Recent Progress on Melatonin-Induced Salinity Tolerance in Plants: An Overview

n this context, it is necessary to select and develop salt-tolerant genotypes that can grow in salty soils and have high yields, and formulate strategies which may enhance the plant survival under salinity stress. Melatonin (N-acetyl-5-methoxytryptamine) is an important biological hormone that provides resistance to abiotic stress conditions and can be secreted by plants. Melatonin concentration in plants varies depending on genotype, temperature and growth period. Increase in melatonin concentration is associated with increased SNAT and HIOMAT/ASMT enzyme activity. It plays an important role in gibberellic acid and abscisic acid biosynthesis during the germination and provides plant growth and development. Exogenous application of melatonin significantly alleviates chlorophyll degradation and stomatal closure caused by salt stress, improves photosynthesis and enhances plants' salt tolerance. Besides it significantly reduces the harmful effects of salinity by regulating plant physiology, improving plant morphology, photosynthesis and activities of antioxidant enzymes. The present review discusses the recent studies on the effect of melatonin on plant growth and physiology against salt stress that have important impacts on plant growth and development have been given according to the findings of various researches. It also highlights the mechanim/s of melatonin-induced salinity stress tolerance in plants.

PDF

___

Ahmad S, Cui W, Kamran M, Ahmad I, Meng X, Wu X, Su W, Javed T, El-Serehy HA, Jia Z, Han Q. 2020. Exogenous Application of Melatonin Induces Tolerance to Salt Stress by Improving the Photosynthetic Efficiency and Antioxidant Defense System of Maize Seedling. J. Plant Growth Regul., 1-14. https://doi.org/10.1007/s00344-020-10187-0
Alharbi BM, Elhakem AH, Alnusairi GSH, Mona H, Soliman MH, Hakeem KR, Hasan MM, Abdelhamid MT. 2021. Exogenous application of melatonin alleviates salt stress- induced decline in growth and photosynthesis in Glycine max (L.) seedlings by improving mineral uptake, antioxidant and glyoxalase system. Plant Soil Environ., 67: 208-220. https://doi.org/10.17221/659/2020-PSE
Arnao MB, Hernandez-Ruiz J. 2007. Melatonin in plants. Plant Signaling and Behavior, 2(5): 381-382 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. Journal of Plant Physiology, 166: 324-328. https://doi.org/10.1016/j.jplph.2008.06.002
Chen YE, Mao JJ, Sun LQ, Huang B, Ding CB, Gu Y, Liao JQ, Hu C, Zhang ZW, Yuan S, Yuan M. 2018. Exogenous melatonin enhances salt stress tolerance in maize seedlings by improving antioxidant and photosynthetic capacity. Physiol Plant, 164: 349-363. https://doi.org/10.1111/ppl.12737
Chen L, Liu L, Lu B, Ma T, Jiang D, Li J, Zhang K, Sun H, Zhang Y, Bai Z. 2020. Exogenous melatonin promotes seed germination and osmotic regulation under salt stress in cotton (Gossypium hirsutum L.). PLoS ONE, 15 e0228241. https://dx.doi.org/10.1371%2Fjournal.pone.0228241
Dawood MG, El-Awadi ME. 2015. Alleviation of salinity stress on Vicia faba L. plants via seed priming with melatonin. Acta Biol Colomb, 20(2): 223-235. https://doi.org/10.15446/ ABC.V20N2.43291
El Mashad AAA, Mohamed HI. 2012. Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis). Protoplasma, 249: 625-635. https://doi. org/10.1007/s00709-011-0300-7
Hacısevki A, Baba B. 2018. An overview of melatonin as an antioxidant molecule: A biochemical approach. Melatonin Mol. Biol. Clin. Pharm. Approaches, 59-85.
Hancı F. 2019. The Effect of L-Tryptophan and Melatonin on Seed Germination of Some Cool Season Vegetable Species Under Salinity Stress. Düzce Üniversitesi Bilim ve Teknoloji Dergisi, 7:1879-1891.
Jahan MS, Wang Y, Shu S, Zhong M, Chen Z, Wu J, Sun J, Guo S. 2019. Exogenous salicylic acid increases the heat tolerance in tomato (Solanum lycopersicum L) by enhancing photosynthesis efficiency and improving antioxidant defense system through scavenging of reactive oxygen species. Sci Hortic, 247:421-429. https://doi.org/10.1016/j.scienta. 2018.12.047
Jiang J, Cui Q, Feng K, Xu D, Li C, Zheng Q. 2016a. Melatonin improves antioxidant capacity and ion homeostasis and enhances salt tolerance in maize seedlings. Acta Physiologiae Plantarum, 38(82): 1-9. https://doi.org/10.1007/s11738-016- 2101-2
Jiang X, Li H, Song X. 2016b. Seed priming with melatonin effects on seed germination and seedling growth in maize under salinity stress. Pak J Bot, 48: 1345-1352
Jiang D, Lu B, Liu L, Duan W, Meng Y, Li J, Zhang K, Sun H, Zhang Y, Dong H, Bai Z, Li C. 2021. Exogenous melatonin improves the salt tolerance of cotton by removing active oxygen and protecting photosynthetic organs. BMC Plant Biol, 331. https://doi.org/10.1186/s12870-021-03082-7
Kabiri R, Hatami A, Oloumi H, Naghizadeh M, Nasibi F, Tahmasebi Z. 2018. Foliar application of melatonin induces tolerance to drought stress in Moldavian balm plants (Dracocephalum moldavica) through regulating the antioxidant system. Folia Hortic, 30: 155-167. https://doi.org/10.2478/fhort-2018-0016
Kamiab F. 2020. Exogenous melatonin mitigates the salinity damages and improves the growth of pistachio under salinity stress. Journal of Plant Nutrition, 43(10): 1468-1484. https://doi.org/10.1080/01904167.2020.1730898
Kaya A, Inan M. 2018. Kuraklık ve Tuz Streslerine Maruz Kalan Tütün (Nicotiana tabacum L.) Bitkisinde Bazı Fizyolojik ve Biyokimyasal Parametreler Üzerine Melatoninin Etkileri. KSÜ Tarım ve Doğa Derg, 21(4): 559-564
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://dx.doi.org/10.3389%2Ffpls.2018.00914
Khan A, Numan M, Khan AL, Lee IJ, Imran M, Asaf S, Al- Harrasi A. 2020. Melatonin: Awakening the Defense Mechanisms during Plant Oxidative Stress. Plants, 9:407. https://dx.doi.org/10.3390%2Fplants9040407
Korkmaz A, Yakupoglu G, Koklu Ş, Cuci Y, Kocacinar F. 2017. Determining Diurnal and Seasonal Changes in Tryptophan and Melatonin Content of Eggplant (Solanum melongena L.). Turkish Journal of Botany, 41:356-366. https://dx.doi.org/ 10.3906/bot-1611-48
Kul R, Esringü A, Dadasoglu E, Sahin Ü, Turan M, Örs S, Ekinci M, Agar G, Yildirim E. 2019. Melatonin: role in increasing plant tolerance in abiotic stress conditions. In: Abiotic and biotic stress in plants. https://doi.org/10.5772/ intechopen. 82590
Li Y, Zhang Y, Feng F, Liang D, Cheng L, Ma F, Shi S. 2010. Overexpression of a Malus vacuolar Na+/H+ antiporter gene (MdNHX1) in apple rootstock M.26 and its influence on salt tolerance. Plant Cell Tissue Org Cult, 102:337-345. http://dx.doi.org/10.1007/s11240-010-9738-0
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.2012.0099 9.x
Li H, Chang J, Chen H, Wang Z, Gu X, Wei C, Zhang Y, Ma J, Yang J, Zhang X. 2017. 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 J, Liu J, Zhu T, Zhao C, Li L, Chen M. 2019a. The role of melatonin in salt stress responses. Int J Mol Sci, 20:1735. https://doi.org/10.3390/ijms20071735
Li JP, Zhao C, Zhang MJ, Yuan F, Chen M. 2019b. Exogenous melatonin improves seed germination in Limonium bicolor under salt stress. Plant Signaling and Behavior, 14: 1659705. https://doi.org/10.1080/15592324.2019.1659705
Liang C, Zheng G, Li W, Wang Y, Hu B, Wang H, Wu H, Qian Y, Zhu XG, Tan DX, Chen SY, 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
Liu J, Shabala S, Zhang J, Ma G, Chen D, Shabala L, Zeng F, Chen ZH, Zhou M, Venkataraman G. 2020. Melatonin improves rice salinity stress tolerance by NADPH oxidase dependent control of the plasma membrane K+ transporters and K+ homeostasis. Plant Cell Environ, https://doi.org/10. 1111/pce.13759
Mohamadi M, Karimi M. 2020. Effect of exogenous melatonin on growth, electrolyte leakage and antioxidant enzyme activity in rosemary under salinity stress. Journal of Plant Process and Function, 9(37): 59-65.
Park HS, Kazerooni EA, Kang SM, Al-Sadi AM, Lee IJ. 2021. Melatonin Enhances the Tolerance and Recovery Mechanisms in Brassica juncea (L.) Czern. under Saline Conditions. Frontiers in plant science, 12:593717. https://doi.org/10.3389/fpls.2021.593717
Shi H, Jiang C, Ye T, Tan DX, Reiter RJ, Zhang H, Liu R, Chan Z. 2015a. Comparative physiological, metabolomic, and transcriptomic analyse several mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. J Exp Bot, 66:681-694. https://doi.org/10.1093/jxb/eru373
Shi H, Wang X, Tan DX, Reiter RJ, Chan Z. 2015b. 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, Qian Y, Tan DX, Reiter RJ, He C. 2015c. 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, Reiter RJ, Tan DX, Chan Z. 2015d. INDOLE-3-ACETIC ACID INDUCIBLE 17 positively modulates natural leaf senescence through melatonin-mediated pathway in Arabidopsis. J. Pineal Res, 58: 26-33. https://doi.org/ 10.1111/jpi.12188
Siddiqui HM, Alamri S, Al-Khaishany YM, Khan NM, Al-Amri A, Ali MH, Alaraidh AI, Alsahli AA. 2019. Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings. Int J Mol Sci, 20: 353. https://doi.org/10.3390/ijms20020353
Simlat M, Szewczyk A, Ptak A. 2020. Melatonin promotes seed germination under salinity and enhances the biosynthesis of steviol glycosides in Stevia rebaudiana Bertoni leaves. PLoS One, 27: 15(3): e0230755. http://dx.doi.org/10.1371/ journal.pone.0230755.
Tan DX, Hardeland R, Manchester LC, Korkmaz A, Ma S, Rosales-Corral S, Reiter RJ. 2012. Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science. Journal of Experimental Botany, 63:577- 597. http://dx.doi.org/10.1093/jxb/err256
Van Tassel DL, Roberts N, Lewy A, O’neill SD. 2001. Melatonin in plant organs. J Pineal Res, 31:8-15
Varghese N, Alyammahi O Nasreddine S, Alhassani A, Gururani MA. 2019. Melatonin positively influences the photosynthetic machinery and antioxidant system of Avena sativa during salinity stress. Plants 8: 610. http://dx.doi.org/10.3390/plants8120610
ang DY, Wang J, Shi SH, Huang LX, Zhu M, Li FH. 2021. Exogenous melatonin ameliorates salinity-induced oxidative stress and improves photosynthetic capacity in sweet corn seedlings. Photosynthetica, 59(2): 327-336. http://dx.doi.org/ 10.1007/s11099-015-0140-3
Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu D H, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY. 2015. Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. Journal of Experimental Botany, 66:695-707. https://doi.org/ 10.1093/jxb/eru392
Wei J, Li DX, Zhang JR, Shan C, Rengel Z, Song ZB, Chen Q. 2018. Phytomelatonin receptor PMTR1 mediated signalling regulates stomatal closure in Arabidopsis thaliana. J Pineal Res, 65:(2). https://doi.org/10.1111/jpi.12500
Xu L, Xiang G, Sun Q, Ni Y, Jin Z, Gao S, Yao Y. 2019. Melatonin enhances salt tolerance by promoting MYB108A- mediated ethylene biosynthesis in grapevines. Hortic Res. 6:114. http://dx.doi.org/10.1038/s41438-019-0197-4
Yakupoglu G, Koklu Ş, Korkmaz A. 2018. Bitkilerde melatonin ve üstlendiği görevler. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 21(2): 264-276
Yakupoglu G. 2020. Biberde Tuz Stresine Karşı Melatonin Uygulamasının Bazı Fide Özellikleri Üzerine Etkisi. Erciyes Üniversitesi, Fen Bilimleri Enstitüsü Dergisi, 36(1): 76-81
Yandi W. 2018. Chinese Changes in Melatonin Content in Grape and Prokaryotic Expression Analysis of Its Synthetic Gene SNAT; Academy of Agricultural Sciences: Beijing, China.
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
Yu Y, Wang A, Li X, Kou, M Wang, W Chen X, Xu T, Zhu M, Ma D, Li Z, Sun J. 2018. Melatonin-stimulated triacylglycerol breakdown and energy turnover under salinity stress contributes to the maintenance of plasma membrane H+-ATPase activity and K+/Na+ homeostasis in sweet potato. Frontiers in Plant Science, 9:256. http://dx.doi.org/ 10.3389/fpls.2018.00256
Yu R, Zuo T, Diao P, Fu J, Fan Y, Wang Y, Wuriyanghan H. 2021. Melatonin Enhances Seed Germination and Seedling Growth of Medicago sativa Under Salinity via a Putative Melatonin Receptor MsPMTR1. Front Plant, 12:702875. http://dx.doi.org/10.3389/fpls.2021.702875
Zafar S, Hasnain Z, Anwar S, Perveen S, Iqbal N, Noman A, Ali M. 2019. Influence of melatonin on antioxidant defence system and yield of wheat (Triticum aestivum L.) genotypes under saline condition. Pak J Bot, 51:1987-1994. http://dx.doi.org/10.30848/PJB2019-6(5)
Zahedi SM, Hosseini MS, Abadía J, Marjani M. 2020. Melatonin foliar sprays elicit salinity stress tolerance and enhance fruit yield and quality in strawberry (Fragaria × ananassa Duch.). Plant Physiology and Biochemistry, 149: 313-323. https://doi.org/10.1016/j.plaphy.2020.02.021
Zeng L, Cai JS, Li JJ, Lu GY, Li CS, Fu GP, Zhang XK, Ma HQ, Liu QY, Zou XL, Cheng Y. 2018. Exogenous application of a low concentration of melatonin enhances salt tolerance in rapeseed (Brassica napus L.) seedlings. J Integ Agr, 17:328- 335. https://doi.org/10.1016/S2095-3119(17)61757-X
Zhan H, Nie X, Zhang T, Li S, Wang X, Du X, Tong W, Song W. 2019. Melatonin: A small molecule but important for salt stress tolerance in plants. Int J Mol Sci, 20:709. https://doi.org/10.3390/ijms20030709
Zhang HJ, Zhang N, Yang RC, Wang L, Sun QQ, Li DB, Cao YY, Weeda S, Zhao B, Ren S, Guo YD. 2014. 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, Sun QQ, Zhang HJ, Cao YY, Weeda S, Ren SX, Guo YD. 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 HJ, Sun QQ, Cao YY, Li X, Zhao B, Wu P, Guo YD. 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 T, Shi Z, Zhang X, Zheng S, Wang J, Mo J. 2020. Alleviating effects of exogenous melatonin on salt stress in cucumber. Scientia Horticulturae, 262: 109070. https://doi.org/10.1016/j.scienta.2019.109070
Zhang P, Liu L, Wang X, Wang Z, Zhang H, Chen J, Liu X, Wang Y, Li C. 2021. Beneficial effects of exogenous melatonin on overcoming salt stress in sugar beets (Beta vulgaris L). Plants, 10:886. https://doi.org/10.3390/plants10050886
Zhou X, Zhao H, Cao K, Hu L, Du T, Baluška F, Zou Z. 2016. Beneficial roles of melatonin on redox regulation of photosynthetic electron transport and synthesis of D1 protein in tomato seedlings