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Review

Relationship of Melatonin and Salicylic Acid in Biotic/Abiotic Plant Stress Responses

Department of Plant Biology (Plant Physiology), Faculty of Biology, University of Murcia, Campus de Espinardo, 30100-Murcia, Spain
*
Author to whom correspondence should be addressed.
Submission received: 22 February 2018 / Revised: 14 March 2018 / Accepted: 21 March 2018 / Published: 22 March 2018
(This article belongs to the Special Issue Salicylic Acid in Plant Stress Responses)

Abstract

:
Melatonin (N-acetyl-5-methoxytryptamine) was discovered in plants in 1995, while salicylic acid was the name given to the active ingredient of willow in 1838. From a physiological point of view, these two molecules present in plants have never been compared, even though they have a great number of similarities, as we shall see in this work. Both molecules have biosynthesis pathways that share a common precursor and both play a relevant role in the physiology of plants, especially in aspects related to biotic and abiotic stress. They have also been described as biostimulants of photosynthetic processes and productivity enhancers in agricultural crops. We review the coincident aspects of both molecules, and propose an action model, by which the relationship between these molecules and other agents and plant hormones can be studied.

1. Melatonin and Salicylic Acid in Plants

Melatonin (N-acetyl-5-methoxytryptamine) is a pleiotropic molecule with a wide range of cellular and physiological actions in living organisms, including animals and plants. It was discovered in animals (cow) by Lerner and colleagues in 1958 and in 1959 in humans [1,2]. Then, in 1995, two papers simultaneously demonstrated the presence of melatonin in plants, and it is now accepted that melatonin is present in all higher plants [3,4], where it is sometimes referred to as phytomelatonin [5,6]. Chemically, melatonin is an indoleamine derivative of the amino acid tryptophan, and its biosynthetic melatonin pathways from tryptophan have been extensively studied in both animals and plants (Figure 1). Tryptophan is converted into 5-hydrotryptophan in animals, whereas in plants tryptophan is mainly transformed into tryptamine. These last two compounds are converted into serotonin (5-hydroxytryptamine), which is finally converted into melatonin (N-acetyl-5-methoxytryptamine) through the compounds N-acetylserotonin or 5-methoxytryptamine (see Figure 1). All the enzymes involved in melatonin biosynthesis have been described and characterized in many species of animals and plants [7].
The name salicylic acid (SA) (ortho-hydroxybenzoic acid) was given to the active ingredient of willow (Salix sp.) bark by Raffaele Piria in 1838. The first commercial production of synthetic SA began in Germany in 1874. Aspirin, a trade name for acetylsalicylic acid, was introduced by the Bayer Company in 1898 and it rapidly replaced the use of SA as it produced less gastrointestinal irritation but had similar medicinal properties [8]. Salicylic acid is a phenolic compound. The shikimic acid pathway takes part in the biosynthesis of most plant phenolic compounds. The most common pathway in plants for SA synthesis is the phenylalanine pathway (Figure 1). However, SA biosynthesis may also be carried out by the isochorismic acid pathway. The hydroxylation of benzoic acid catalyzed by the enzyme benzoic acid 2-hydroxylase synthesizes SA. Benzoic acid is synthesized by trans-cinnamic acid (produced from phenylalanine by the action of enzyme phenylalanine ammonia lyase), either via β-oxidation of fatty acids or via a non-oxidative pathway in which trans-cinnamic acid is hydroxylated to form ortho-coumaric acid followed by oxidation of the side chain (Figure 1) [9,10,11,12].
Melatonin and SA biosynthesis pathways share a final common precursor—chorismic acid—which is generated from shikimic acid (a condensation product of phosphoenolpyruvic acid from glycolysis and erythrose 4-phosphate from the pentose phosphate pathway (Figure 1). Chorismic acid is the precursor of the synthesis of three aromatic amino acids—phenylalanine, tryptophan and tyrosine. Melatonin is synthetized from tryptophan through the anthranilate/indole pathway and SA from phenylalanine, in addition to the direct isochorismic acid route (Figure 1).
With respect to catabolism, melatonin is usually hydroxylated in different positions of the indole ring, with 2-hydroxymelatonin being the major catabolite [13]. In the case of SA, several conjugates have been described, such as methyl salicylic acid, salicyloyl-l-aspartic acid, salicylic acid 2-O-β-glucoside and salicyloyl-glucose ester [9].

2. Common Effects of Melatonin and SA in Abiotic Plant Stress

Melatonin has been considered a multiregulatory molecule in higher plants because of the wide and diverse range of cellular and physiological actions attributed to it. In 2004, the action of melatonin as a growth promoter was demonstrated in etiolated Lupinus albus [14]. Also, melatonin is able to induce root primordials from pericycle cells, generating new adventitious and lateral roots [15]. A significant role of melatonin against abiotic stress was also postulated, using a cold-induced apoptosis model in carrot cells [16]. Thus, melatonin has been attributed with the capacity to regulate cellular and plant growth; promote seed germination and rooting; optimize photosynthetic efficiency and water/CO2 foliar exchange; regulate the internal biological clock and flowering and ripening/senescence processes; and finally, to act as an endogenous biostimulator against abiotic or biotic stressors [17,18].
Many physiological functions have also been assigned to SA. In 1989, Carswell and colleagues reported that acetyl SA can promote colony formation in maize protoplasts, suggesting a role in the regulation of the cell cycle [19]. The first indication of a physiological effect on the part of SA was the discovery of it role in flowering induction and bud formation in tobacco cell cultures [20]. The pioneering works of Malamy et al. (1990) on the effect of SA in Tobacco Mosaic Virus [21] and of Métraux et al. (1990) on the role of SA as signaling in systemic acquired resistance (SAR) [22] clearly demonstrated the implications of SA in plant pathogen responses. Also, SA influences seed germination, seedling establishment, cell growth, respiration, stomatal closure, senescence-associated gene expression, basal thermotolerance, nodulation in legumes, and fruit yield, among others [8,9,23,24]. In both cases (melatonin and SA), the role in some of these processes may be indirect because they modulate the synthesis and/or signaling of other plant hormones [25,26] (see below). Table 1 presents a list of the physiological effects in which both molecules (melatonin and SA) seem to play a relevant role. As can be seen, there are many coincidences between both molecules, but undoubtedly the aspects that have aroused most interest are those related to their actions in improving resistance to stress situations.
Table 2 and Table 3 show some representative examples in which the protective roles of melatonin and SA against different abiotic stresses have been studied. As can be seen, many aspects show close similarities between both molecules. In general, both are involved in responses to abiotic stress situations, including a marked improvement in the water status in drought situations, enhanced biosynthesis of photosynthetically active pigments as well as of the photosynthetic rate, an increase in metabolites and antioxidant enzymes to balance the redox status, osmotic adjustment to reduce of membrane injury under stress conditions, and in some cases, growth promotion and enhanced productivity and yield [8,17,18,27,28,29,30].

3. Melatonin and SA in Biotic Stress (Plant Pathogen Response)

Table 4 and Table 5 provide a list of the papers related to the positive effect of melatonin and SA on plant pathogen responses. In the first paper, related to melatonin and fungus plant-pathogen infection, melatonin-treated apple trees using root irrigation improved the resistance of Malus prunifolia against the fungus Diplocarpon mali (Marssonina apple blotch). At 20 days, the treated trees showed a lower number of damaged leaves, higher chlorophyll content, a more efficient Photosystem II, and less defoliation than infected untreated trees. In general, melatonin helped plants with resistance to fungal infection, reducing lesions, inhibiting pathogen expansion, and generally alleviating disease damage [87]. Also, in some in vitro assays, different concentrations of melatonin showed growth inhibition activities against plant fungal pathogens such as Alternaria spp., Botrytis spp., and Fusarium spp. The same occurred in plant-pathogen attacks by Penicillium spp. in non-sterilized Lupinus albus seeds [17]. Table 4 shows five papers that used the Arabidopsis/Pseudomonas syringae as a model of plant–bacterial pathogen interaction. Melatonin induced pathogen-related genes in Arabidopsis (also in tobacco plants), which is in accordance with the possible role of this methoxyindole as a defence signalling molecule against pathogens in plants. In a recent and significant paper, Zhang et al. (2017) demonstrated that melatonin attenuates severe potato late blight caused by Phytophthora infestans. Melatonin induced plant innate immunity against fungal infection, inhibiting mycelial growth and changing expression of many genes associated with stress and virulence [88]. In sum, melatonin up-regulates pathogenesis-related, SA and ethylene-dependent genes, an effect that was suppressed in mutants defective in SA and ethylene signalling. Also, melatonin increased nitric oxide (NO) and SA-related genes, accompanied by reduced susceptibility to the pathogen, leading to an increase in both melatonin and NO. SNAT knockout mutants not only exhibited reduced levels of melatonin, but also lower levels of SA, along with a greater susceptibility to the pathogen [89]. No studies on plant viruses and melatonin have been published to date. Nevertheless, in animals, melatonin is a good therapeutic alternative for fighting bacterial, viral and parasitic infections [90]. Also, during sepsis, melatonin has been reported to block the overproduction of pro-inflammatory cytokines and increase interleukin-10 levels. With respect to viral infection, Venezuelan equine encephalomyelitis (VEE) is an important human and equine disease caused by the VEE virus. Reactive oxygen species (ROS) have been implicated in the dissemination of the responsible virus, and its deleterious effects may be diminished by melatonin treatment. The administration of melatonin significantly decreased the virus level in the blood and brain compared with the levels seen in infected control mice [90].
With respect to SA, the exogenous application of SA at non-toxic concentrations to susceptible fruits and vegetables could enhance resistance to pathogens and help control post-harvest decay [97]. SA effectively reduced fungal decay in a concentration-dependent manner, as can be seen in the examples of Table 5. In the case of SA, some studies indicate that it inhibits viral replication [98,99,100].

4. Melatonin, SA and ROS/RNS Network

A relevant role for NO in melatonin responses is proposed, mainly for auxin-like and plant immune responses. NO and other radical nitrogen species (RNS) and ROS are key signals that increase under abiotic/biotic stress [8,106]. Generally, RNS and ROS signals tend to act in a coordinated way. NO levels are self-regulated and also regulate the ROS network through NO-dependent, post-translational modifications [107]. NO modulates several functions through protein modifications by nitration, S-nitrosylation and the ligation of NO to transition metals, but also through the modification of lipids (nitro-fatty acids) and DNA (8-nitroguanine) [108,109,110,111,112]. Moreover, NO triggers a set of responses to alleviate stress and cellular damage, which includes transient metabolic reprogramming in both primary and secondary metabolic pathways [107].
Abiotic and biotic stress induce an increase in endogenous melatonin through the upregulation of melatonin biosynthetic genes [96,113]. Melatonin also increases NO levels through the upregulation of nitrate reductase (which usually reduces nitrate to nitrite, but can also reduce nitrite to NO using NADPH as a cofactor). Also melatonin induces the NO synthase-like pathway, in iron deficiency-induced NO in rice [114]. Thus, melatonin can also act as an NO and ROS scavenger, and curiously, in an NO feedback mechanism, NO induces melatonin biosynthesis [113].
Although some data point to the possibility that melatonin might act as an upstream signal, the complexity of the melatonin–NO interaction makes it difficult to elucidate whether melatonin is upstream or downstream of NO. Also, H2O2 (an important signal molecule in stress situations), seems to be decisive in the upregulation of melatonin biosynthesis enzymes, taking as a response an increase in melatonin levels in stressed plants. In short, mitogen-activated protein kinase (MAPK) signalling, SA, NO, and H2O2, as well as their cross-talk, are required for melatonin-mediated innate immunity in Arabidopsis. Also, melatonin and NO change the expression of several transcription factors and hormone signalling elements, which determines the overall anti-stress response. Also, some plant hormones such as IAA, CKs and ABA can stimulate NO production [25,26].
This complex relationship between ROS, NO and melatonin is pictured in Figure 2. In the case of abiotic stress, no model including the signalling cascade for melatonin and SA has been proposed to date. Fleta-Soriano et al. (2017) studied the role of melatonin in plant response to drought stress and recovery in maize plants [115]. Furthermore, in that study, the endogenous contents of melatonin positively correlated with those of stress-related phytohormones, particularly with those of SA, although exogenous application of melatonin did not alter the contents of any phytohormone.
A model of melatonin/SA/NO/ROS action in biotic stress responses (pathogen resistance) has been proposed [9,25] (Figure 3). Pathogen attack increases NO, SA and melatonin levels through ROS. In the well-known model of Arabidopsis/Pseudomonas syringae DC3000 (avrRpt2), plant–pathogen interactions revealed that the mitogen-activated protein kinase cascade (MAPKKK3) and OXI1 (oxidative signal-inducible1) kinases are responsible for triggering melatonin-induced defence signalling pathways [93,116]. The key enzyme in SA biosynthesis—isochorismate synthase-1 (ICS-1)—was upregulated by melatonin, increasing SA levels and triggering a pathogen-induced response. Also, melatonin and NO were able to induce jasmonic acid (JA) biosynthesis and increase several sugar and glycerol levels, all of which activate pathogen-related gene expression. The melatonin-induction of ethylene biosynthesis, through ACC synthase (ACS6), collaborates in the induction of pathogenesis-related genes (PR), whereby ethylene insensitive (EIN), enhanced disease susceptibility 1 (EDS1), phytoalexin deficient 4 (PAD4) and NPR1 factors are key signalling components in the plant SA- and ethylene-mediated defence responses [17,41,91,92,96,116,117,118,119]. More recently, it has been demonstrated that MeRAV1 and MeRAV2 factors (apetala2/ethylene response factor, AP2/ERF) are essential for plant disease resistance against bacterial blight in cassava through the upstream of transcription factors of melatonin biosynthesis genes [96].

5. Future Perspectives for Melatonin and SA in Agronomic Applications

Both molecules are of great interest as modulating agents of anti-stress responses in plants. Also, both have the capacity to directly or indirectly interact with ROS and RNS. Knowledge of the possible relationships with other hormones in aspects related to pathogen resistance and the response to abiotic stresses is of great relevance. The possibility of “sensitizing” plants to abiotic agents through priming or other methods might be of interest in order to increase the resistance of crops. SA- or melatonin-induced activation to reduce damage caused by water deficits (drought), while maintaining the proper metabolism in the face of this stress situation is clearly an essential objective for increasing plant/crop development and yield. Obtaining transgenic plants that overexpressed SA and melatonin biosynthesis genes could be another interesting approach, both for research per se and for application in crops, provided that the limitations to the use of transgenic plants are not transgressed. In both cases, the over-accumulation of SA and melatonin in plant tissues increase the resistance response against stressors. Figure 4 shows a schematic model in which both molecules studied in this paper present agonist behaviour to reduce or moderate the harm caused by stressors with the final aim of improving plant development and crop yield.

Acknowledgments

Thanks to P. Díaz Vivancos for his generous invitation.

Author Contributions

Marino B. Arnao conceived and designed work. Marino B. Arnao and Josefa Hernández-Ruiz analyzed the data. Marino B. Arnao wrote the manuscript. Marino B. Arnao and Josefa Hernández-Ruiz critically revised the final version of manuscript. Marino B. Arnao and Josefa Hernández-Ruiz read and approved the final article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Lerner, A.B.; Case, J.D.; Takahashi, Y.; Lee, T.H.; Mori, W. Isolation of melatonin, a pineal factor that lightens melanocytes. J. Am. Chem. Soc. 1958, 80, 2587. [Google Scholar] [CrossRef]
  2. Lerner, A.; Case, J.; Mori, W.; Wright, M. Melatonin in peripheral nerve. Nature 1959, 183, 1821. [Google Scholar] [CrossRef] [PubMed]
  3. Hattori, A.; Migitaka, H.; Iigo, M.; Yamamoto, K.; Ohtani-Kaneko, R.; Hara, M.; Suzuki, T.; Reiter, R.J. Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates. Biochem. Mol. Biol. Int. 1995, 35, 627–634. [Google Scholar] [PubMed]
  4. Dubbels, R.; Reiter, R.J.; Klenke, E.; Goebel, A.; Schnakenberg, E.; Ehlers, C.; Schiwara, H.W.; Schloot, W. Melatonin in edible plants identified by radioimmunoassay and by HPLC-MS. J. Pineal Res. 1995, 18, 28–31. [Google Scholar] [CrossRef] [PubMed]
  5. Blask, D.E.; Dauchy, R.T.; Sauer, L.A.; Krause, J.A. Melatonin uptake and growth prevention in rat hepatoma 7288CTC in response to dietary melatonin: Melatonin receptor-mediated inhibition of tumor linoleic acid metabolism to the growth signaling molecule 13-hydroxyoctadecadienoic acid and the potential role of phytomelatonin. Carcinogenesis 2004, 25, 951–960. [Google Scholar] [PubMed]
  6. Arnao, M.B.; Hernández-Ruiz, J. The potential of phytomelatonin as a nutraceutical. Molecules 2018, 23, 238. [Google Scholar] [CrossRef] [PubMed]
  7. Back, K.; Tan, D.X.; Reiter, R.J. Melatonin biosynthesis in plants: Multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J. Pineal Res. 2016, 61, 426–437. [Google Scholar] [CrossRef] [PubMed]
  8. Shamsul, H.; Aqil, A.; Alyemeni, M.N. (Eds.) Salicylic Acid: Plant. Growth and Development; Springer: London, UK, 2013; ISBN 978-94-007-6427-9. [Google Scholar]
  9. Vlot, A.C.; Dempsey, D.A.; Klessig, D.F. Salicylic acid, a multi-faceted hormone to combat disease. Annu. Rev. Phytopathol. 2009, 47, 177–206. [Google Scholar] [CrossRef] [PubMed]
  10. Mustafa, N.R.; Kim, H.K.; Choi, Y.H.; Erkelens, C.; Lefeber, A.W.M.; Spijksma, G.; Heijden, R.V.D.; Verpoorte, R. Biosynthesis of salicylic acid in fungus elicited Catharanthus roseus cells. Phytochemistry 2009, 70, 532–539. [Google Scholar] [CrossRef] [PubMed]
  11. Horváth, E.; Pál, M.; Szalai, G.; Páldi, E.; Janda, T. Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. Biol. Plant. 2007, 51, 480–487. [Google Scholar] [CrossRef]
  12. An, C.; Mou, Z. Salicylic acid and its function in plant immunity. J. Integr. Plant Biol. 2011, 53, 412–428. [Google Scholar] [CrossRef] [PubMed]
  13. Byeon, Y.; Tan, D.X.; Reiter, R.J.; Back, K. Predominance of 2-hydroxymelatonin over melatonin in plants. J. Pineal Res. 2015, 59, 448–454. [Google Scholar] [CrossRef] [PubMed]
  14. Hernández-Ruiz, J.; Cano, A.; Arnao, M.B. Melatonin: Growth-stimulating compound present in lupin tissues. Planta 2004, 220, 140–144. [Google Scholar] [CrossRef] [PubMed]
  15. Arnao, M.B.; Hernández-Ruiz, J. Melatonin promotes adventitious- and lateral root regeneration in etiolated hypocotyls of Lupinus albus L. J. Pineal Res. 2007, 42, 147–152. [Google Scholar] [CrossRef] [PubMed]
  16. Lei, X.Y.; Zhu, R.Y.; Zhang, G.Y.; Dai, Y.R. Attenuation of cold-induced apoptosis by exogenous melatonin in carrot suspension cells: The possible involvement of polyamines. J. Pineal Res. 2004, 36, 126–131. [Google Scholar] [CrossRef] [PubMed]
  17. Arnao, M.B.; Hernández-Ruiz, J. Functions of melatonin in plants: A review. J. Pineal Res. 2015, 59, 133–150. [Google Scholar] [CrossRef] [PubMed]
  18. Arnao, M.B.; Hernández-Ruiz, J. Melatonin: Plant growth regulator and/or biostimulator during stress? Trends Plant Sci. 2014, 19, 789–797. [Google Scholar] [CrossRef] [PubMed]
  19. Carswell, G.K.; Johnson, C.M.; Shillito, R.D.; Harms, C.T. O-acetyl-salicylic acid promotes colony formation from protoplasts of an elite maize inbred. Plant Cell Rep. 1989, 8, 282–284. [Google Scholar] [CrossRef] [PubMed]
  20. Eberhard, S.; Doubrava, N.; Marfa, V.; Mohnen, D.; Southwick, A.; Darvill, A.; Albersheim, P. Pectic cell wall fragments regulate tobacco thin-cell-layer explant morphogenesis. Plant Cell 1989, 1, 747. [Google Scholar] [CrossRef] [PubMed]
  21. Malamy, J.; Carr, J.P.; Klessig, D.F.; Raskin, I. Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 1990, 250, 100–1004. [Google Scholar] [CrossRef] [PubMed]
  22. Métraux, J.P.; Signer, H.; Ryals, J.; Ward, E.; Wyss-Benz, M.; Gaudin, J.; Raschdorf, K.; Schmid, E.; Blum, W.; Inverardi, B. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 1990, 250, 1004–1006. [Google Scholar] [CrossRef] [PubMed]
  23. Pál, M.; Kovács, V.; Szalai, G.; Soós, V.; Ma, X.; Liu, H.; Mei, H.; Janda, T. Salicylic acid and abiotic stress responses in rice. J. Agron. Crop Sci. 2014, 200, 1–11. [Google Scholar] [CrossRef]
  24. Raskin, I.; Ehmann, A.; Melander, W.R.; Bastiaan, J.D.M. Salicylic acid: A natural inducer of heat production in Arum lilies. Science 1987, 237, 1601–1602. [Google Scholar] [CrossRef] [PubMed]
  25. Arnao, M.B.; Hernández-Ruiz, J. Melatonin in its relationship to plant hormones. Ann. Bot. 2018, 211, 195–207. [Google Scholar] [CrossRef] [PubMed]
  26. Verma, V.; Ravindran, P.; Kumar, P.P. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016, 16, 86. [Google Scholar] [CrossRef] [PubMed]
  27. Khan, M.I.; Fatma, M.; Per, T.S.; Anjum, N.A.; Khan, N.A. Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front. Plant Sci. 2015, 6, 462. [Google Scholar] [CrossRef] [PubMed]
  28. Pál, M.; Szalai, G.; Kovács, V.; Gondor, O.K.; Janda, T. Salicylic acid-mediated abiotic stress tolerance. In Salicylic Acid: Plant Growth and Development; Shamsul, H., Aqil, A., Alyemeni, M.N., Eds.; Springer: London, UK, 2013; pp. 183–247. ISBN 978-94-007-6427-9. [Google Scholar]
  29. Arnao Marino, B.; Hernández-Ruiz, J. Melatonin: Synthesis from tryptophan and its role in higher plants. In Amino Acids in Higher Plants; D’Mello, J.P.F., Ed.; CAB International: Boston, MA, USA, 2015; pp. 390–435. ISBN 978-1-78064-263-5. [Google Scholar]
  30. Wang, Y.; Reiter, R.J.; Chan, Z. Phytomelatonin: A universal abiotic stress regulator. J. Exp. Bot. 2018, 69, 963–974. [Google Scholar] [CrossRef] [PubMed]
  31. Bajwa, V.S.; Shukla, M.R.; Sherif, S.M.; Murch, S.J.; Saxena, P.K. Role of melatonin in alleviating cold stress in Arabidopsis thaliana. J. Pineal Res. 2014, 56, 238–245. [Google Scholar] [CrossRef] [PubMed]
  32. Shi, H.; Chan, Z. The Cysteine2/Histidine2-type transcription factor ZINC FINGER OF ARABIDOPSIS THALIANA 6-activated C-REPEAT-BINDING FACTOR pathway is essential for melatonin-mediated freezing stress resistance in Arabidopsis. J. Pineal Res. 2014, 57, 185–191. [Google Scholar] [CrossRef] [PubMed]
  33. Balabusta, M.; Szafranska, K.; Posmyk, M.M. Exogenous melatonin improves antioxidant defense in cucumber seeds germinated under chilling stress. Front. Plant Sci. 2016, 7, 575. [Google Scholar] [CrossRef]
  34. Zhao, Y.; Qi, L.W.; Wang, W.M.; Saxena, P.K.; Liu, C.Z. Melatonin improves the survival of cryopreserved callus of Rhodiola crenulata. J. Pineal Res. 2011, 50, 83–88. [Google Scholar] [CrossRef] [PubMed]
  35. Uchendu, E.E.; Shukla, M.R.; Reed, B.M.; Saxena, P.K. Melatonin enhances the recovery of cryopreserved shoot tips of American elm (Ulmus americana L.). J. Pineal Res. 2013, 55, 435–442. [Google Scholar] [PubMed]
  36. Li, H.; Dong, Y.; Chang, J.; He, J.; Chen, H.; Liu, Q.; Wei, C.; Ma, J.; Zhang, Y.; Yang, J.; et al. High-throughput microRNA and mRNA sequencing reveals that microRNAs may be involved in melatonin-mediated cold tolerance in Citrullus lanatus L. Front. Plant Sci. 2016, 7, 1231. [Google Scholar] [CrossRef] [PubMed]
  37. Turk, H.; Erdal, S.; Genisel, M.; Atici, O.; Demir, Y.; Yanmis, D. The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul. 2014, 74, 139–152. [Google Scholar] [CrossRef]
  38. Zhang, N.; Sun, Q.; Li, H.; Cao, Y.; Zhang, H.; Li, S.; Zhang, L.; Qi, Y.; Ren, S.; Zhao, B.; et al. Melatonin improved anthocyanin accumulation by regulating gene expressions and resulted in high reactive oxygen species scavenging capacity in cabbage. Front. Plant Sci. 2016, 7, 197. [Google Scholar] [CrossRef] [PubMed]
  39. Shi, H.; Jiang, C.; Ye, T.; Tan, D.; Reiter, R.J.; Zhang, H.; Liu, R.; Chan, Z. Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. J. Exp. Bot. 2015, 66, 681–694. [Google Scholar] [CrossRef] [PubMed]
  40. Fan, J.; Hu, Z.; Xie, Y.; Chan, Z.; Chen, K.; Amombo, E.; Chen, L.; Fu, J. Alleviation of cold damage to photosystem II and metabolisms by melatonin in Bermudagrass. Front. Plant Sci. 2015, 6, 925. [Google Scholar] [CrossRef] [PubMed]
  41. Shi, H.; Qian, Y.; Tan, D.X.; Reiter, R.J.; He, C. Melatonin induces the transcripts of CBF/DREB1s and their involvement in both abiotic and biotic stresses in Arabidopsis. J. Pineal Res. 2015, 59, 334–342. [Google Scholar] [CrossRef] [PubMed]
  42. Li, X.; Tan, D.X.; Jiang, D.; Liu, F. Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley. J. Pineal Res. 2016, 61, 328–339. [Google Scholar] [CrossRef] [PubMed]
  43. Tiryaki, I.; Keles, H. Reversal of the inhibitory effect of light and high temperature on germination of Phacelia tanacetifolia seeds by melatonin. J. Pineal Res. 2012, 52, 332–339. [Google Scholar] [CrossRef] [PubMed]
  44. Shi, H.; Tan, D.X.; Reiter, R.J.; Ye, T.; Yang, F.; Chan, Z. Melatonin induces class A1 heat shock factors (HSFA1s) and their possible involvement of thermotolerance in Arabidopsis. J. Pineal Res. 2015, 58, 335–342. [Google Scholar] [CrossRef] [PubMed]
  45. Xu, W.; Cai, S.Y.; Zhang, Y.; Wang, Y.; Ahammed, G.J.; Xia, X.J.; Shi, K.; Zhou, Y.H.; Yu, J.Q.; Reiter, R.J.; et al. Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. J. Pineal Res. 2016, 61, 457–469. [Google Scholar] [CrossRef] [PubMed]
  46. Tan, D.X.; Manchester, L.C.; Helton, P.; Reiter, R.J. Phytoremediative capacity of plants enriched with melatonin. Plant Signal. Behav. 2007, 2, 514–516. [Google Scholar] [CrossRef] [PubMed]
  47. Posmyk, M.M.; Kuran, H.; Marciniak, K.; Janas, K.M. Presowing seed treatment with melatonin protects red cabbage seedlings against toxic copper ion concentrations. J. Pineal Res. 2008, 45, 24–31. [Google Scholar] [CrossRef] [PubMed]
  48. Hasan, M.; Ahammed, G.J.; Yin, L.; Shi, K.; Xia, X.; Zhou, Y.; Yu, J.; Zhou, J. Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration and antioxidant potential in Solanum lycopersicum L. Front. Plant Sci. 2015, 6, 601. [Google Scholar] [CrossRef] [PubMed]
  49. Kobylinska, A.; Posmyk, M.M. Melatonin restricts Pb-induced PCD by enhancing BI-1 expression in tobacco suspension cells. Biometals 2016, 29, 1059–1074. [Google Scholar] [CrossRef] [PubMed]
  50. Wang, P.; Sun, X.; Wang, N.; Tan, D.X.; Ma, F. Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings. J. Pineal Res. 2015, 58, 479–489. [Google Scholar] [CrossRef] [PubMed]
  51. Szafranska, K.; Reiter, R.J.; Posmyk, M.M. Melatonin application to Pisum sativum L. seeds positively influences the function of the photosynthetic apparatus in growing seedlings during paraquat-induced oxidative stress. Front. Plant Sci. 2016, 7, 1663. [Google Scholar] [CrossRef] [PubMed]
  52. Li, C.; Wang, P.; Wei, Z.; Liang, D.; Jia, D.; Fu, M.; Ma, F. The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. J. Pineal Res. 2012, 53, 298–306. [Google Scholar] [CrossRef] [PubMed]
  53. Li, C.; Liang, B.; Chang, C.; Wei, Z.; Zhou, S.; Ma, F. Exogenous melatonin improved potassium content in Malus under different stress conditions. J. Pineal Res. 2016, 61, 218–229. [Google Scholar] [CrossRef] [PubMed]
  54. Kostopoulou, Z.; Therios, I.; Roumeliotis, E.; Kanellis, A.K.; Molassiotis, A. Melatonin combined with ascorbic acid provides salt adaptation in Citrus aurantium L. seedlings. Plant Physiol. Biochem. 2015, 86, 155–165. [Google Scholar] [CrossRef] [PubMed]
  55. Mukherjee, S.; David, A.; Yadav, S.; Baluska, F.; Bhatla, S.C. Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiol. Plant. 2014, 152, 714–728. [Google Scholar] [CrossRef] [PubMed]
  56. Zhang, H.J.; Zhang, N.; Yang, R.C.; Wang, L.; Sun, Q.Q.; Li, D.B.; Cao, Y.Y.; Weeda, S.; Zhao, B.; Ren, S.; et al. Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J. Pineal Res. 2014, 57, 269–279. [Google Scholar] [CrossRef] [PubMed]
  57. Dawood, M.G.; El-Awadi, M.E. Alleviation of salinity stress on Vicia faba L. plants via seed priming with melatonin. Acta Biol. Colomb. 2015, 20, 223–235. [Google Scholar] [CrossRef]
  58. Zhou, X.; Zhao, H.; Cao, K.; Hu, L.; Du, T.; Baluska, F.; Zou, Z. Beneficial roles of melatonin on redox regulation of photosynthetic electron transport and synthesis of D1 protein in tomato seedlings under salt stress. Front. Plant Sci. 2016, 7, 1823. [Google Scholar] [CrossRef] [PubMed]
  59. Liu, N.; Jin, Z.; Wang, S.; Gong, B.; Wen, D.; Wang, X.; Wei, M.; Shi, Q. Sodic alkaline stress mitigation with exogenous melatonin involves reactive oxygen metabolism and ion homeostasis in tomato. Sci. Hortic. 2015, 181, 18–25. [Google Scholar] [CrossRef]
  60. Wei, W.; Li, Q.; Chu, Y.-N.; Reiter, R.J.; Yu, X.M.; Zhu, D.H.; Zhang, W.K.; Ma, B.; Lin, Q.; Zhang, J.S.; et al. Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J. Exp. Bot. 2015, 66, 695–707. [Google Scholar] [CrossRef] [PubMed]
  61. Zhang, N.; Zhao, B.; Zhang, H.J.; Weeda, S.; Yang, C.; Yang, Z.C.; Ren, S.; Guo, Y.D. Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J. Pineal Res. 2013, 54, 15–23. [Google Scholar] [CrossRef] [PubMed]
  62. Meng, J.F.; Xu, T.F.; Wang, Z.Z.; Fang, Y.L.; Xi, Z.M.; Zhang, Z.W. The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: Antioxidant metabolites, leaf anatomy, and chloroplast morphology. J. Pineal Res. 2014, 57, 200–212. [Google Scholar] [CrossRef] [PubMed]
  63. Li, C.; Liang, D.; Chang, C.; Jia, D.; Ma, F. Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behavior in two Malus species under drought stress. J. Exp. Bot. 2015, 66, 669–680. [Google Scholar] [CrossRef] [PubMed]
  64. Arnao, M.B.; Hernández-Ruiz, J. Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves. J. Pineal Res. 2009, 46, 58–63. [Google Scholar] [CrossRef] [PubMed]
  65. 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. [Google Scholar] [CrossRef] [PubMed]
  66. Wang, P.; Sun, X.; Li, C.; Wei, Z.; Liang, D.; Ma, F. Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. J. Pineal Res. 2013, 54, 292–302. [Google Scholar] [CrossRef] [PubMed]
  67. Shi, H.; Reiter, R.J.; Tan, D.X.; Chan, Z. INDOLE-3-ACETIC ACID INDUCIBLE 17 positively modulates natural leaf senescence through melatonin-mediated pathway in Arabidopsis. J. Pineal Res. 2015, 58, 26–33. [Google Scholar] [CrossRef] [PubMed]
  68. Liang, C.; Zheng, G.; Li, W.; Wang, Y.; Hu, B.; Wang, H.; Wu, H.; Qian, Y.; Zhu, X.G.; Tan, D.X.; et al. Melatonin delays leaf senescence and enhances salt stress tolerance in rice. J. Pineal Res. 2015, 59, 91–101. [Google Scholar] [CrossRef] [PubMed]
  69. Zhang, J.; Li, H.; Xu, B.; Li, J.; Huang, B. Exogenous melatonin suppresses dark-induced leaf senescence by activating the superoxide dismutase-catalase antioxidant pathway and down-regulating chlorophyll degradation in excised leaves of perennial ryegrass (Lolium perenne L.). Front. Plant Sci. 2016, 7, 1500. [Google Scholar] [CrossRef] [PubMed]
  70. Mutlu, S.; Karadagoglu, O.; Atici, O.; Nalbantoglu, B. Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. Biol. Plant. 2013, 57, 507–513. [Google Scholar] [CrossRef]
  71. Kang, G.Z.; Wang, Z.X.; Xia, K.F.; Sun, G.C. Protection of ultrastructure in chilling-stressed banana leaves by salicylic acid. J. Zhejiang Univ. Sci. B 2007, 8, 277–282. [Google Scholar] [CrossRef] [PubMed]
  72. Ding, C.K.; Wang, C.; Gross, K.C.; Smith, D.L. Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 2002, 214, 895–901. [Google Scholar] [CrossRef] [PubMed]
  73. Wang, L.; Chen, S.; Kong, W.; Li, S.; Archbold, D.D. Salicylic acid pretreatment alleviates chilling injury and affects the antioxidant system and heat shock proteins of peaches during cold storage. Postharvest Biol. Technol. 2006, 41, 244–251. [Google Scholar] [CrossRef]
  74. Khan, M.I.; Iqbal, N.; Masood, A.; Per, T.S.; Khan, N.A. Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal. Behav. 2013, 8, e26374. [Google Scholar] [CrossRef] [PubMed]
  75. Larkindale, J.; Knight, M.R. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 2002, 128, 682–695. [Google Scholar] [CrossRef] [PubMed]
  76. Ahmad, P.; Nabi, G.; Ashraf, M. Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. S. Afr. J. Bot. 2011, 77, 36–44. [Google Scholar]
  77. Zhang, Y.; Xu, S.; Yang, S.; Chen, Y. Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 2015, 252, 911–924. [Google Scholar] [CrossRef] [PubMed]
  78. Noriega, G.; Caggiano, E.; Lecube, M.L.; Cruz, D.S.; Batlle, A.; Tomaro, M.; Balestrasse, K.B. The role of salicylic acid in the prevention of oxidative stress elicited by cadmium in soybean plants. Biometals 2012, 25, 1155–1165. [Google Scholar] [CrossRef] [PubMed]
  79. Liu, C.; Guo, J.; Cui, Y.; Láo, T.; Zhang, X.; Shi, G. Effects of cadmium and salicylic acid on growth, spectral reflectance and photosynthesis of castor bean seedlings. Plant Soil 2011, 344, 131–141. [Google Scholar] [CrossRef]
  80. Ardebili, N.O.; Saadatmand, S.; Niknam, V.; Khavari-Nejad, R.A. The alleviating effects of selenium and salicylic acid in salinity exposed soybean. Acta Physiol. Plant. 2014, 36, 3199–3205. [Google Scholar] [CrossRef]
  81. Khan, M.I.; Asgher, M.; Khan, N.A. Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol. Biochem. 2014, 80, 67–74. [Google Scholar] [CrossRef] [PubMed]
  82. Li, T.; Hu, Y.; Du, X.; Tang, H.; Shen, C.; Wu, J. Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. PLoS ONE 2014, 9, e109492. [Google Scholar] [CrossRef] [PubMed]
  83. Saruhan, N.; Saglam, A.; Kadioglu, A. Salicylic acid pretreatment induces drought tolerance and delays leaf rolling by inducing antioxidant systems in maize genotypes. Acta Physiol. Plant. 2012, 34, 97–106. [Google Scholar] [CrossRef]
  84. Awate, P.D.; Gaikwad, D.K. Influence of growth regulators on secondary metabolites of medicinally important oil yielding plant Simarouba glauca DC. under water stress conditions. J. Stress Physiol. Biochem. 2014, 10, 222–229. [Google Scholar]
  85. Singh, B.; Usha, K. Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul. 2003, 39, 137–141. [Google Scholar] [CrossRef]
  86. Ervin, E.H.; Zhang, X.Z.; Fike, J.H. Ultraviolet-B radiation damage on Kentucky Bluegrass II: Hormone supplement effects. Hortic. Sci. 2004, 39, 1471–1474. [Google Scholar]
  87. Yin, L.; Wang, P.; Li, M.; Ke, X.; Li, C.; Liang, D.; Wu, S.; Ma, X.; Li, C.; Zou, Y.; et al. Exogenous melatonin improves Malus resistance to Marssonina apple blotch. J. Pineal Res. 2013, 54, 426–434. [Google Scholar] [CrossRef] [PubMed]
  88. Zhang, S.; Zheng, X.; Reiter, R.J.; Feng, S.; Wang, Y.; Liu, S.; Jin, L.; Li, Z.; Datla, R.; Ren, M. Melatonin attenuates potato late blight by disrupting cell growth, stress tolerance, fungicide susceptibility and homeostasis of gene expression in Phytophthora infestans. Front. Plant Sci. 2017, 8, 1993. [Google Scholar] [CrossRef] [PubMed]
  89. Lee, H.Y.; Byeon, Y.; Tan, D.X.; Reiter, R.J.; Back, K. Arabidopsis serotonin N-acetyltransferase knockout mutant plants exhibit decreased melatonin and salicylic acid levels resulting in susceptibility to an avirulent pathogen. J. Pineal Res. 2015, 58, 291–299. [Google Scholar] [CrossRef] [PubMed]
  90. Vielma, J.R.; Bonilla, E.; Chacín-Bonilla, L.; Mora, M.; Medina-Leendertz, S.; Bravo, Y. Effects of melatonin on oxidative stress, and resistance to bacterial, parasitic, and viral infections: A review. Acta Trop. 2014, 137, 31–38. [Google Scholar] [CrossRef] [PubMed]
  91. Lee, H.Y.; Byeon, Y.; Back, K. Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco. J. Pineal Res. 2014, 57, 262–268. [Google Scholar] [CrossRef] [PubMed]
  92. Shi, H.; Chen, Y.; Tan, D.X.; Reiter, R.J.; Chan, Z.; He, C. Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis. J. Pineal Res. 2015, 59, 102–108. [Google Scholar] [CrossRef] [PubMed]
  93. Lee, H.Y.; Back, K. Mitogen-activated protein kinase pathways are required for melatonin-mediated defense responses in plants. J. Pineal Res. 2016, 60, 327–335. [Google Scholar] [CrossRef] [PubMed]
  94. Shi, H.; Wei, Y.; He, C. Melatonin-induced CBF/DREB1s are essential for diurnal change of disease resistance and CCA1 expression in Arabidopsis. Plant. Physiol. Biochem. 2016, 100, 150–155. [Google Scholar] [CrossRef] [PubMed]
  95. Wei, Y.; Zeng, H.; Hu, W.; Chen, L.; He, C.; Shi, H. Comparative transcriptional profiling of melatonin synthesis and catabolic genes indicates the possible role of melatonin in developmental and stress responses in rice. Front. Plant Sci. 2016, 7, 676. [Google Scholar] [CrossRef] [PubMed]
  96. Wei, Y.; Chang, Y.; Zeng, H.; Liu, G.; He, C.; Shi, H. RAV transcription factors are essential for disease resistance against cassava bacterial blight via activation of melatonin biosynthesis genes. J. Pineal Res. 2018, 64, e12454. [Google Scholar] [CrossRef] [PubMed]
  97. Wang, Y.Y.; Li, B.Q.; Qin, G.Z.; Li, L.; Tian, S.P. Defense response of tomato fruit at different maturity stages to salicylic acid and ethephon. Sci. Hortic. 2011, 129, 183–188. [Google Scholar] [CrossRef]
  98. Chivasa, S.; Murphy, A.M.; Naylor, M.; Carr, J.P. Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 1997, 9, 547–557. [Google Scholar] [CrossRef] [PubMed]
  99. Murphy, A.M.; Carr, J.P. Salicylic acid has cell-specific effects on tobacco mosaic virus replication and cell-to-cell movement. Plant Physiol. 2002, 128, 552–563. [Google Scholar] [CrossRef] [PubMed]
  100. Tian, M.; Sasvari, Z.; Gonzalez, P.A.; Friso, G.; Rowland, E.; Liu, X.M.; van Wijk, K.J.; Nagy, P.D.; Klessig, D.F. Salicylic acid inhibits the replication of tomato bushy stunt virus by directly targeting a host component in the replication complex. Mol. Plant Microbe Interact. 2015, 28, 379–386. [Google Scholar] [CrossRef] [PubMed]
  101. Babalar, M.; Asghari, M.; Talaei, A.; Khosroshahi, A. Effect of pre- and postharvest salicylic acid treatment on ethylene production, fungal decay and overall quality of Selva strawberry fruit. Food Chem. 2007, 105, 449–453. [Google Scholar] [CrossRef]
  102. Joyce, D.C.; Wearing, H.; Coates, L.; Terry, L. Effects of phosphonate and salicylic acid treatments on anthracnose disease development and ripening of ‘Kensington Pride’ mango fruit. Aust. J. Exp. Agric. 2001, 41, 805–813. [Google Scholar]
  103. Yu, T.; Zheng, X.D. Salicylic acid enhances biocontrol efficacy of the antagonist Cryptococcus laurentii in apple fruit. J. Plant Growth Regul. 2006, 25, 166–174. [Google Scholar] [CrossRef]
  104. Xu, X.; Tian, S. Salicylic acid alleviated pathogen-induced oxidative stress in harvested sweet cherry fruit. Postharvest Biol. Technol. 2008, 49, 379–385. [Google Scholar] [CrossRef]
  105. Cao, J.; Zeng, K.; Jiang, W. Enhancement of postharvest disease resistance in Ya Li pear (Pyrus bretschneideri) fruit by salicylic acid sprays on the trees during fruit growth. Eur. J. Plant Pathol. 2006, 114, 363–370. [Google Scholar] [CrossRef]
  106. Astier, J.; Loake, G.; Velikova, V.; Gaupels, F. Editorial: Interplay between NO signaling, ROS, and the antioxidant system in plants. Front. Plant Sci. 2016, 7, 1731. [Google Scholar] [CrossRef] [PubMed]
  107. León, J.; Costa, A.; Castillo, M.C. Nitric oxide triggers a transient metabolic reprogramming in Arabidopsis. Sci. Rep. 2016, 6, 37945. [Google Scholar] [CrossRef] [PubMed]
  108. Pucciariello, C.; Perata, P. New insights into reactive oxygen species and nitric oxide signalling under low oxygen in plants. Plant Cell Environ. 2017, 40, 473–482. [Google Scholar] [CrossRef] [PubMed]
  109. Del Rio, L.A.; López-Huertas, E. ROS generation in peroxisomes and its role in cell signaling. Plant Cell Environ. 2016, 57, 1364–1376. [Google Scholar] [CrossRef] [PubMed]
  110. Saxena, I.; Srikanth, S.; Chen, Z. Cross talk between H2O2 and interacting signal molecules under plant stress response. Front. Plant Sci. 2016, 7, 570. [Google Scholar] [CrossRef] [PubMed]
  111. Damiani, I.; Pauly, N.; Puppo, A.; Brouquisse, R.; Boscari, A. Reactive oxygen species and nitric oxide control early steps of the legume-Rhizobium symbiotic interaction. Front. Plant Sci. 2016, 7, 454. [Google Scholar] [CrossRef] [PubMed]
  112. Molassiotis, A.; Job, D.; Ziogas, V.; Tanou, G. Citrus Plants: A model system for unlocking the secrets of NO and ROS-inspired priming against salinity and drought. Front. Plant Sci. 2016, 7, 229. [Google Scholar] [CrossRef] [PubMed]
  113. Wen, D.; Gong, B.; Sun, S.; Liu, S.; Wang, X.; Wei, M.; Yang, F.; Li, Y.; Shi, Q. Promoting roles of melatonin in adventitious root development of Solanum lycopersicum L. by regulating auxin and nitric oxide signaling. Front. Plant Sci. 2016, 7, 718. [Google Scholar] [CrossRef] [PubMed]
  114. Sun, H.; Feng, F.; Liu, J.; Zhao, Q. The Interaction between auxin and nitric oxide regulates root growth in response to iron deficiency in rice. Front. Plant Sci. 2017, 8, 2169. [Google Scholar] [CrossRef] [PubMed]
  115. Fleta-Soriano, E.; Díaz, L.; Bonet, E.; Munné-Bosch, S. Melatonin may exert a protective role against drought stress in maize. J. Agron. Crop Sci. 2017, 203, 286–294. [Google Scholar] [CrossRef]
  116. Lee, H.Y.; Back, K. Melatonin is required for H2O2- and NO-mediated defense signaling through MAPKKK3 and OXI1 in Arabidopsis thaliana. J. Pineal Res. 2017, 62, e12379. [Google Scholar] [CrossRef] [PubMed]
  117. Shyu, C.; Brutnell, T.P. Growth-defence balance in grass biomass production: The role of jasmonates. J. Exp. Bot. 2015, 66, 4165–4176. [Google Scholar] [CrossRef] [PubMed]
  118. Qian, Y.; Tan, D.X.; Reiter, R.J.; Shi, H. Comparative metabolomic analysis highlights the involvement of sugars and glycerol in melatonin-mediated innate immunity against bacterial pathogen in Arabidopsis. Sci. Rep. 2015, 5, 15815. [Google Scholar] [CrossRef] [PubMed]
  119. Overmyer, K.; Vuorinen, K.; Brosché, M. Interaction points in plant stress signaling pathways. Physiol. Plant 2018, 162, 191–204. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Biosynthetic routes of salicylic acid and melatonin in plants.
Figure 1. Biosynthetic routes of salicylic acid and melatonin in plants.
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Figure 2. Effect of abiotic/biotic stressors on the antioxidant network ROS/NO/melatonin.
Figure 2. Effect of abiotic/biotic stressors on the antioxidant network ROS/NO/melatonin.
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Figure 3. Model of ROS/NO/melatonin action on biotic stress responses (pathogen resistance).
Figure 3. Model of ROS/NO/melatonin action on biotic stress responses (pathogen resistance).
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Figure 4. Melatonin/SA model of biostimulating activity in plants to enhance resistance to stress situations and increase crop yield.
Figure 4. Melatonin/SA model of biostimulating activity in plants to enhance resistance to stress situations and increase crop yield.
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Table 1. Common physiological effects described for melatonin and SA in plants.
Table 1. Common physiological effects described for melatonin and SA in plants.
Physiological Effect
Vegetative development
Seed germination
Plant growth
Photosynthesis
Mineral nutrition
Crop yield
Carbohydrate metabolism
Nitrate metabolism
Antioxidant network
Senescence
Plant pathogen response
Reproductive development
Flowering
Seed formation
Abiotic stresss
Water stress: drought, flooding Agronomy 08 00033 i001
Salinity
Metals
UV, extreme light
Temperature stress: cold, heat
Biotic stressors
Fungi
Bacteria
Table 2. Effects of melatonin in abiotic stress responses.
Table 2. Effects of melatonin in abiotic stress responses.
Abiotic StressPlant SpeciesMelatonin Treatment (µM) Effects ObservedReference
ColdArabidopsis10–30↑ fresh weight, shoot height and primary roots, survival[31,32]
ColdCucumber50–500↑ GSH pool, ↓ ROS burst[33]
ColdRhodiola crenulata0.1↑ cryopreservation of callus[34]
ColdAmerican elm0.1–0.5↑ regrowth frozen shoots[35]
ColdWatermelon150↑ photosynthesis, ↓ cold-related microRNA[36]
ColdWheat1 mM↑ redox balance, Chls, osmorregulation, ↓ ROS burst[37]
ColdCabbage10–1000↑ anthocyanins, proline, redox balance, ↓ ROS burst[38]
Cold, salt, droughtBermudagrass20–100↑ fresh weight, osmorregulation, ↓ ROS burst, cell damage[39,40]
Cold, salt, droughtArabidopsis50↑ sucrose, survival rate[41]
Cold, droughtBarley1 mM↑ photosynthesis efficiency, ABA, water content, ↓ ROS burst[42]
HeatPhacelia0.3–90↑ germination[43]
HeatArabidopsis5–20↑ thermotolerance[44]
HeatTomato10↑ thermotolerance and cell protection[45]
Metal-CuPea5↑ plant survival[46]
Metal-CuRed cabbage1–100↑ fresh weight, germination, ↓ membrane peroxidation[47]
Metal-CdTomato25–500↑ Cd tolerance, phytochelatins, ATPase activity[48]
Metal-PbTobacco0.2↑ cell culture growth, ↓ mortality cells, ROS burst[49]
OxidativeArabidopsis5–10↑ plant survival, autophagy, ↓ oxidized proteins[50]
OxidativePisum sativum50–200↑ photosynthesis efficiency, pigments, water content, ↓ ROS burst[51]
SalinityMalus0.1↑ shoot height, leaf number, chlorophylls, ↓ electrolyte leakage[52]
SalinityMalus0.1↑ shoot height, K+ channels, K+ level, ↓ ROS burst[53]
SalinityCitrus1↑ osmorregulation, Chls, ↓ ROS burst, membrane peroxidation[54]
SalinitySunflower15↑ root and hypocotyl growth, antioxidant potential[55]
SalinityCucumber1↑ germination, GA4, ↓ ROS burst, membrane peroxidation, ABA[56]
SalinityVicia faba100–500↑ plant height, RWC, photosynthetic pigments, osmolites, phenolic[57]
SalinityTomato50–150↑ photosynthesis, PSII efficiency, D1 protein turnover, ↓ ROS burst [58]
AlkalinityTomato0.25–1↑ seedling growth, photosynthesis, ion homeostasis, ↓ ROS burst[59]
Salinity, droughtSoybean50–100↑ seedling growth, leaf size, biomass, seed yield[60]
DroughtCucumber100↑ germination, root growth[61]
DroughtGrape0.05–0.2↑ seedling growth, osmorregulation, photosynthesis, ↓ ROS burst[62]
DroughtMalus100↑ water status, Chls, photosynthesis efficiency, ↓ ROS burst [63]
Leaf-senescenceBarley0.01–1↓ senescence, ↑ Chls[64]
Leaf-senescenceMalus10 mM↓ senescence, ROS burst, ↑ Chls, photosynthesis efficiency[65,66]
Leaf-senescenceArabidopsis20–125↓ senescence, ROS burst, ↑ Chls, photosynthesis efficiency[67]
Leaf-senescenceRice10–20↓ senescence, ROS burst, cell death, ↑ Chls[68]
Leaf-senescencePerennial ryegrass20–100↓ senescence, ROS burst, ↑ Chls, photosynthesis efficiency[69]
↑, Increased content or increased action. ↓ Decreased content or decreased action.
Table 3. Effects of SA in abiotic stress responses.
Table 3. Effects of SA in abiotic stress responses.
Abiotic StressPlant SpeciesSA Treatment (µM) Effects ObservedReference
ColdHordeum vulgare100↑ antioxidative enzymes, ice nucleation activity[70]
ColdMusa acuminata500↑ chloroplast and mitochondria ultrastructure[71]
ColdLycopersicon esculentum100↑ resistance, antioxidative enzymes, PR proteins[72]
ColdPrunus persica1 mM↑ antioxidative enzymes, antioxidant metabolites, firmness[73]
HeatTriticum aestivum500↑ proline content, water potential, gas exchange, glutamyl kinase activity [74]
HeatArabidopsis thaliana10↑ survival, thermotolerance, ↓ oxidative damage[75]
Metal-CdBrassica juncea1 mM↑ mineral nutrients[76]
Metal-CdCucumis melo100↑ photosynthesis efficiency, water use efficiency[77]
Metal-CdGlycine max120 mM↑ Chls, photosynthesis efficiency, antioxidative enzymes, GSH[78]
Metal-CdRicinus communis500↓ gas exchange, Chls [79]
SalinityGlycine max500↑ antioxidative enzymes, ascorbate[80]
SalinityVigna radiata500↑ photosynthesis efficiency, plant dry mass, glycinebetaine[81]
SalinityTorreya grandis500↑ photosynthesis efficiency, net CO2 assimilation rates, Chls[82]
DroughtZea mays1↑ net dry weight, water potential, leaf rolling[83]
DroughtSimarouba glauca50↑ polyphenols, alkaloids[84]
DroughtTriticum aestivum1 mM↑ moisture content, dry mass, Rubisco, SOD, Chls[85]
UV-BPoa pratensis150 mg/m2α-tocopherol, SOD, CAT, anthocyanins[86]
↑, Increased content or increased action. ↓, Decreased content or decreased action.
Table 4. Effects of melatonin in biotic stress responses.
Table 4. Effects of melatonin in biotic stress responses.
Plant SpeciesBiotic StressorMelatonin Treatment (µM)Effects ObservedReference
Malus prunifoliaDiplocarpon mali50–500↑ Resistance to fungal infection
↓ Leaf lesions, cell death
↓ Pathogen expansion
[87]
Arabidopsis and tobaccoPseudomonas syringae DC300010↑ Defence related genes
↑ Resistance (10-fold vs. mock)
[91]
ArabidopsisPseudomonas syringae DC3000SE of SNAT↓ Melatonin (50%), SA
↓ Defence related genes
↓ Resistance to infection
[89]
ArabidopsisPseudomonas syringae DC300020↑ NO and melatonin
↑ Defence related genes
↑ Resistance
[92]
Arabidopsis and tobaccoPseudomonas syringae DC30001↑ MAP kinases cascade[93]
ArabidopsisPseudomonas syringae DC300050↑ CBF/DREB1 (stress factors)
↑ CCA1 (internal clock factors)
↑ Defence related genes
[41,94]
Lupinus albusPenicillium spp.20–70↑ Resistance to fungal infection[17]
RiceXanthomonas oryzae, XooMagnaporthe oryzae, blast fungus--Changes in melatonin biosynthesis enzymes transcripts[95]
Solanum tuberosumPhytophthora infestans10 mM↑ Resistance to fungal infection
↑ fungicide effects, ↓ virulence
[88]
Manihot esculentaXanthomonas axonopodis MeRAV1/2 (AP2/ERF) upregulate 7 melatonin biosynthesis genes[96]
↑, Increased content or increased action. ↓, Decreased content or decreased action.
Table 5. Effects of SA in biotic stress responses.
Table 5. Effects of SA in biotic stress responses.
Plant SpeciesBiotic StressorSA Treatment (mM)Effects ObservedReference
Fragaria ananassaBotrytis cinerea1–2↓ ethylene, fungal disease, ↑ fruit quality[101]
Lycopersicon esculentumBotrytis cinerea5↓ ethylene, lycopene, fungal disease, ↑ fruit quality[97]
Mangifera indicaCollectotrichum gloeosporioides2↑ colour, firmness, ↓ disease severity[102]
Malus domesticaPenicillium expansum0.07–0.7↑ efficacy of antagonist C. laurentii[103]
Prunus aviumPenicillium expansum2↑ antioxidative enzymes, chitinase, glucanase, fungal resistance[104]
PyrusbretschneideriPenicillium expansum2.5↑ antioxidative enzymes, PAL, chitinase, glucanase, ↓ disease severity[105]
↑, Increased content or increased action. ↓, Decreased content or decreased action.

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MDPI and ACS Style

Hernández-Ruiz, J.; Arnao, M.B. Relationship of Melatonin and Salicylic Acid in Biotic/Abiotic Plant Stress Responses. Agronomy 2018, 8, 33. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy8040033

AMA Style

Hernández-Ruiz J, Arnao MB. Relationship of Melatonin and Salicylic Acid in Biotic/Abiotic Plant Stress Responses. Agronomy. 2018; 8(4):33. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy8040033

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Hernández-Ruiz, Josefa, and Marino B. Arnao. 2018. "Relationship of Melatonin and Salicylic Acid in Biotic/Abiotic Plant Stress Responses" Agronomy 8, no. 4: 33. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy8040033

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