biosynthesis is subject to various from a common intermediate precursor tryptamine. Preliminary in- environmental factors (Kaur et al., 2015). The role of serotonin in vestigations implying C14-tryptophan tracer method in St. John's wort regulating circadian rhythm in plants is thus under the control of (Hypericum perforatum L.) has revealed the formation of 5-hydro- temporal regulation of tryptophan and serotonin biosynthesis (Kang xytryotophan as a precursor of serotonin (Fig. 1). Serotonin biosynth- et al. 2007a,b, 2008; Schreoder et al., 1999). Regulation of tryptophan esis is accomplished by two step enzymatic process (Posmyk and Janas, biosynthesis genes have been observed to be in coordination with those 2009). It involves the activity of tryptophan decarboxylase (TDC; EC of auxin and serotonin biosynthesis pathway (Dharmawardhana et al., 4.1.1.28), which catalyzes the conversion of tryptophan to tryptamine, 2013; Kang et al. 2007a, 2008; Schreoder et al., 1999). In this context it followed by formation of serotonin catalyzed by the activity of trypta- is also important to note that tryptophan biosynthesis and activity of mine hydroxylase (T5H; EC 1.14.13). Melatonin is produced down- anthranilate synthase is under the regulation of feedback inhibition by stream in this pathway by the turnover of serotonin to N-acetylser- tryptophan (Kanno et al., 2004; Zhao and Last, 1996). The enzyme otonin (precursor for melatonin) accomplished by an acetylation tryptophan synthetase is also subject to tissue specific expression re- reaction (Fig. 1). The final step of melatonin biosynthesis from N-acetyl ported in maize and Arabidopsis (Last et al., 1991; Zhao and Last, 1995; serotonin is catalyzed by the activity of hydroxyindole O-methyl Kriechbaumer et al., 2008). Serotonin biosynthesis from tryptophan is transferase (HIOMT; EC 2.1.1.4). However, in an alternative pathway initiated by TDC (Kang et al., 2008). TDC isoforms have been reported melatonin may also be synthesised from 5-methoxytryptamine cata- to exhibit diurnal regulations for their temporal expressions in rice. lyzed by the acetylation reaction of serotonin N-acetyltransferase Interestingly the tryptophan biosynthesis genes have been spatially (SNAT; EC 2.3.1.87)(Byeon et al., 2015a,b; Zuo et al., 2014). Trypto- detected to be active in the root apex and stele regions. Therefore these phan decarboxylase appears to be the major rate limiting regulatory sites remain active for the biosynthesis of downstream derivatives of enzyme of the pathway, exhibiting a high Km (690 μM) for its substrate tryptophan namely auxin and serotonin. Investigations from in silico i.e. tryptophan (Kang et al., 2008). Tryptophan biosynthesis regulates analysis in rice, and other reports from Arabidopsis suggest tryptophan, TDC activity, which in turn affects the rate of serotonin and melatonin auxin and serotonin biosynthesis to jointly regulate root development formation in various plant organs. Metabolic regulation of tryptophan and root architecture (Dharmawardhana et al., 2013). Current in- biosynthesis and subsequent partitioning of auxin, serotonin and mel- vestigations of Sekiguchi lesion (SL) gene in rice revealed that it encodes atonin accumulation has been elaborately discussed in the following for a cytochrome P450 monooxygenase enzyme which bears tryptamine sections of the review. The first detection of melatonin in vascular 5 hydroxylase activity (Fujiwara et al., 2010). This enzyme catalyzes plants dates back to 1995, which was followed by detailed investiga- the conversion of tryptamine to serotonin in plants. The divergence of tions of its biosynthetic pathway (Arnao and Hernández-Ruiz, 2006). auxin and serotonin biosynthesis from tryptophan is partially regulated

Tryptophan decarboxylase has been characterized in Arabidopsis by the elevated activity of TDC having Km value > 690 μm(Kang et al., thaliana, Oryza sativa and other angiospermic members (Arnao and 2008). The downstream enzyme of this biosynthetic pathway i.e.

Hernández-Ruiz, 2006). Functional characterization of N- Tryptamine 5-hydroxylase has a much lower Km value. Thus it is

34 S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45

Fig. 1. Biosynthesis of serotonin and melatonin from tryptophan regulated by the enzymes tryptophan decarboxylase, aromatic L-amino acid decarboxylase (AADC), tryptamine 5 hydroxylase (Trp 5H), tryptamine deaminase, serotonin-N-acetyl transferase and hydroxyindole O-methyl transferase (Modified from Fan et al., 2018). evident that serotonin biosynthesis is more likely to be induced by not be regulated by JA signals. A negative correlation was observed higher tryptophan levels in the tissue. However, Kang et al. (2007a) between SHT activity and serotonin derivatives in shoot tissues. reported dose dependent increase in serotonin levels obtained by exo- Therefore the authors suggest long distance transport of serotonin de- genous tryptamine application in rice accompanied by a parallel in- rivatives from root to the shoot of transgenic rice. Addition of tyramine crease in T5H activity. Serotonin accumulation in this case was in- induced higher serotonin derivative production was independent of dependent of the tryptophan levels. Gene expression analysis in surge in SHT activity. Further investigations are necessary to correlate Capsicum annuum L. exhibited increased mRNA levels for TDC induced SHT activity with serotonin derivative production in plants. Ectopic by fungal infection and ethylene response. This was followed by a expression of SHT in transgenic tomato plants showed higher accu- concomitant increase in the levels of serotonin and its derivatives (Park mulation of serotonin derivatives to be present in the leaves (Kang et al., 2009). This response of elevated TDC activity and enhanced et al., 2008). Accumulation of such compounds also showed age de- serotonin levels was unaccompanied by surge in tryptophan biosynth- pendent increase in their content. Takahashi and Miyazawa (2011) esis. Although tryptophan is an important precursor for serotonin, reported tyrosinase inhibitory activity in synthesised phenylporopanoid regulation of serotonin biosynthesis remains under the multiple reg- amides of serotonin. The serotonin and amide moiety along with the ulations of ethylene crosstalk, biotic stress elicitation and tryptamine cinnamic acid group is responsible for anti-tyrosinase activity. Similar levels. Senescence induced serotonin biosynthesis in rice has been re- investigations also revealed a-glucosidase inhibitory activity present ported by Kim et al. (2009). due to the olefin group present in cinnamic moiety. These evidences Serotonin derivatives namely coumaroyl serotonin and feruloyl provide new insights to some of the possible physiological functions of serotonin are involved in defense mechanisms against biotic stress re- the serotonin derivatives in vivo. However, unlike serotonin the exact sponses. Transgenic rice plants with higher activity of serotonin N-hy- mechanisms of their mode of action and crosstalk events are yet to be droxycinnamoyl transferase (SHT) gene have been reported to exhibit deciphered. higher amounts of N-hydroxycinnamoylserotonins (p-coumaroyl serotonin and feruloyl serotonin) (Jang et al., 2004). Interestingly this 3.2. Auxin-serotonin crosstalk regulates plant growth and morphogenesis enzyme (SHT) has been reported to have higher affinity to serotonin with 16 fold lower Km value in comparison with tyramine. Functional Serotonin and auxin have been reported to exhibit functional si- expression of SHT protein in rice was primarily observed to be pre- milarities in promoting plant growth and morphogenesis. Since both of valent in the roots with a higher level of serotonin derivatives. Exo- these molecules share common biosynthetic pathway (from trypto- genous response by JA or wounding, however, did not produce suitable phan), it is important to understand the regulation of their biosynthetic amine substrate for SHT. Thus synthesis of serotonin derivatives may partitioning in plants (Fig. 2). Roots are the main sites for auxin and

35 S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45

Fig. 2. Metabolic partitioning of auxin and serotonin biosynthesis and downstream signaling response of serotonin modulating root growth and development. (Source: author). serotonin biosynthesis in plants (Kaur et al., 2015). Investigations have Arabidopsis which reveal multiple signaling responses to be elicited by been reported for both growth promoting and auxin antagonistic effects serotonin. Serotonin induced primary root growth inhibition has been of serotonin (Pelagio-Flores et al., 2011). Now the question needs to be observed to be mediated by the downstream action of jasmonic acid- addressed as to how the plant partitions between auxin and serotonin ethylene and ROS crosstalk (Pelagio-Flores et al., 2016). Higher con- biosynthesis. Further investigations are required to decipher their se- centrations of serotonin are growth inhibitory and it induces jasmonic parations at temporal and spatial levels. This shall be a complex ana- acid synthesis. Involvement of serotonin in biotic stress acclimatization lysis in various plant systems with effect to developmental and en- and modulation of growth response is congruent to the above facts. vironmental contexts. Auxin transport in plants is commonly Arabidopsis mutants for jasmonic acid and ethylene pathways exhibited accomplished by a diverse set of PIN family efflux proteins (Petrasek poor serotonin sensitivity measured in terms of root growth inhibition et al. 2006). However, no information has to date been reported on the (Pelagio-Flores et al., 2016). Exogenous serotonin application at extra possibilities of serotonin transporters in plants. Queries remain un- physiological concentrations (300 μM) has been inferred to operate answered as to how the plant responds to different concentrations of through jasmonic acid pathway. Mutant analysis revealed COI 1 and auxin and serotonin at cellular levels. Serotonin signaling across plant JAR 1 elements of JA pathway to be important components of serotonin cell membranes may possibly operate through receptor mediated pro- induced root growth regulation (Fig. 2). Therefore it appears that ser- cess. This effect is evident from its dose dependency manifested by otonin-JA crosstalk acts as a negative regulator for root growth in changes in growth rates. Auxin and serotonin share structural simila- Arabidopsis. rities which bring possibilities of auxin receptors being surrogated for The modulation of root apex architecture is highly regulative in serotonin transport in plants. Investigations in Arabidopsis have re- terms of its meristematic activity. Serotonin mediated downstream vealed uptake of exogenous serotonin and its dose-dependent response signal response primarily operates through ROS generation and sub- in promotion of lateral root development (Pelagio-Flores et al., 2011). sequent crosstalk to JA biosynthesis. Serotonin application in Higher concentrations of serotonin (> 160 μm), however, proved in- Arabidopsis promotes redistribution of ROS localization in the primary hibitory to lateral root formation but promoted adventitious rooting. roots thus causing growth retardation. Serotonin mediated ethylene Interrelationship of auxin and serotonin can be better observed by in- pathway negatively affects primary root growth response. Mutant vestigating the changes in auxin status at varying concentrations of analysis with etr1 revealed poorer sensitivity to serotonin induced root exogenous serotonin in plant cells. Serotonin activity in Arabidopsis growth inhibition (Pelagio-Flores et al., 2016). Serotonin mediated ROS manifests inhibitory effect on the auxin responsive gene elements. The surge has also been reported to be ineffective in etr1 mutants thus fact that serotonin promotes lateral root initiation has been found to be causing negligible effect on root growth inhibition. ROS stands to be an independent of auxin mediated action (Pelagio-Flores et al., 2011). The important primary mediator of serotonin mediated growth response. inhibitory effect of serotonin in growth response thus puts forward Serotonin induced multiple pathway of signaling shall therefore involve possibilities of complete impairment of auxin activity and subsequent ROS, auxin, JA and ethylene (Table 1). Recent developments on the changes in signaling cascade. Abiotic stress induced increase in en- metabolic regulation of serotonin biosynthesis in the High Free Lysine dogenous serotonin levels has been reported in Helianthus annuus L. (HFL) phenotype of rice have been associated with induction of JA seedling roots (Mukherjee et al., 2014). NaCl stress induced inhibition pathway (Yang et al., 2018). The authors reported the coordinated in root growth has also been reported to be ameliorated by exogenous events of serotonin biosynthesis (triggered by TDC expression) to be serotonin application. Decrease in auxin levels in response to abiotic coupled with JA pathway in the endosperm of rice grains. Such in- stress has been reported in various plant systems (Shen et al., 2010; Sun vestigations of JA-serotonin crosstalk add value to the context of amino et al., 2010; Yuan et al., 2013). Impairment of auxin transport and in- acid metabolism and nutritional values in rice grains. Biotic stress hibition of auxin biosynthesis are different aspects in this context. This mediated serotonin accumulation and changes in cell wall integrity are provides the possible avenue to investigate the levels of serotonin in also regulated by one, if not many, similar mechanisms (Hayashi et al., auxin deprived cells. Possibilities of tryptophan getting metabolized to 2016). Serotonin induced attenuation of biotic stress and alleviation of serotonin in higher amount cannot be ruled out in such cases. abiotic stress in plants may therefore operate through different pathways. Although serotonin possesses antioxidative properties, ROS activity is a primary reason of serotonin mediated growth inhibition. The 3.3. Serotonin mediated ROS distribution operates through jasmonic acid- stability of serotonin and its turnover into melatonin is important to- ethylene and ABA crosstalk wards regulating the intensity of the response. NaCl stress-induced serotonin accumulation in sunflower seedling roots also culminates in Significant insights have been obtained from investigations in

36 S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45

Table 1 Crosstalk events associated with serotonin.

Signaling molecule Response Reference

PIN eﬄux family proteins Diﬀerential expression, serotonin elicits auxin like action Sun et al., 2010 Pelagio-Flores et al., 2011 Jasmonic acid Induces JA synthesis, JA mutants (COI 1 and JAR 1) exhibit reduced serotonin sensitivity Pelagio-Flores et al., 2016

Reactive oxygen species Serotonin induced ROS surge and its differential redistribution in roots Pelagio-Flores et al., 2016 Induces localized hypersensitive response towards biotic stress Hayashi et al., 2016 Ethylene Positive regulator for root development. Etr 1 mutant with poor sensitivity to serotonin Pelagio-flores et al. 2016 Methyl jasmonate (exogenous) Induces serotonin biosynthesis genes to overexpress Sato et al., 2013 ABA (exogenous) Induces serotonin biosynthesis genes to overexpress Sato et al., 2013 higher accumulation of melatonin (Mukherjee et al., 2014). Thus it is other organelles signify its evolutionary importance in appearing from possible that serotonin induced growth inhibitory effects may be tran- prokaryotic symbiotic organisms (Tan et al., 2013; Beilby et al., 2015). siently altered by its conversion to melatonin in cells. In this context it The chloroplastic biosynthesis of melatonin has been elaborately in- is important to analyze the activity of melatonin biosynthesizing en- vestigated by Zheng et al. (2017). The localization of ASMT has been zymes in response to environmental variations. Serotonin elicits hy- successfully reported in chloroplasts which catalyze the conversion of persensitive response to fungal infection in rice but, however, protects N-acetyl serotonin to melatonin. This enzyme has also been stated to be the surrounding non-infected regions by delimitation of free radical regulated by salt stress and high light intensity. Thus regulation of distribution (Hayashi et al., 2016). Interestingly serotonin biosynthesis melatonin biosynthesis can be attributed to environmental cues like is also inversely reported to be enhanced by exogenous methyl jasmo- diurnal changes and abiotic stress. nate application. The response of serotonin in triggering defence re- Wang et al. (2017) reported melatonin biosynthesis in mitochondria sponse depends upon its turnover from tryptamine. Microanalysis data of isolated apple tissue. Further analysis revealed SNAT isoform, of 7d old seedlings obtained from RiceXPro database suggests serotonin MzSNAT5 to be expressed in mitochondria of both Arabidopsis proto- biosynthesis genes to be affected primarily by ABA and JA (Sato et al., plast and apple callus tissue. This enzyme catalyzes the conversion of N- 2013). Interestingly enough, serotonin mediated HR response in rice acetyl serotonin to melatonin. Melatonin biosynthesis in mitochondria was found to be primarily mediated by light and ABA dependent was also reported to be elevated by drought induced activity of pathway. Photomodulatory role of serotonin has been stated to be MzSNAT5. Thus transgenic Arabidopsis with ectopic expression of controlled by the expression of rate limiting enzyme TDC (tryptophan MzSNAT5 were conferred with better drought tolerance and detox- decaboxylase) (Kang et al., 2008). Serotonin being oxidised to its de- ification abilities. Although there are several other exogenous factors rivatives promote biotic stress defense by lesion formation. As men- regulating melatonin accumulation from serotonin, in non photo- tioned earlier, the role of serotonin in biotic stress attenuation is op- synthetic tissues long distance transport can be one of the possible ways erative through light and ABA–dependent pathway acting different of melatonin accumulation. Senescence associated increase in mela- from JA and ethylene action. In this context serotonin promotes free tonin synthesis has been reported to be primarily regulated by light radical scavenging in adjacent areas of non-infected tissue. ABA de- intensity in rice leaves (Byeon et al., 2012). This operates through pendent serotonin accumulation and its turnover from tryptamine are upregulation of melatonin biosynthesis genes and surge in their mRNA thus regulatory towards tissue detoxification and free radical homo- levels. Furthermore melatonin synthesis and its turn over into 2-hy- eostasis. droxymelatonin by the activity of melatonin 2-hydroxylase has been reported by Byeon and Back (2015). Similarly melatonin biosynthesis genes have been evidenced to be coordinated in presence of cadmium 4. Melatonin signaling in plants stress in rice (Byeon et al., 2015a,b). Temperature elevation also positively regulates melatonin synthesis which, however, is also accom- 4.1. Perspectives of melatonin biosynthesis in plants panied by induction of dark period. The surge in melatonin levels is regulated by higher activity of SNAT and ASMT respectively (Byeon and Melatonin has been investigated in various aspects of plant func- Back, 2014). Levels of endogenous serotonin have also been attributed tioning, reproduction, growth and stress alleviation (biotic and abiotic) to be a limiting factor for melatonin accumulation in transgenic rice (Mukherjee et al., 2014; Odjakova and Hadjiivanova, 1997; Paredes seedlings (Kang et al., 2010). Regulation of melatonin biosynthesis and et al., 2008; Park and Back, 2012; Pelagio-Flores et al., 2012; Shi et al., its turnover therefore appear to be one of the important aspects in re- 2016a). This potent multiregulatory molecule is synthesised from ser- lation with its role in crosstalk with other biomolecules. Helianthus otonin. Following serotonin formation from tryptophan, serotonin N- annuus L. seedlings induced by NaCl stress exhibit high melatonin acetyltransferase (SNAT) catalyzes the conversion of serotonin to N- content appearing in the cotyledons (Mukherjee et al., 2014). Further acetylserotonin (Kang et al., 2008). This is further metabolized by the investigations are necessary for the fate of melatonin and its turnover in enzyme acetylserotonin methyl transferase (ASMT) to form melatonin. various plant organs. Substantiating these lacunas will provide new Alternatively melatonin may also be synthesised from tryptamine information of its interaction and stability during signaling events in where serotonin may be transformed into 5-methoxytryptamine by cells. ASMT and COMT (caffeic acid O-methyltransferase) to generate melatonin through the activity of serotonin N-acetyltransferase (Byeon et al., 2015a,b; Zuo et al., 2014). Most of the enzymes involved in the bio- 4.2. Melatonin-auxin crosstalk synthetic pathway have been identified and characterized. Inter- mediates of the melatonin biosynthesis pathway are produced in var- Relationships of melatonin and auxin in plants have been in- ious intracellular reserves of endoplasmic reticulum, chloroplasts or vestigated across varied plant systems. The two molecules share some cytoplasm (Tan et al., 2013). Various molecular methods have been degree of structural and functional similarities in plants (Arnao and implied to trace the biosynthesis of melatonin in plants. However, re- Hernandez-ruiz 2006). Pharmacological effects of exogenous melatonin ceptor mediated signaling of this biomolecule still requires further in- in growth promotion and inhibition as well has been revealed to be a vestigations in plants. The biosynthesis of melatonin in chloroplasts and function of its exogenous concentrations. Auxin mediated melatonin

37 S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45 signaling primarily operates through the activity of auxin transcription expressions (Koyama et al., 2013; Pelagio-Flores et al., 2012). Gravi- factors. Auxin Resistant 3 (AXR3)/Indole-3-Acetic Acid inducible 17 tropic response guided by melatonin has been elucidated in lupin roots (IAA17) response is downregulated by exogenous melatonin in relation (Arnao and Hernández-Ruiz, 2017). In addition to lupin roots some with leaf senescence in Arabidopsis (Shi et al., 2015b). Furthermore monocot plants have also been reported to exhibit melatonin gradient AtAA17 overexpressing lines exhibited delayed senescence as an effect in roots similar to auxin activity. This suggests the similarities of mel- of exogenous melatonin treatment. Thus it was evidenced that mela- atonin and auxin action in terms of its spatial compartmentalization in tonin induced delay in leaf senescence was operative through down- young roots (Hernández-Ruiz et al., 2004; Hernández-Ruiz and Arnao, regulation of auxin element IAA 17. In association with exogenous 2008). Exogenous melatonin induced downregulation of auxin genes melatonin treatment the authors also reported accumulation of en- which involved lateral root development, root gravitropism and root dogenous melatonin in response to developmental changes in Arabi- hair proliferation were mostly associated with AUX1 or LAX elements dopsis leaves. Thus temporal differences in the expression of melatonin (Swarup and Péret, 2012; Weeda et al., 2014). According to Wang et al. and auxin responsive elements highlight their signaling mechanisms. (2016) investigations using Triiodobenzoic acid (TIBA; an auxin polar Reports have been obtained for dose-dependent growth promoting ef- transporter inhibitor) revealed that the polar gradient of auxin is, fects of melatonin similar to that of auxins (Arnao and Hernandez-Ruiz, however, necessary to execute melatonin induced root growth and 2007a, Chen et al., 2009, Tan et al., 2012, Park and Back, 2012, development in Arabidopsis. Thus conclusions derived from recent in- Pelagio-Flores et al., 2012). Weeda et al. (2014) performed Arabidopsis vestigations reveal the overlapping effects of melatonin and auxin in transcriptome analysis where most of the auxin response genes were rhizogenesis and root gravitropism. The fact that melatonin is antag- found to be downregulated by melatonin. Concentration dependent onistic to auxin in action is not universally effective. Rather the two effect of melatonin on root length and lateral root proliferation has biomolecules are similar in their line of action but melatonin exhibits been manisfested to be growth inhibitory at higher concentrations both positive and negative regulation of auxin activity subject to its (Park, 2011). However such inhibitory effects were found to be in- concentration (Fig. 3). The mechanism of melatonin induced auxin dependent of auxin action. Interestingly the downregulated auxin re- signaling primarily operates through its biosynthesis, conjugation, sponse genes in response to melatonin treatment were mostly asso- transport and further expression of auxin responsive elements down- ciated with auxin influx transporters and its homoeostasis (Weeda et al., stream in the cascade (Table 2). 2014). Melatonin mediated deactivation of auxin response was also attributed to the upregulation of GH3 genes which encode for IAA- 4.3. Melatonin-cytokinin effects aminosynthase enzyme catalyzing aminoacid conjugation to auxin. Melatonin (50 μM) induced proliferation of adventitious roots was also The possible role of melatonin in antisenescence activity has been associated with alteration in the expression of IAA/IBA genes and efflux reported in various plant systems including Arabidopsis (Arnao and transporters namely PIN1, PIN3, PIN7, IAA19, and IAA24 (Wen et al., Hernández-Ruiz, 2009; Gao et al., 2016; Hu et al., 2016; Liang et al., 2016). 2015; Shi et al., 2015b; Wang et al. 2012, 2013; Zhang et al., 2013). Adventitious root formation and its proliferation is a unique system The current understanding of the mechanism of melatonin induced to study the role of morphogens namely auxin and melatonin (López- senescence delay mostly relates to the modulation of senescence genes Bucio et al., 2015; Sarropoulou et al., 2012). However, in this context (Wang et al., 2013; Weeda et al., 2014). Melatonin induced down- the crosstalk event between these biomolecules have provided insights regulation of chlorophyll-degrading enzymes namely chlorophyllase to endogenous regulation of auxin in response to melatonin. Wen et al. and pheophorbide a oxygenase has been reported in Arabidopsis and (2016) reported the positive effect of melatonin treatment in upregu- Malus huphehensis (Wang et al., 2013; Weeda et al., 2014). In this lating IAA levels and subsequent expression of PIN 1, PIN 3 and PIN 7 in context it is worth mentioning that the protective role of melatonin in apex and hypocotyls of Solanum lycopersicum L. PIN 1 gene responded as pigment accumulation, stress tolerance and senescence has similarities an early signaling component induced by melatonin treatment. This to cytokinin effects. Recent investigations have confirmed the ameli- pertains to the basipetal transport of auxin responsible to trigger in- orative effects of melatonin towards photosynthetic quantum yield, PS itiation and elongation of adventitious roots. These evidences ascertain II functioning and availability of D1 protein (Zhou et al., 2016a,b). the fact that downstream action of melatonin triggers auxin accumu- Protective role of melatonin towards senescence induced by heat stress lation and its subsequent cellular efflux. Control of root architecture at has been reported by Zhang et al. (2017) in perennial ryegrass (Lolium the meristematic zone is highly regulative in terms of melatonin in- perenne L.). This effect has been associated with downregulation of duced auxin response (Liang et al., 2017). In rice melatonin induced senescence genes namely LpSAG12 and Lph36. There are recent reports changes in the expression of auxin associated transcription factors, of melatonin affecting accumulation of cytokinin during heat stress namely WRKY, NAC, MYB (Liang et al., 2017). On contrary to the re- which, however, is not the same during normal conditions (Zhang et al., sults of Wen et al. (2016) melatonin at high concentrations negatively 2017). The authors reported upregulation of cytokinin biosynthesis regulates auxin biosynthesis and expression of PIN proteins in Arabi- genes (LpIPT2 and LpOG1) in response to melatonin treatment. Further dopsis (Wang et al., 2016). Extra physiological concentrations of mel- analysis revealed increased levels of isopentenyladenine and trans- atonin as high as 1 mM suppressed root meristem cells in number and zeatin riboside in response to exogenous melatonin treatment. En- length thus reducing primary root growth. In this context the transcript dogenous levels of cytokinin and melatonin were also in positive cor- levels of YUC1, YUC2, YUC5, YUC6, and TAR2 (auxin biosynthesis gene relation to each other. Melatonin also induced changes in the expres- elements) decreased upon exposure to 600 μM melatonin. Interestingly sion patterns of cytokinin responsive transcription factors called A- enough the PIN1, PIN 3 and PIN 7 genes were also suppressed in effect ARRs and B-ARRs. to melatonin treatment. These genes encode for auxin efflux transporter Significant contributions regarding the mediator proteins involved proteins expressed in provascular tissue, cortex and root cap. Thus the in the molecular mechanism of cytokinin and melatonin crosstalk have intricacy of auxin response in relation to melatonin lies in the dose of been provided by Sliwiak et al. (2018). The author and co-workers melatonin experienced by the plant tissue. Lower concentrations of report the affinity of LlPR-10.2B, (pathogenesis related protein; PR-10) melatonin (50 μM) appear positive to auxin elements which, however, towards melatonin as well cytokinin at its specific binding sites. Crys- get inhibited at higher concentrations. Transgenic lines in tomato and tallographic studies of the protein obtained from yellow lupine (Lupinus Arabidopsis (SNAT/ASMT) overexpressed for endogenous melatonin luteus) reveals ability of quaternary complex formation between the biosynthesis has been reported with decreased levels of auxins. The protein and equal concentrations of melatonin and trans-zeatin. Com- mechanism of action for melatonin induced formation of lateral root parisons of binding affinity of such complex with that of PR-10/zeatin primordia does not essentially operate through auxin induced gene complex or melatonin independently revealed PR-10 to be a low affinity

38 S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45

Fig. 3. Melatonin induced crosstalk events mediated by modulation of gene expressions of metabolic pathways and subsequent downstream signaling responses. (Source: author). melatonin binder. Thus at elevated concentrations of melatonin in plant 4.4. Melatonin interacts with GA, ABA and ethylene over multiple pathways cells it is likely that PR-10 shall act as a connector to melatonin-cytokinin crosstalk. These novel ﬁndings therefore provide suitable insights A wide number of investigations have been obtained to highlight the to the mechanisms of melatonin-cytokinin crosstalk mostly operative at metabolic interconnectivity of melatonin with gibberellic acid, abscisic higher concentrations of melatonin and associated with abiotic stress acid and ethylene (Fig. 3; Table 2). Melatonin induced alteration in the conditions (Fig. 3; Table 2). levels of these hormones have been pertained to various physiological processes like heat stress acclimatization, cold stress primimg, modulation of fruit ripening and associated antioxidative roles. Cold stress mediated tolerance in Citrullus plant has been reported to have been

Table 2 Crosstalk events associated with melatonin.

Signaling event Response Reference

Auxin response elements Downregulation of Auxin Resistant 3 (AXR3)/Indole-3-Acetic Acid inducible 17 (IAA17) Shi et al., 2015 response Auxin conjugation pathway Upregulation of GH3 genes (IAA-aminosynthase enzyme) catalyzing aminoacid conjugation to Weeda et al., 2014 auxin. Auxin efflux transporters Alteration in the expression of IAA/IBA genes and efflux transporters namely PIN1, PIN3, PIN7, Wen et al., 2016 IAA19, and IAA24 Auxin induced transcription Auxin associated transcription factors, namely WRKY, NAC, MYB are altered in activity Liang et al., 2017 Auxin biosynthesis YUC1, YUC2, YUC5, YUC6, and TAR2 get downregulated Wang et al., 2016 Cytokinin induced senescence Downregulation of senescence genes namely LpSAG12 and Lph36 Zhang et al., 2017 Cytokinin biosynthesis Upregulation of cytokinin biosynthesis genes (LpIPT2 and LpOG1) Zhang et al., 2017 Cytokinin responsive transcription factors Changes in expression patterns of A-ARRs and B-ARRs Zhang et al., 2017 Cytokinin – PR protein interaction PR-10 investigated to be a low affinity melatonin binder Sliwiak et al., 2018 Gibberellic acid pathway Upregulation of gibberellin pathway (GA) genes like D-limonene synthase, Gibberellin 2-oxidase Li et al., 2017 GA biosynthesis genes Upregulation of GA20ox and GA3ox Zhang et al., 2014a; Zhang et al., 2014b Abscisic acid catabolism Upregulation of CYP707 monooxygenases Zhang et al., 2014a ABA biosynthesis Downregulation of enzyme 9-cis-epoxycarotenoid dioxygenase (NCED), LpZEP and LpNCED1 Zhang et al., 2014a Zhang et al., 2017 ABA receptor Downregulation of PYL8 Li et al., 2017 ABA responsive transcription factors Upregulation of LpABI3 and LpABI5 Zhang et al., 2017 Salicylic acid biosynthesis Upregulation of isochorismate synthase-1 (ICS-1); SA biosynthetic enzyme Lee and Back, 2016 Kinases Immune response triggered by mitogen-activated protein kinase (MAPK) and OXI1 (oxidative Lee and Back, 2016, 2017 signal-inducible1) kinase pathway Nitric oxide Differential modulation of Cu/Zn and Mn SOD isoforms Arora and Bhatla, 2017 glutathione homoeostasis Kaur and Bhatla, 2016 Ethylene biosynthesis Upregulation of aminocyclopropane- 1-carboxylic acid (ACC) synthase expression Sun et al., 2015 Ethylene receptor Upregulation of ethylene receptor genes, NR and ETR4, and signaling mediator elements, EIL1, Sun et al., 2015 EIL3 and ERF2. Brassinosteroids Upregulation of DWARF4, a rate-limiting BR biosynthetic gene Hwang and Back, 2018 Polyamines (putrescine, spermidine) Triggering NO biosynthesis Zhou et al., 2016a,b Ding et al., 2017

39 S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45 achieved as a result of long distance signaling response produced by melatonin in its downstream pathway triggers ethylene biosynthesis by melatonin (Li et al., 2017). In this context the effect of exogenous overexpressing ACC synthase activity. Alternately in another report by melatonin treatment has significantly up regulated the transcriptomic Arnao and Hernández-Ruiz (2007b) melatonin treatment in etiolated profile of some major gibberellin pathway (GA) genes like D-limonene lupin seedlings reduced ethylene synthesis. Similar observations have synthase, Gibberellin 2-oxidase, and Gibberellin-regulated family pro- also been proposed by Kim et al. (2001). This observation was in con- teins. These effects have been attributed to induce a systemic response gruence to Weeda et al. (2014). The author and co-workers reported of melatonin towards inducing cold stress tolerance through long dis- two ACC genes to be upregulated by melatonin in Arabidopsis of which tance signaling from roots to the aerial parts of the plant (Li et al., one was auxin inducible. Thus the act of melatonin induced ethylene 2017). Melatonin induced salt stress alleviation has been reported in crosstalk involves IAA inducible steps in ACC synthase activation. Cucumis sativus where promotion of seed germination has been attributed to the partial increase in the GA biosynthetic genes GA20ox and 4.5. Melatonin crosstalk with jasmonates and salicylic acid GA3ox. These genes exhibited 2.3 and 3.9 fold higher expression levels induced by exogenous melatonin treatment at 0 and 12 h of NaCl stress Biotic stress defense, metabolic regulation of sugars and pigment respectively. The seeds of Cucumis were found to possess higher content biosynthesis appear to be some of the major outcomes of melatonin of GA4 thus suggesting the potential role of melatonin in regulation of crosstalk with SA and JA (Fig. 3; Table 2). Salicylic acid is an important GA catabolism (Zhang et al. 2014a, 2014b). A recent finding on the role defense molecule in plants which triggers hypersensitive responses of melatonin induced repression of floral transition in Arabidopsis has against various pathogens. In the metabolic pathway melatonin and been reported to be mediated by stabilization of DELLA proteins. salicylic acid share their common precursor chorismic acid which However, endogenous GA levels did not show any change in response to produces tryptophan (precursor for melatonin) and shikimic acid exogenous melatonin (Shi et al., 2016b). Gene expression analysis re- (precursor for salicylic acid) (Hernandez-Ruiz and Arnao, 2018). In vealed diurnal regulation of gibberellins and serotonin biosynthesis in respect of functional significance both the molecules have been ob- rice. The two pathways were reported to be independently activated served to exhibit similar effects in terms of seed germination, seedling under a similar photoperiodic duration of 20 h (Dharmawardhana et al., growth, stomatal regulation, biotic and abiotic stress (Hernandez-Ruiz 2013). The effect of melatonin on salt stress amelioration in Cucumis and Arnao, 2018). Oxidative and drought stress primimg can be pre- also operates through alteration of ABA metabolism. ABA catabolism ferentially obtained by the help of exogenous treatments from both genes (CYP707 monooxygenases) were upregulated while ABA bio- these molecules. They regulate water potential changes, redox system synthesis enzyme 9-cis-epoxycarotenoid dioxygenase (NCED) has been management and maintain photosynthetic pigment components (Arnao observed to be downregulated upon treatment with melatonin (Zhang and Hernandez-Ruiz, 2014; Pal et al., 2013; Shamshul, 2013). The et al., 2014a). Similar evidences in Malus leaves also support the fact mechanism of melatonin and salicylic induced biotic stress tolerance that melatonin mediated suppression of ABA levels primarily acts has gathered several reports mentioning tolerance against pathogens through upregulation of its catabolism and down regulation of its namely Diplocarpon, Penicillium, Pseudomonas, Phytophthora, Botrytis, synthesis (Li et al., 2015). Interestingly in barley melatonin treatment Fusarium and Collectotrichum (Arnao and Hernandez-Ruiz, 2015; Lee associated with cold stress was accompanied by increased ABA accu- et al., 2014, Wei at al. 2016, Yin et al., 2013; Yu and Zhu, 2006; Zhang mulation manifested as a result of drought priming (Li et al., 2016). et al., 2017b). Analysis of SA pathway mutant has revealed the role of However, endogenous melatonin accumulation was independent of melatonin in upregulation of isochorismate synthase-1 (ICS-1; SA bio- ABA biosynthesis. In another investigation of cold stress tolerance of synthetic enzyme) and SA related genes induced by pathogen stress chinese wild rye grass genotypes, melatonin upregulated ABA bio- (Lee and Back, 2016, 2017; Zhang et al., 2017b). SNAT mutants were synthesis (Fu et al., 2017). Such elevation in ABA levels induced by observed with both reduced levels of melatonin and salicylic acids (Lee melatonin imparted cold tolerance by modulating ROS levels, mal- et al., 2015). Melatonin mediated immunity has been reported to be ondialdehyde content and accumulation of major antioxidants. The triggered by mitogen-activated protein kinase (MAPK) and OXI1 (oxi- effect of melatonin induced ABA surge suggested that ABA was a dative signal-inducible1) kinase pathway (Lee and Back, 2016, 2017). downstream component in the melatonin-ABA crosstalk. In contrast Association of melatonin with jasmonic acid signaling pathway is sug- watermelon plants induced by cold stress exhibited downregulation of gested to be inclusive of models proposed by Wasternack and Hause ABA receptor PYL8 (Li et al., 2017). Heat stress induced senescence in (2013) and Shyu and Brutnell (2015). In the pathway of disease re- perennial rye grass leaves has been observed to be delayed by mela- sistance melatonin acts upstream to JA and SA signaling (Zhu and Lee, tonin (Zhang et al., 2017a). This effect was partially attributed to the 2015). The interrelationship of SA, ethylene and nitric oxide has been decrease in ABA synthesis caused by downregulation of two ABA bio- reported for melatonin induced immunity against fungal and bacterial synthesis genes (LpZEP and LpNCED1). Furthermore melatonin also pathogens (Lee and Back, 2017; Qian et al., 2015; Shi et al., 2015a; c; suppressed the upregulation of two ABA associated transcription factors 2016b). Apart from biotic stress defense anthocyanin pathway regula- LpABI3 and LpABI5. Evidences briefly signify that melatonin appear as tion has been recently reported to be under the control of JA-melatonin both positive and negative regulator of ABA biosynthesis and signaling crosstalk in Arabidopsis (Yu and Ziqiang, 2018). The authors reported (Dharmawardhana et al., 2017). Considering cold stress tolerance and the role of melatonin in suppressing JA-induced suppression of antho- heat stress-induced senescence delay, both the effects of ABA is bene- cyanin biosynthesis in leaves. However, the act of melatonin-induced ficiary. anthocyanin biosynthesis does not disrupt JA signaling. Current un- Melatonin induced elevation of ethylene levels are associated with derstandings of the physiological implications of flavonoid biosynthesis climacteric fruit ripening in tomato and other fruits (Sun et al., 2016). regulation by these two molecules are still at its initial stage. However, Sun et al. (2015) reported the biochemical changes associated with fruit based on the initial reports further possibilities of melatonin-JA ripening induced by melatonin. The downstream action of melatonin pathway are yet to be investigated. Since anthocyanin accumulation in induced little increase in ethylene synthesis accompanied by lycopene plant organs is often a inducible stress marker resulting due to altered accumulation, fruit softening and colour change. Melatonin treatment nitrogen metabolism it is possible that melatonin-JA signaling may, elevated 1-aminocyclopropane- 1-carboxylic acid (ACC) synthase ex- however, regulate such responses. pression followed by ethylene receptor genes, NR and ETR4, and signaling mediator elements, EIL1, EIL3 and ERF2. The parameters of fruit 4.6. Nitrosative stress induced melatonin-nitric oxide crosstalk operates ripening including ethylene synthesis and increase in ascorbic acid, through ROS/RNS homoeostasis and polyamine accumulation in plants sugars, cell wall loosening and pigmentation have been evidenced as an effect of melatonin treatment. Thus the current evidences clarify that Nitric oxide and reactive oxygen species are transiently expressed

40 S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45

Fig. 4. Illustrative account of melatonin-auxin-nitric oxide crosstalk regulating seedling growth and development in plants. (Source: author). rapid signaling molecules modulating various developmental and me- methyltransferase (HIOMT). Liu et al. (2015a) reported the ameliora- tabolic functions in normal and stressed plant systems (Astier et al., tive effects of melatonin induced NO generation in tomato roots sub- 2016). NO-mediated signaling process operates separately through both jected to sodic alkaline stress. Furthermore Liu et al. (2015b) reported reactive nitrogen species and reactive oxygen species pathways. Among the significance of exogenous melatonin (0.5 μM) in promoting anti- various effects induced by NO protein S-nitrosylation, modification of oxidative defense in sodic stress affected tomato plants and subsequent lipids and DNA and enzyme activity modulation are involved in stress regulation of ion channel activity. Melatonin treatment decreased sodic acclimatization in plants (Damiani et al., 2016; Pucciariello and Perata, stress induced sodium accumulation while increased potassium reten- 2017). Interestingly enough, the mode of action of melatonin-nitric tion in the plants. Evidences therefore suggest that melatonin induced oxide crosstalk operates through mutual influences. There lies certain ROS homoeostasis is also accompanied by ion channel modulation thus degree of complexity in the pathway of melatonin-NO interaction regulating Na+/K+ exchange in tomato plant roots. Melatonin-NO which makes it difficult to understand their upstream or downstream signaling in response to bacterial infection involves elevation of sugars position in the signaling cascade. Melatonin jointly interacts with hy- and glycerol induced by exogenous melatonin treatments (Qian et al., drogen peroxide and nitric oxide to undergo post-translational mod- 2015; Shi et al., 2015a; d). These molecules were reported to promote ifications and modulation of hormone activities (Arnao and Hernández- downstream surge in NO biosynthesis in Arabidopsis leaves. Ruiz, 2015; Nawaz et al., 2016). Melatonin mediated cold stress toler- The current understandings of melatonin-NO crosstalk associated ance operates through decreased ROS, malondialdehyde contents and with polyamine accumulation have been established on the evidences increasing antioxidants (glutathione, ascorbate) and associated en- of few reports although much remains to be investigated. Melatonin zymes (SOD, CAT, APX and GR) (Fu et al., 2017). Salinity stress-in- induced nutrient stress tolerance in Arabidopsis has been reported to be duced ROS generation and its homeostasis have been reported to be associated with polyamine accumulation coupled to NO synthesis (Zhou regulated by melatonin-nitric oxide signaling in etiolated sunflower et al., 2016a,b). Cold stress and melatonin treatment have been re- seedlings (Arora and Bhatla, 2017). The authors reported that salinity ported to alter polyamine levels (putrescine, spermidine, and spermine) induced Mel-NO crosstalk is manifested by differential modulation of together with sucrose and proline in tomato plants (Ding et al., 2017). Cu/Zn and Mn SOD isoforms in seedling cotyledons. Furthermore NO- Alternately polyamine induced nitric oxide synthesis in cold stressed induced melatonin accumulation has been correlated with its detox- tomato seedlings provide clue towards NO-polyamine relation mediated •- ifying effect on superoxide anion (O2 ) and peroxynitrite anion by ROS/RNS levels. Therefore it is worthwhile to think that melatonin- − (ONOO ) in salt stress-induced seedling cotyledons. Another instance NO operate through ROS and RNS levels and is mediated by polyamine of NO-melatonin crosstalk in mediating glutathione homoeostasis in accumulation in plants. However, as far it appears, IAA and SA are also salt stressed-sunflower seedlings has been reported by Kaur and Bhatla possible candidates in the NO-melatonin cascade associated with root (2016). Melatonin and nitric oxide regulated GR activity and GSH development and regulation of biotic stress defense (Fig. 4; Table 2). content in sunflower seedlings. Investigations from animal system have revealed the modulatory role of melatonin in mitochnondria of HeCat 4.7. Melatonin-induced alleviation of photosynthetic activity inhibition cells where the amine triggered the expression of nitric oxide synthase operates through ROS scavenging mechanisms during abiotic stress tolerance (NOS; nitric oxide biosynthesizing enzyme) (Sarti et al., 2013). The effects were manifested as signaling response of melatonin in nano- Chloroplasts are susceptible to alterations in their structural and molar concentrations effective within a time span of few hours. This physiological properties in response to abiotic stress (Tambussi et al., evidence in congruence with reports from plant systems therefore re- 2004; Foyer and Shigeoka, 2011). Abiotic stress-induced decrease in veals the similar pattern of NO-melatonin crosstalk, where melatonin chlorophyll content has been associated with a reduction in chlorophyll appears to be a positive regulator of NO accumulation. In contrast re- fluorescence and decreased ATP/NADPH generation (Moustaka et al., ports by Kaur and Bhatla (2016) infer that sodium nitroprusside (exo- 2015). Incomplete dissipation of energy through the electron transport genous NO donor) down regulates the activity of hydroxyindole-O- chain of photosystem I and II often result in excitation of chlorophyll

41 S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45 molecules and generation of reactive oxygen species (ROS). These free mutant wheat (ANK32B) exhibited better carbon assimilation cap- radicals disrupt the redox potential of protein components in and be- abilities in response to melatonin priming in maternal plants during the tween PS I and PS II centres. Analysis of fluorescence from chlorophyll grain filling stage (Li et al., 2018). To summarize, the effect of mela- molecules is a measure of photosynthetic efficiency, where a part of the tonin in protection of photosynthetic pigments mostly operates through energy received is dissipated in form of fluorescence (Iriel et al., 2014; scavenging of ROS and elevation of antioxidant enzyme activities. Moustaka et al., 2015). Melatonin has been reported to possess alle- Briefly, it appears that melatonin exerts multiple signaling mechanisms viating properties towards photosynthetic pigment loss and quantum to restore chloroplast integrity, redox homoeostasis, photosystem pro- yield efficiency in response to abiotic stress. Recent investigations over tein restoration and improved energy transport efficiency during abiotic the past few years have revealed the antioxidative property of mela- stress. tonin to be effective in maintaining the pigment constitution of chloroplasts. Additionally, photosynthetic proteins associated with photo- 4.8. Brassinosteroid and hydrogen sulphide crosstalk with melatonin: system I and II have also been reported to be restored by exogenous avenues for future research melatonin treatment. Melatonin induced-response in relation to major abiotic stress factors (salinity, drought, temperature and herbicide ef- Various roles of brassinosteroids (BR) have already been in- fect) have been analyzed for chlorophyll and carotenoid content, D1 vestigated widely in several plant systems. However, recent investiga- protein levels, energy transport efficiency. Apart from angiosperms tion has revealed the molecular mechanism of melatonin-brassinos- melatonin-induced regulation of photosynthetic efficiency has also teroid crosstalk regulating seedling development in rice (Hwang and been reported to be operative among algal (Characeae) and dino- Back, 2018). Expression of SNAT2 isogene involved for encoding mel- flagellate members (Lazár et al., 2013; Roopin et al., 2013). Exogenous atonin biosynthesizing enzyme is diurnally regulated in rice plants. melatonin supplementation (10 μM) to pond water reveals a 34% in- Analysis with suppressed expression of SNAT2 (RNAi lines) revealed crease in the quantum yield of PSII in Chara australis (Lazár et al., lesser production of BR in comparison with that of wild type. Ad- 2013). The better functionality of PS II signifies an efficient electron ditionally exogenous melatonin treatment upregulated the expression transport chain coupled to higher photosynthetic efficiency. Con- of one or more BR genes. The authors report the significance of sidering the fact that ROS liberation damages both photosynthetic DWARF4, a rate-limiting BR biosynthetic gene being mediated by pigments and associated proteins it is worthwhile to appreciate the melatonin (Table 2). This observation suggests that regulation of BR antioxidative properties of melatonin. Wang et al. (2012) reported the biosynthetic gene is one of the main mechanisms of melatonin mediated anti-senescence property of melatonin to be operative through the as- BR crosstalk assisting in plant development. The morphological aspects corbate-glutathione pathway. Chilling stress-induced damage of chlor- of the SNAT2 gene suppression by RNAi lines resulted in dwarf habit of oplast integrity in Cucumis sativus has been reported to be resulting due rice seedlings with erect leaves. Melatonin-BR crosstalk was found to be to ROS generation (Zhao et al., 2016). Exogenous melatonin (200 μM) associated with skotomorphogenesis of the seedlings. In another report was reported to enhance the ascorbate-glutathione system for ROS by Alam et al. (2018) turf grass (Festuca arundinacea Schreb.) was in- scavenging in chloroplasts subjected to chilling stress. The surge in ROS vestigated to have attained better thermotolerance in response to exo- count in chloroplast mostly arises from disrupted electron transport genous melatonin and 24-epibrassinolide. Treatments with both these system of PSII component of light reaction. Similar investigations with biomolecules reduced ROS levels, electrolytic leakage and mal- exogenous melatonin (100 μM) following chilling stress in Bermuda ondialdehyde content while increased protein and cholorophyll synth- grass [Cynodon dactylon (L).Pers.] revealed increased superoxide dis- esis. Furthermore the activity of antioxidant enzymes namely POD, SOD mutase (SOD) and peroxidase (POD) activity accompanied by higher and CAT were elevated within hours of treatment. The mode of action chlorophyll content (Fan et al., 2015). Melatonin-induced retention of of melatonin and epibarssinolide although appearing similar require higher chl a/b ratio in presence of chilling stress was thus attributed to further investigations. This shall unveil the multiple pathways of Mel- better functioning of redox homoeostasis in the chloroplasts. The au- BR crosstalk assisting in growth, development and stress tolerance. thors also reported a higher quantum yield of PS II manifested as an Possibilities of other biomolecules acting as Mel-BR crosstalk mediator effect of exogenous melatonin. Interesting observations of the effect of cannot be ruled out. Since the last decade of research hydrogen sul- melatonin on photosynthetic efficiency and carbon assimilation have phide has emerged as a potential signaling molecule in plants. This been reported in wheat plants induced by nano–ZnO stress (Zuo et al., gaseous molecule has been associated with rapid signaling events like 2017). The authors mentioned the relevance of various nano-particles stomatal opening, ion channel regulation and nitric oxide accumula- being released into the environment which often contributes to abiotic tion. However, further investigations are required to decipher the stress. Exogenous melatonin application improved chlorophyll content, possible crosstalk mechanisms of hydrogen sulphide and melatonin in enhanced energy transport system and elevated Rubisco and ATPase plants. Considering the fact that hydrogen sulphide interacts with activity. Melatonin-induced enhancement of Rubisco activity plays a several biomolecules it is possible that melatonin may also likely crucial role in maintaining carbon assimilation during ZnO stress. Dose- modulate hydrogen sulphide mediated physiological effects in plants. dependent response of exogenous melatonin (20 and 100 μM) has been reported to be more effective in seed priming and root immersion ex- 4.9. Phytomelatonin receptor mediated stomatal closure operates through periments. In rice seedlings subjected to cold stress, the effect of mel- hydrogen peroxide and calcium signaling: recent development atonin was manifested by responses of improved PSII photochemical efficiency and antioxidative mechanisms (Han et al., 2017). Melatonin has been anticipated as a putative phytohormone with Apart from maintaining chlorophyll content and photosystem effi- plethora of physiological effects in plants. In this context recent de- ciency, melatonin has also been reported to exhibit translational reg- velopments have revealed the involvement of CAND2/PMTR1 as a po- ulation over D1 protein (Zhou et al., 2016a,b). Salinity stress-induced tent phytomelatonin receptor in Arabidopsis (Wei et al., 2018). Mela- regulation of D1 protein translation operates through downstream tonin induced stomatal closure in Arabidopsis operates through CAND2 signaling of melatonin action. Melatonin-induced alleviation of D1 membrane protein-melatonin binding. The authors reported specific protein and S protein level (PSII subunit) has also been evidenced in salt and saturable binding affinities of the receptor towards melatonin. The stress-induced maize seedlings (Chen et al., 2018). Carotenoids are downstream action of receptor mediated melatonin binding has been accessory pigments acting to shield chlorophyll molecules from harmful reported to be manifested by H2O2 production and calcium influx thus photo bleaching effects. Melatonin-induced restoration of pigment regulating stomatal closure. Arabidopsis mutants lacking cand2 activity system in response to paraquat herbicide stress involves an increase in were found to be insensitive to melatonin induced stomatal closure. 2+ carotenoid content (Szafrańska et al., 2016). Chlorophyll b-deficient Absence of receptor functioning completely abolished H2O2 and Ca

42 S. Mukherjee Plant Physiology and Biochemistry 132 (2018) 33–45 signaling. Thus melatonin receptor mediated hydrogen peroxide and Arnao, M.B., Hernández-Ruiz, J., 2007b. Inhibition of ACC oxidase activity by melatonin calcium signaling in plants remains as an upcoming area for further and IAA in etiolated lupin hypocotyls. In: Ramina, A., Chang, C., Giovannoni, J., Klee, H., Perata, P., Woltering, E. (Eds.), Advances in Plant Ethylene Research. Springer, investigations. Dordrecht, pp. 101–103. Arnao, M.B., Hernández-Ruiz, J., 2009. Protective effect of melatonin against chlorophyll 5. Conclusions degradation during the senescence of barley leaves. J. Pineal Res. 46, 58–63. Arnao, M.B., Hernández-Ruiz, J., 2014. Melatonin: plant growth regulator and/or bios- timulator during stress? Trends Plant Sci. 19, 789–797. The pleotropic nature of serotonin and melatonin has been evi- Arnao, M.B., Hernández-Ruiz, J., 2015. Functions of melatonin in plants: a review. J. denced in the form of plant growth modulator, effector molecule, me- Pineal Res. 59, 133–150. tabolic mediator and rapid signaling molecule in various plants sys- Arnao, M.B., Hernández-Ruiz, J., 2017. Growth activity, rooting capacity, and tropism: three auxinic precepts fulfilled by melatonin. Acta Physiol. Plant. 39, 127. tems. The amphiphatic nature of serotonin and melatonin impart them Arora, D., Bhatla, S.C., 2017. Melatonin and nitric oxide regulate sunflower seedling the capability to move across membranes. The molecules although growth accompanying differential expression of Cu/Zn SOD and Mn SOD. Free Radic. – present in most plant organs has been more pronounced in stressful Biol. Med. 106, 315 328. Astier, J., Loake, G., Velikova, V., Gaupels, F., 2016. Editorial: interplay between NO situations. Melatonin has been widely involved with several pathways signaling, ROS, and the antioxidant system in plants. Front. Plant Sci. 7, 1731. modulated by hormones, ROS and other growth regulators. The cross- Beilby, M.J., Turi, C.E., Baker, T.C., Tymm, F.J.M., Murch, S.J., 2015. Circadian changes talk mechanisms of serotonin and melatonin are mostly operated by in endogenous concentrations of indole-3-acetic acid, melatonin, serotonin, abscisic acid and jasmonic acid in Characeae (Chara australis Brown). Plant Signal. Behav. 10 receptor mediated downstream signaling components for various mo- (11) e1082697. lecules such as IAA, GA, CK, ABA, ethylene, jasmonates, SA or NO. Back, K., Tan, D.X., Reiter, R.J., 2016. Melatonin biosynthesis in plants: multiple path- Auxin-serotonin crosstalk in response to various environmental cues ways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J. Pineal Res. 61, 426–437. requires to be further investigated. Possibilities of tryptophan getting Burkhardt, S., Tan, D.X., Manchester, L.C., Hardeland, R., Reiter, R.J., 2001. 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