Abstract
Melatonin is an evolutionarily conserved multifunctional molecule that is widely found in different parts of plants. In addition to its role in regulating plant growth and development, melatonin plays an important role in improving plant biotic and abiotic stress tolerance, which is an important molecule for protecting plants from abiotic and biotic stresses. The role of melatonin in plant growth and development is manifested in the regulation of seed germination, root development, fruit maturation, and senescence. Melatonin primarily improves plant stress resistance by improving plant antioxidant efficiency, reducing the inhibition of photosynthesis, and changing the expression of stress resistance-related genes. This paper reviews the regulation of melatonin on plant growth and development and the molecular mechanisms by which melatonin improves plant tolerance to abiotic and biogenic stresses and analyzes the relationship between melatonin and other signaling molecules and signaling pathways. The future research direction of plant melatonin is prospected.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aghdam M, Fard J (2017) Melatonin treatment attenuates postharvest decay and maintains nutritional quality of strawberry fruits (Fragaria×anannasa cv. Selva) by enhancing GABA shunt activity. Food Chem 221:1650–1657. https://doi.org/10.1016/j.foodchem.2016.10.123
Ahammed GJ, Xu W, Liu A, Chen S (2018) COMT1 silencing aggravates heat stress-induced reduction in photosynthesis by decreasing chlorophyll content, photosystem II activity, and electron transport efficiency in tomato. Front Plant Sci 9:998. https://doi.org/10.3389/fpls.2018.00998
Ahmad S, Su W, Kamran M, Ahmad I, Meng X, Wu X, Javed T, Han Q (2020) Foliar application of melatonin delay leaf senescence in maize by improving the antioxidant defense system and enhancing photosynthetic capacity under semi-arid regions. Protoplasma 257:1079–1092. https://doi.org/10.1007/s00709-020-01491-3
Alam MN, Wang Y, Chan Z (2018a) Physiological and biochemical analyses reveal drought tolerance in cool-season tall fescue (Festuca arundinacea) turf grass with the application of melatonin. Crop Pasture Sci 69(10):1041–1049. https://doi.org/10.1071/CP18394
Alam MN, Zhang L, Yang L, Islam MR, Liu Y, Luo H, Yang P, Wang Q, Chan Z (2018b) Transcriptomic profiling of tall fescue in response to heat stress and improved thermotolerance by melatonin and 24-epibrassinolide. BMC Genomics 19:224. https://doi.org/10.1186/s12864-018-4588-y
Arnao MB, Hernández-Ruiz J (2009) Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves. J Pineal Res 46:58–63. https://doi.org/10.1111/j.1600-079X.2008.00625.x
Arnao MB, Hernández-Ruiz J (2015) Functions of melatonin in plants: a review. J Pineal Res 59:133–150. https://doi.org/10.1111/jpi.12253
Arnao MB, Hernández-Ruiz J (2018) Melatonin and its relationship to plant hormones. Ann Bot 121:195–207. https://doi.org/10.1093/aob/mcx114
Arnao MB, Hernández-Ruiz J (2019a) Melatonin: a new plant hormone and/or a plant master regulator? Trends Plant Sci 24:38–48. https://doi.org/10.1016/j.tplants.2018.10.010
Arnao MB, Hernández-Ruiz J (2019b) Melatonin and reactive oxygen and nitrogen species: a model for the plant redox network. Melatonin Res 2:152–168
Arnao MB, Hernández-Ruiz J (2019c) Role of melatonin to enhance phytoremediation capacity. Appl Sci 9:5293. https://doi.org/10.3390/app9245293
Arora D, Bhatla SC (2017) Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/Zn SOD and Mn SOD. Free Radic Bio Med 106:315–328. https://doi.org/10.1016/j.freeradbiomed.2017.02.042
Back K (2020) Melatonin metabolism, signaling and possible roles in plants. Plant J. https://doi.org/10.1111/tpj.14915
Back K, Tan DX, Reiter RJ (2016) Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J Pineal Res 61:426–437. https://doi.org/10.1111/jpi.12364
Bajwa V, Shukla M, Sherif S, Murch S, Saxena P (2014) Role of melatonin in alleviating cold stress in Arabidopsis thaliana. J Pineal Res 56:238–245. https://doi.org/10.1111/jpi.12115
Byeon Y, Back K (2014) An increase in melatonin in transgenic rice causes pleiotropic phenotypes, including enhanced seedling growth, delayed flowering, and low grain yield. J Pineal Res 56:408–414. https://doi.org/10.1111/jpi.12129
Byeon Y, Back K (2016) Low melatonin production by suppression of either serotonin N-acetyltransferase or N-acetylserotonin methyltransferase in rice causes seedling growth retardation with yield penalty, abiotic stress susceptibility, and enhanced coleoptile growth under anoxic conditions. J Pineal Res 60:348–359. https://doi.org/10.1111/jpi.12317
Byeon Y, Lee HY, Hwang OJ, Lee HJ, Lee K, Back K (2015) Coordinated regulation of melatonin synthesis and degradation genes in rice leaves in response to cadmium treatment. J Pineal Res 58:470–478. https://doi.org/10.1111/jpi.12232
Byeon Y, Lee HY, Back K (2016) Cloning and characterization of the serotonin N-acetyltransferase-2 gene (SNAT2) in rice (Oryza sativa). J Pineal Res 61:198–207. https://doi.org/10.1111/jpi.12339
Cai SY, Zhang Y, Xu YP et al (2017) HsfA1a upregulates melatonin biosynthesis to confer cadmium tolerance in tomato plants. J Pineal Res. https://doi.org/10.1111/jpi.12387
Cao S, Shao J, Shi L, Xu L, Shen Z, Chen W, Yang Z (2018) Melatonin increases chilling tolerance in postharvest peach fruit by alleviating oxidative damage. Sci Rep 8:806. https://doi.org/10.1038/s41598-018-19363-5
Cao Y, Qi C, Li S, Wang Z, Wang X, Wang J, Ren S, Li X, Zhang N, Guo Y (2019) Melatonin alleviates copper toxicity via improving copper sequestration and ROS scavenging in cucumber. Plant Cell Physiol 60:562–574. https://doi.org/10.1093/pcp/pcy226
Chen G, Huo Y, Tan DX, Liang Z, Zhang W, Zhang Y (2003) Melatonin in Chinese medicinal herbs. Life Sci 73:19–26. https://doi.org/10.1016/s0024-3205(03)00252-2
Chen Q, Qi WB, Reiter RJ, Wei W, Wang BM (2009) Exogenously applied melatonin stimulates root growth and raises endogenous indoleacetic acid in roots of etiolated seedlings of Brassica juncea. J Plant Physiol 166:324–328. https://doi.org/10.1016/j.jplph.2008.06.002
Chen L, Fan J, Hu Z, Huang X, Amombo E, Liu A, Bi A, Chen K, Xie Y, Fu J (2017a) Melatonin is involved in regulation of bermudagrass growth and development and response to low K+ stress. Front Plant Sci 8:2038. https://doi.org/10.3389/fpls.2017.02038
Chen Z, Xie Y, Gu Q, Zhao G, Zhang Y, Cui W, Xu S, Wang R, Shen W (2017b) The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radical Bio Med 108:465–477. https://doi.org/10.1016/j.freeradbiomed.2017.04.009
Chen YE, Mao JJ, Sun LQ, Huang B, Ding CB, Gu Y, Liao JQ, Hu C, Zhang ZW, Yuan S, Yuan M (2018a) Exogenous melatonin enhances salt stress tolerance in maize seedlings by improving antioxidant and photosynthetic capacity. Physiol Plantarum 164:349–363. https://doi.org/10.1111/ppl.12737
Chen Z, Gu Q, Yu X, Huang L, Xu S, Wang R, Shen W, Shen W (2018b) Hydrogen peroxide acts downstream of melatonin to induce lateral root formation. Ann Bot 121:1127–1136. https://doi.org/10.1093/aob/mcx207
Chen J, Li H, Yang K, Wang Y, Yang L, Hu L, Liu R, Shi Z (2019) Melatonin facilitates lateral root development by coordinating PAO-derived hydrogen peroxide and Rboh-derived superoxide radical. Free Radical Bio Med 143:534–544. https://doi.org/10.1016/j.freeradbiomed.2019.09.011
Cui G, Sun F, Gao X, Xie K, Zhang C, Liu S, Xi Y (2018) Proteomic analysis of melatonin-mediated osmotic tolerance by improving energy metabolism and autophagy in wheat (Triticum aestivum L.). Planta 248:69–87. https://doi.org/10.1007/s00425-018-2881-2
Debnath B, Islam W, Li M, Sun Y, Lu X, Mitra S, Hussain M, Liu S, Qiu D (2019) Melatonin mediates enhancement of stress tolerance in plants. Int J Mol Sci. https://doi.org/10.3390/ijms20051040
Ding F, Wang M, Liu B, Zhang S (2017) Exogenous melatonin mitigates photoinhibition by accelerating non-photochemical quenching in tomato seedlings exposed to moderate light during chilling. Front Plant Sci 8:244. https://doi.org/10.3389/fpls.2017.00244
Ding F, Wang G, Wang M, Zhang S (2018) Exogenous melatonin improves tolerance to water deficit by promoting cuticle formation in tomato plants. Molecules. https://doi.org/10.3390/ijms20051040
Dubbels R, Reiter R, Klenke E, Goebel A, Schnakenberg E, Ehlers C, Schiwara H, Schloot W (1995) Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry. J Pineal Res 18:28–31. https://doi.org/10.1111/j.1600-079x.1995.tb00136.x
Erdal S (2019) Melatonin promotes plant growth by maintaining integration and coordination between carbon and nitrogen metabolisms. Plant Cell Rep 38:1001–1012. https://doi.org/10.1007/s00299-019-02423-z
Fan J, Xie Y, Zhang Z, Chen L (2018) Melatonin: a multifunctional factor in plants. Int J Mol Sci. https://doi.org/10.3390/ijms19051528
Galano A, Tan D, Reiter R (2013) On the free radical scavenging activities of melatonin’s metabolites, Afmk and Amk. J Pineal Res 54:245–257. https://doi.org/10.1111/jpi.12010
Gao H, Zhang Z, Chai H, Cheng N, Yang Y, Wang D, Yang T, Cao W (2016) Melatonin treatment delays postharvest senescence and regulates reactive oxygen species metabolism in peach fruit. Postharvest Biol Tec 118:103–110. https://doi.org/10.1016/j.postharvbio.2016.03.006
Gao W, Zhang Y, Feng Z, Bai Q, He J, Wang Y (2018) Effects of melatonin on antioxidant capacity in naked oat seedlings under drought stress. Molecules. https://doi.org/10.3390/molecules23071580
Gao W, Feng Z, Bai Q, He J, Wang Y (2019) Melatonin-mediated regulation of growth and antioxidant capacity in salt-tolerant naked oat under salt stress. Int J Mol Sci. https://doi.org/10.3390/ijms20051176
Gong X, Shi S, Dou F, Song Y, Ma F (2017) Exogenous melatonin alleviates alkaline stress in Malus hupehensis Rehd. by regulating the biosynthesis of polyamines. Molecules. https://doi.org/10.3390/molecules22091542
Hasan MK, Ahammed GJ, Yin L, Shi K, Xia X, Zhou Y, Yu J, Zhou J (2015) Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Front Plant Sci 6:601. https://doi.org/10.3389/fpls.2015.00601
Hernández-Ruiz J, Arnao M (2018) Relationship of melatonin and salicylic acid in biotic/abiotic plant stress responses. Agronomy 8:33. https://doi.org/10.3390/agronomy8040033
Huang YH, Liu SJ, Yuan S, Guan C, Tian DY, Cui X, Zhang YW, Yang FY (2017) Overexpression of ovine AANAT and HIOMT genes in switchgrass leads to improved growth performance and salt-tolerance. Sci Rep-uk. https://doi.org/10.1038/s41598-017-12566-2
Huang B, Chen YE, Zhao YQ, Ding CB, Liao JQ, Hu C, Zhou LJ, Zhang ZW, Yuan S, Yuan M (2019) Exogenous melatonin alleviates oxidative damages and protects photosystem II in maize seedlings under drought stress. Front Plant Sci 10:677. https://doi.org/10.3389/fpls.2019.00677
Hwang OJ, Back K (2018) Melatonin is involved in skotomorphogenesis by regulating brassinosteroid biosynthesis in rice plants. J Pineal Res 65:e12495. https://doi.org/10.1111/jpi.12495
Jahan MS, Shu S, Wang Y, Chen Z, He M, Tao M, Sun J, Guo S (2019) Melatonin alleviates heat-induced damage of tomato seedlings by balancing redox homeostasis and modulating polyamine and nitric oxide biosynthesis. BMC Plant Biol 19:414. https://doi.org/10.1186/s12870-019-1992-7
Janice L, Tebello N, Santy D (1998) The interaction of melatonin and its precursors with aluminium, cadmium, copper, iron, lead, and zinc: an adsorptive voltammetric study. J Pineal Res 24:15–21. https://doi.org/10.1111/j.1600-079x.1998.tb00361.x
Kang K, Kim Y, Park S, Back K (2009) Senescence-induced serotonin biosynthesis and its role in delaying senescence in rice leaves. Plant Physiol 150:1380–1393. https://doi.org/10.1104/pp.109.138552
Kang K, Lee K, Park S, Kim Y, Back K (2010) Enhanced production of melatonin by ectopic overexpression of human serotonin N-acetyltransferase plays a role in cold resistance in transgenic rice seedlings. J Pineal Res 49:176–182. https://doi.org/10.1111/j.1600-079X.2010.00783.x
Kang K, Kong K, Park S, Natsagdor U, Kim YS, Back K (2011) Molecular cloning of a plant N-acetylserotonin methyltransferase and its expression characteristics in rice. J Pineal Res 50:304–309. https://doi.org/10.1111/j.1600-079X.2010.00841.x
Ke Q, Ye J, Wang B, Ren J, Yin L, Deng X, Wang S (2018) Melatonin mitigates salt stress in wheat seedlings by modulating polyamine metabolism. Front Plant Sci 9:914. https://doi.org/10.3389/fpls.2018.00914
Lee HY, Back K (2016a) 2-Hydroxymelatonin promotes the resistance of rice plant to multiple simultaneous abiotic stresses (combined cold and drought). J Pineal Res 61:303–316. https://doi.org/10.1111/jpi.12347
Lee HY, Back K (2016b) Mitogen-activated protein kinase pathways are required for melatonin-mediated defense responses in plants. J Pineal Res 60:327–335. https://doi.org/10.1111/jpi.12314
Lee HY, Back K (2017a) Melatonin is required for H2O2- and NO-mediated defense signaling through MAPKKK3 and OXI1 in Arabidopsis thaliana. J Pineal Res. https://doi.org/10.1111/jpi.12379
Lee K, Back K (2017b) Overexpression of rice serotonin N-acetyltransferase 1 in transgenic rice plants confers resistance to cadmium and senescence and increases grain yield. J Pineal Res. https://doi.org/10.1111/jpi.12392
Lee HJ, Back K (2019a) 2-Hydroxymelatonin confers tolerance against combined cold and drought stress in tobacco, tomato, and cucumber as a potent anti-stress compound in the evolution of land plants. Melatonin Res 2:35–46
Lee K, Back K (2019b) Melatonin-deficient rice plants show a common semidwarf phenotype either dependent or independent of brassinosteroid biosynthesis. J Pineal Res 66:e12537. https://doi.org/10.1111/jpi.12537
Lee H, Byeno Y, Back K (2014a) Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco. J Pineal Res 57:262–268. https://doi.org/10.1111/jpi.12165
Lee H, Byeon Y, Lee K, Lee H, Back K (2014b) Cloning of Arabidopsis serotonin N-acetyltransferase and its role with caffeic acid O-methyltransferase in the biosynthesis of melatonin in vitro despite their different subcellular localization. J Pineal Res 75:418–426. https://doi.org/10.1111/jpi.12181
Lee K, Zawadzka A, Czarnocki Z, Reiter RJ, Back K (2016) Molecular cloning of melatonin 3-hydroxylase and its production of cyclic 3-hydroxymelatonin in rice (Oryza sativa). J Pineal Res 61:470–480. https://doi.org/10.1111/jpi.12361
Lei X, Zhu R, Zhang G, Dai Y (2004) Attenuation of cold-induced apoptosis by exogenous melatonin in carrot suspension cells: the possible involvement of polyamines. J Pineal Res 36:126–131. https://doi.org/10.1046/j.1600-079x.2003.00106.x
Lerner A, Case J, Takahashi Y, Lee T, Mori W (1958) Isolation of melatonin, a pineal factor that lightens melanocytes. J Am Chem Soc 80:2587. https://doi.org/10.1021/ja01543a060
Li C, Wang P, Wei Z, Liang D, Liu C, Yin L, Jia D, Fu M, Ma F (2012) The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. J Pineal Res 53:298–306. https://doi.org/10.1111/j.1600-079X.2012.00999.x
Li C, Tan DX, Liang D, Chang C, Jia D, Ma F (2015) Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behaviour in two Malus species under drought stress. J Exp Bot 66:669–680. https://doi.org/10.1093/jxb/eru476
Li C, Liang B, Chang C, Wei Z, Zhou S, Ma F (2016a) Exogenous melatonin improved potassium content in Malus under different stress conditions. J Pineal Res 61:218–229. https://doi.org/10.1111/jpi.12342
Li H, He J, Yang X, Li X, Luo D, Wei C, Ma J, Zhang Y, Yang J, Zhang X (2016b) Glutathione-dependent induction of local and systemic defense against oxidative stress by exogenous melatonin in cucumber (Cucumis sativus L.). J Pineal Res 60:206–216. https://doi.org/10.1111/jpi.12304
Li X, Tan DX, Jiang D, Liu F (2016c) Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley. J Pineal Res 61:328–339. https://doi.org/10.1111/jpi.12350
Li H, Chang J, Chen H, Wang Z, Gu X, Wei C, Zhang Y, Ma J, Yang J, Zhang X (2017a) Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis. Front Plant Sci 8:295. https://doi.org/10.3389/fpls.2017.00295
Li H, Chang J, Zheng J, Dong Y, Liu Q, Yang X, Wei C, Zhang Y, Ma J, Zhang X (2017b) Local melatonin application induces cold tolerance in distant organs of Citrullus lanatus L. via long distance transport. Sci Rep 7:40858. https://doi.org/10.1038/srep40858
Li X, Yu B, Cui Y, Yin Y (2017c) Melatonin application confers enhanced salt tolerance by regulating Na+ and Cl- accumulation in rice. Plant Growth Regul 83:441–454. https://doi.org/10.1007/s10725-017-0310-3
Li C, Zhao Q, Gao T, Wang H, Zhang Z, Liang B, Wei Z, Liu C, Ma F (2018a) The mitigation effects of exogenous melatonin on replant disease in apple. J Pineal Res 65:e12523. https://doi.org/10.1111/jpi.12523
Li J, Arkorful E, Cheng S, Zhou Q, Li H, Chen X, Sun K, Li X (2018b) Alleviation of cold damage by exogenous application of melatonin in vegetatively propagated tea plant (Camellia sinensis (L.) O. Kuntze). Sci Hortic-amsterdam 238:356–362. https://doi.org/10.1016/j.scienta.2018.04.068
Li C, He Q, Zhang F, Yu J, Li C, Zhao T, Zhang Y, Xie Q, Su B, Mei L, Zhu S, Chen J (2019) Melatonin enhances cotton immunity to Verticillium wilt via manipulating lignin and gossypol biosynthesis. Plant J 100:784–800. https://doi.org/10.1111/tpj.14477
Liang C, Zheng G, Li W, Wang Y, Hu B, Wang H, Wu H, Qian Y, Zhu X, Tan D, Chen S, Chu C (2015) Melatonin delays leaf senescence and enhances salt stress tolerance in rice. J Pineal Res 59:91–101. https://doi.org/10.1111/jpi.12243
Liang C, Li A, Yu H, Li W, Liang C, Guo S, Zhang R, Chu C (2017) Melatonin regulates root architecture by modulating auxin response in rice. Front Plant Sci 8:134. https://doi.org/10.3389/fpls.2017.00134
Liang D, Gao F, Ni Z, Lin L, Deng Q, Tang Y, Wang X, Luo X, Xia H (2018) Melatonin improves heat tolerance in kiwifruit seedlings through promoting antioxidant enzymatic activity and glutathione s-transferase transcription. Molecules 23:584. https://doi.org/10.3390/molecules23030584
Liu N, Gong B, Jin Z, Wang X, Wei M, Yang F, Li Y, Shi Q (2015) Sodic alkaline stress mitigation by exogenous melatonin in tomato needs nitric oxide as a downstream signal. J Plant Physiol 186:68–77. https://doi.org/10.1016/j.jplph.2015.07.012
Ma X, Zhang J, Burgess P, Rossi S, Huang B (2018) Interactive effects of melatonin and cytokinin on alleviating drought-induced leaf senescence in creeping bentgrass (Agrostis stolonifera). Environ Exp Bot 145:1–11. https://doi.org/10.1016/j.envexpbot.2017.10.010
Martinez V, Nieves-Cordones M, Lopez-Delacalle M, Rodenas R, Mestre TC, Garcia-Sanchez F, Rubio F, Nortes PA, Mittler R, Rivero RM (2018) Tolerance to stress combination in tomato plants: new insights in the protective role of melatonin. Molecules. https://doi.org/10.3390/molecules23030535
Mauriz J, Collado P, Veneroso C, Reiter R, González-Gallego J (2013) A review of the molecular aspects of melatonin’s anti-inflammatory actions: recent insights and new perspectives. J Pineal Res 54:1–14. https://doi.org/10.1111/j.1600-079X.2012.01014.x
Meng J, Xu T, Wang Z, Fang Y, Xi Z, Zhang Z (2014) The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology. J Pineal Res 57:200–212. https://doi.org/10.1111/jpi.12159
Moustafa-Farag M, Almoneafy A, Mahmoud A, Elkelish A, Arnao MB, Li L, Ai S (2020) Melatonin and its protective role against biotic stress impacts on plants. Biomolecules 10:54. https://doi.org/10.3390/biom10010054
Mukherjee S, David A, Yadav S, Baluška F, Bhatla S (2014) Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiol Plantarum 152:714–728. https://doi.org/10.1111/ppl.12218
Nawaz MA, Jiao Y, Chen C, Shireen F, Zheng Z, Imtiaz M, Bie Z, Huang Y (2018) Melatonin pretreatment improves vanadium stress tolerance of watermelon seedlings by reducing vanadium concentration in the leaves and regulating melatonin biosynthesis and antioxidant-related gene expression. J Plant Physiol 220:115–127. https://doi.org/10.1016/j.jplph.2017.11.003
Ni J, Wang Q, Shah FA, Liu W, Wang D, Huang S, Fu S, Wu L (2018) Exogenous melatonin confers cadmium tolerance by counterbalancing the hydrogen peroxide homeostasis in wheat seedlings. Molecules 23:799. https://doi.org/10.3390/molecules23040799
Park S, Back K (2012) Melatonin promotes seminal root elongation and root growth in transgenic rice after germination. J Pineal Res 53:385–389. https://doi.org/10.1111/j.1600-079X.2012.01008.x
Park S, Lee D, Jang H, Byeon Y, Kim Y, Back K (2013) Melatonin-rich transgenic rice plants exhibit resistance to herbicide-induced oxidative stress. J Pineal Res 54:258–263. https://doi.org/10.1111/j.1600-079x.2012.01029.x
Pelagio-Flores R, Muñoz-Parra E, Ortiz-Castro R, López-Bucio J (2012) Melatonin regulates Arabidopsis root system architecture likely acting independently of auxin signaling. J Pineal Res 53:279–288. https://doi.org/10.1111/j.1600-079X.2012.00996.x
Pickles V, Sutcliffe J (1955) The effects of 5-hydroxytryptamine, indole-3-acetic acid, and some other substances, on pigment effusion, sodium uptake, and potassium efflux, by slices of red beetroot in vitro. Biochim Biophys Acta 17:244–251. https://doi.org/10.1016/0006-3002(55)90356-5
Qi ZY, Wang KX, Yan MY, Kanwar MK, Li DY, Wijaya L, Alyemeni MN, Ahmad P, Zhou J (2018) Melatonin alleviates high temperature-induced pollen abortion in solanum lycopersicum. Molecules 23:386. https://doi.org/10.3390/molecules23020386
Qiao Y, Yin L, Wang B, Ke Q, Deng X, Wang S (2019) Melatonin promotes plant growth by increasing nitrogen uptake and assimilation under nitrogen deficient condition in winter wheat. Plant Physiol Biochem 139:342–349. https://doi.org/10.1016/j.plaphy.2019.03.037
Ren S, Rutto L, Katuuramu D (2019) Melatonin acts synergistically with auxin to promote lateral root development through fine tuning auxin transport in Arabidopsis thaliana. PLoS ONE. https://doi.org/10.1371/journal.pone.0221687
Sami A, Shah FA, Abdullah M, Zhou X, Zhou K (2020) Melatonin mitigates cadmium and aluminium toxicity through modulation of antioxidant potential in Brassica napus L. Plant Biol. https://doi.org/10.1111/plb.13093
Sarropoulou V, Therios I, Dimassi-Theriou K (2012) Melatonin promotes adventitious root regeneration in in vitro shoot tip explants of the commercial sweet cherry rootstocks CAB-6P (Prunus cerasus L.), Gisela 6 (P. cerasus × P. canescens), and MxM 60 (P. avium × P. mahaleb). J Pineal Res 52:38–46. https://doi.org/10.1111/j.1600-079X.2011.00914.x
Shah AA, Ahmed S, Yasin NA (2020) 2-Hydroxymelatonin induced nutritional orchestration in Cucumis sativus under cadmium toxicity: modulation of non-enzymatic antioxidants and gene expression. Int J Phytoremediation 22:497–570. https://doi.org/10.1080/15226514.2019.1683715
Shi H, Chen Y, Tan D, Reiter R, Chan Z, He C (2015a) Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis. J Pineal Res 59:102–108. https://doi.org/10.1111/jpi.12244
Shi H, Qian Y, Tan D, Reiter R, He C (2015b) Melatonin induces the transcripts of CBF/DREB1s and their involvement in both abiotic and biotic stresses in Arabidopsis. J Pineal Res 59:334–342. https://doi.org/10.1111/jpi.12262
Shi H, Tan D, Reiter R, Ye T, Yang F, Chan Z (2015c) Melatonin induces class A1 heat-shock factors (HSFA1s) and their possible involvement of thermotolerance in Arabidopsis. J Pineal Res 58:335–342. https://doi.org/10.1111/jpi.12219
Shi H, Wang X, Tan D, Reiter R, Chan Z (2015d) Comparative physiological and proteomic analyses reveal the actions of melatonin in the reduction of oxidative stress in Bermuda grass (Cynodon dactylon (L). Pers.). J Pineal Res 59:120–131. https://doi.org/10.1111/jpi.12246
Shi H, Wei Y, He C (2016) Melatonin-induced CBF/DREB1s are essential for diurnal change of disease resistance and CCA1 expression in Arabidopsis. Plant Physiol Biochem 100:150–155. https://doi.org/10.1016/j.plaphy.2016.01.018
Simlat M, Ptak A, Skrzypek E, Warchoł M, Morańska E, Piórkowska E (2018) Melatonin significantly influences seed germination and seedling growth of Stevia rebaudiana Bertoni. PeerJ 6:e5009. https://doi.org/10.7717/peerj.5009
Su X, Xin L, Li Z, Zheng H, Mao J, Yang Q (2018) Physiology and transcriptome analyses reveal a protective effect of the radical scavenger melatonin in aging maize seeds. Free Radic Rese 52:1094–1109. https://doi.org/10.1080/10715762.2018.1472378
Sun Q, Zhang N, Wang J, Zhang H, Li D, Shi J, Li R, Weeda S, Zhao B, Ren S, Guo Y (2015) Melatonin promotes ripening and improves quality of tomato fruit during postharvest life. J Exp Bot 66:657–668. https://doi.org/10.1093/jxb/eru332
Sun Q, Zhang N, Wang J, Cao Y, Li X, Zhang H, Zhang L, Tan D, Guo Y (2016) A label-free differential proteomics analysis reveals the effect of melatonin on promoting fruit ripening and anthocyanin accumulation upon postharvest in tomato. J Pineal Res 61:138–153. https://doi.org/10.1111/jpi.12315
Sun C, Lv T, Huang L, Liu X, Jin C, Lin X (2020a) Melatonin ameliorates aluminum toxicity through enhancing aluminum exclusion and reestablishing redox homeostasis in roots of wheat. J Pineal Res. https://doi.org/10.1111/jpi.12642
Sun S, Wen D, Yang W, Meng Q, Shi Q, Gong B (2020b) Overexpression of caffeic acid o-methyltransferase 1 (COMT1) increases melatonin level and salt stress tolerance in tomato plant. J Plant Growth Regul 39:1221–1235. https://doi.org/10.1007/s00344-019-10058-3
Tan D (2015) Melatonin and plants. J Exp Bot 66:625–626. https://doi.org/10.1093/jxb/eru523
Tan DX, Reiter RJ (2020) An evolutionary view of melatonin synthesis and metabolism related to its biological functions in plants. J Exp Bot 71(16):4677–4689. https://doi.org/10.1093/jxb/eraa235
Tan DX, Manchester LC, Mascio P, Martinez GR, Prado FM, Reiter RJ (2007) Novel rhythms of N1-acetyl-N2-formyl-5-methoxykynuramine and its precursor melatonin in water hyacinth: importance for phytoremediation. FASEB J 21:1724–1729. https://doi.org/10.1096/fj.06-7745com
Tan XL, Fan ZQ, Kuang JF, Lu WJ, Reiter RJ, Lakshmanan P, Su XG, Zhou J, Chen JY, Shan W (2019) Melatonin delays leaf senescence of Chinese flowering cabbage by suppressing ABFs-mediated abscisic acid biosynthesis and chlorophyll degradation. J Pineal Res 67:e12570. https://doi.org/10.1111/jpi.12570
Wang P, Yin L, Liang D, Li C, Ma F, Yue Z (2012) Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate-glutathione cycle. J Pineal Res 53:11–20. https://doi.org/10.1111/j.1600-079X.2011.00966.x
Wang L, Zhao Y, Reiter R, He C, Liu G, Lei Q, Zuo B, Zheng X, Li Q, Kong J (2014) Changes in melatonin levels in transgenic ‘Micro-Tom’ tomato overexpressing ovine AANAT and ovine HIOMT genes. J Pineal Res 56:134–142. https://doi.org/10.1111/jpi.12105
Wang P, Sun X, Wang N, Tan D, Ma F (2015) Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings. J Pineal Res 58:479–489. https://doi.org/10.1111/jpi.12233
Wang Q, An B, Wei Y, Reiter RJ, Shi H, Luo H, He C (2016) Melatonin regulates root meristem by repressing auxin synthesis and polar auxin transport in Arabidopsis. Front Plant Sci 7:1882. https://doi.org/10.3389/fpls.2016.01882
Wang L, Feng C, Zheng X, Guo Y, Zhou F, Shan D, Liu X, Kong J (2017) Plant mitochondria synthesize melatonin and enhance the tolerance of plants to drought stress. J Pineal Res 63:e12429. https://doi.org/10.1111/jpi.12429
Wang M, Zhang T, Ding F (2019) Exogenous melatonin delays methyl jasmonate-triggered senescence in tomato leaves. Agronomy 9:795. https://doi.org/10.3390/agronomy9120795
Wang M, Zhang S, Ding F (2020a) Melatonin mitigates chilling-induced oxidative stress and photosynthesis inhibition in tomato plants. Antioxidants 9:218. https://doi.org/10.3390/antiox9030218
Wang X, Zhang H, Xie Q, Liu Y, Lv H, Bai R, Ma R, Li X, Zhang X, Guo YD, Zhang N (2020b) SlSNAT interacts with HSP40, a molecular chaperone, to regulate melatonin biosynthesis and promote thermotolerance in tomato. Plant Cell Physiol 61:909–921. https://doi.org/10.1093/pcp/pcaa018
Weeda S, Zhang N, Zhao X, Ndip G, Guo Y, Buck G, Fu C, Ren S (2014) Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems. PLoS ONE 9:e93462. https://doi.org/10.1371/journal.pone.0093462
Wei W, Li Q, Chu Y, Reiter R, Yu X, Zhu D, Zhang W, Ma B, Lin Q, Zhang J, Chen S (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66:695–707. https://doi.org/10.1093/jxb/eru392
Wei J, Li DX, Zhang JR, Shan C, Rengel Z, Song ZB, Chen Q (2018a) Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. J Pineal Res 65:e12500. https://doi.org/10.1111/jpi.12500
Wei Z, Gao T, Liang B, Zhao Q, Ma F, Li C (2018b) Effects of exogenous melatonin on methyl viologen-mediated oxidative stress in apple leaf. Int J Mol Sci 19:316. https://doi.org/10.3390/ijms19010316
Wen D, Gong B, Sun S, Liu S, Wang X, Wei M, Yang F, Li Y, Shi Q (2016) Promoting roles of melatonin in adventitious root development of solanum lycopersicum L. by regulating auxin and nitric oxide signaling. Front Plant Sci 7:718. https://doi.org/10.3389/fpls.2016.00718
Xiao S, Liu L, Wang H, Li D, Bai Z, Zhang Y, Sun H, Zhang K, Li C (2019) Exogenous melatonin accelerates seed germination in cotton (Gossypium hirsutum L.). PLoS ONE 14:e0216575. https://doi.org/10.1101/618959
Xu W, Cai S, Zhang Y, Wang Y, Ahammed G, Xia X, Shi K, Zhou Y, Yu J, Reiter R, Zhou J (2016) Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. J Pineal Res 61:457–469. https://doi.org/10.1111/jpi.12359
Xu L, Yue Q, Xiang G, Bian F, Yao Y (2018) Melatonin promotes ripening of grape berry via increasing the levels of ABA, H2O2, and particularly ethylene. Hortic Res 5:41. https://doi.org/10.1038/s41438-018-0045-y
Yang WJ, Du YT, Zhou YB, Chen J, Xu ZS, Ma YZ, Chen M, Min DH (2019) Overexpression of TaCOMT improves melatonin production and enhances drought tolerance in transgenic Arabidopsis. Int J Mol Sci 20:652. https://doi.org/10.3390/ijms20030652
Ye T, Yin X, Yu L, Zheng SJ, Cai WJ, Wu Y, Feng YQ (2019) Metabolic analysis of the melatonin biosynthesis pathway using chemical labeling coupled with liquid chromatography-mass spectrometry. J Pineal Res 66:e12531. https://doi.org/10.1111/jpi.12531
Ye J, Yang W, Li Y, Wang S, Yin L, Deng X (2020) Seed pre-soaking with melatonin improves wheat yield by delaying leaf senescence and promoting root development. Agronomy 10:84. https://doi.org/10.3390/agronomy10010084
Yin L, Wang P, Li M, Ke X, Li C, Liang D, Wu S, Ma X, Li C, Zou Y, Ma F (2013) Exogenous melatonin improves Malus resistance to Marssonina apple blotch. J Pineal Res 54:426–434. https://doi.org/10.1111/jpi.12038
Yin Z, Lu J, Meng S, Liu Y, Mostafa I, Qi M, Li T (2019) Exogenous melatonin improves salt tolerance in tomato by regulating photosynthetic electron flux and the ascorbate-glutathione cycle. J Plant Interact 14:453–463. https://doi.org/10.1080/17429145.2019.1645895
Zeng L, Cai J, Li J, Lu G, Li C, Fu G, Zhang X, Ma H, Liu Q, Zou X, Cheng Y (2018) Exogenous application of a low concentration of melatonin enhances salt tolerance in rapeseed (Brassica napus L.) seedlings. J Integr Agr 17:328–335. https://doi.org/10.1016/S2095-3119(17)61757-X
Zhang N, Zhao B, Zhang H, Weeda S, Yang C, Yang Z, Ren S, Guo Y (2013) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res 54:15–23. https://doi.org/10.1111/j.1600-079X.2012.01015.x
Zhang H, Zhang N, Yang R, Wang L, Sun Q, Li D, Cao Y, Weeda S, Zhao B, Ren S, Guo Y (2014a) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J Pineal Res 57:269–279. https://doi.org/10.1111/jpi.12167
Zhang N, Zhang H, Zhao B, Sun Q, Cao Y, Li R, Wu X, Weeda S, Li L, Ren S, Reiter R, Guo Y (2014b) The RNA-seq approach to discriminate gene expression profiles in response to melatonin on cucumber lateral root formation. J Pineal Res 56:39–50. https://doi.org/10.1111/jpi.12095
Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S, Guo Y (2015) Roles of melatonin in abiotic stress resistance in plants. J Exp Bot 66:647–656. https://doi.org/10.1093/jxb/eru336
Zhang J, Shi Y, Zhang X, Du H, Xu B, Huang B (2017a) Melatonin suppression of heat-induced leaf senescence involves changes in abscisic acid and cytokinin biosynthesis and signaling pathways in perennial ryegrass (Lolium perenne L.). Environ Exp Bot 138:36–45. https://doi.org/10.1016/j.envexpbot.2017.02.012
Zhang N, Zhang H, Sun Q, Cao Y, Li X, Zhao B, Wu P, Guo Y (2017b) Proteomic analysis reveals a role of melatonin in promoting cucumber seed germination under high salinity by regulating energy production. Sci Rep 7:503. https://doi.org/10.1038/s41598-017-00566-1
Zhang H, Wang L, Shi K, Shan D, Zhu Y, Wang C, Bai Y, Yan T, Zheng X, Kong J (2019a) Apple tree flowering is mediated by low level of melatonin under the regulation of seasonal light signal. J Pineal Res 66:e12551. https://doi.org/10.1111/jpi.12551
Zhang Q, Liu X, Zhang Z, Liu N, Li D, Hu L (2019b) Melatonin improved waterlogging tolerance in alfalfa (Medicago sativa) by reprogramming polyamine and ethylene metabolism. Front Plant Sci 10:44. https://doi.org/10.3389/fpls.2019.00044
Zhang T, Shi Z, Zhang X, Zheng S, Wang J, Mo J (2020) Alleviating effects of exogenous melatonin on salt stress in cucumber. Sci Hortic 262:109070. https://doi.org/10.1016/j.scienta.2019.109070
Zhao H, Xu L, Su T, Jiang Y, Hu L, Ma F (2015) Melatonin regulates carbohydrate metabolism and defenses against Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis thaliana. J Pineal Res 59:109–119. https://doi.org/10.1111/jpi.12245
Zheng X, Tan DX, Allan AC, Zuo B, Zhao Y, Reiter RJ, Wang L, Wang Z, Guo Y, Zhou J, Shan D, Li Q, Han Z, Kong J (2017) Chloroplastic biosynthesis of melatonin and its involvement in protection of plants from salt stress. Sci Rep 7:41236. https://doi.org/10.1038/srep41236
Zhou C, Liu Z, Zhu L, Ma Z, Wang J, Zhu J (2016a) Exogenous melatonin improves plant iron deficiency tolerance via increased accumulation of polyamine-mediated nitric oxide. Int J Mol Sci 17:1777. https://doi.org/10.3390/ijms17111777
Zhou X, Zhao H, Cao K, Hu L, Du T, Baluska F, Zou Z (2016b) 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 7:1823. https://doi.org/10.3389/fpls.2016.01823
Zia SF, Berkowitz O, Bedon F, Whelan J, Franks AE, Plummer KM (2019) Direct comparison of Arabidopsis gene expression reveals different responses to melatonin versus auxin. BMC Plant Biol 19:567. https://doi.org/10.1186/s12870-019-2158-3
Zuo B, Zheng X, He P, Wang L, Lei Q, Feng C, Zhou J, Li Q, Kong J (2014) Overexpression of MzASMT improves melatonin production and enhances drought tolerance in transgenic Arabidopsis thaliana plants. J Pineal Res 57:408–417. https://doi.org/10.1111/jpi.12180
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31860054, 32060711, 31460099).
Author information
Authors and Affiliations
Contributions
TZ and SZ wrote manuscript. JW, YS and LZ collected literature and wrote manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Handling editor: Rhonda Peavy.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zhang, T., Wang, J., Sun, Y. et al. Versatile Roles of Melatonin in Growth and Stress Tolerance in Plants. J Plant Growth Regul 41, 507–523 (2022). https://doi.org/10.1007/s00344-021-10317-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-021-10317-2