Abstract
Melatonin is a ubiquitous signaling plant hormone that plays a crucial role in regulating the growth and development of plants under stress conditions. Since a few species have been investigated to unveil the effect of exogenous melatonin on salt stress, in the current research study, we investigated the effects of melatonin by measuring the photosynthetic characteristics and antioxidant defense system of maize seedling under salt stress (200 mM NaCl), along with different concentrations of melatonin (MT1—30, MT2–60, and MT3–90 µM) treatments. Salt stress reduced the plant growth characteristics and photosynthetic efficiency by increasing the ROS accumulation and reducing the antioxidant enzyme activities of maize seedling. However, pretreatment with melatonin on roots alleviated NaCl-induced decrease in photosynthetic rate and oxidative stress in a dose-dependent manner. Our results revealed that exogenous application of melatonin at an optimum concentration (60 µM) under salt stress conditions significantly increased the growth of plants, chlorophyll content, photosynthetic efficiency, antioxidant enzymes activities, i.e., superoxide dismutase (SOD), peroxide (POD), catalase (CAT) and ascorbate peroxidase (APX), and reduced the reactive oxygen species (ROS). This study unraveled the crucial role of melatonin in salt stress mitigation and thus can be implicated in the management of salinity in maize seedling.
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Ahmad S, Su W, Kamran M et al (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
Ahmed MN, Yasin KA, Ayub K, Mahmood T, Tahir MN, Khan BA, Hafeez M, Ahmedz M, ul-Haq I (2018) Click one pot synthesis, spectral analyses, crystal structures, DFT studies and brine shrimp cytotoxicity assay of two newly synthesized 1,4,5-trisubstituted 1,2,3-triazoles. J Mol Struct 1106:430–439
Arnao MB, Hernández RJ (2010) Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves. J Pineal Res 46:58–63
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Bajwa VS, Shukla MR, Sherif SM, Murch SJ, Saxena PK (2014) Role of melatonin in alleviating cold stress in Arabidopsis thaliana. J Pineal Res 56:238–245
Barrett P, Bolborea M (2012) Molecular pathways involved in seasonal body weight and reproductive responses governed by melatonin. J Pineal Res 52:376–388
Bleiss W, Ehwald R (1993) Transient changes in length and growth of wheat coleoptile segments following treatments with osmotica and auxin. Physiol Plant 88:541–548
Bui EN (2013) Soil salinity: A neglected factor in plant ecology and biogeography. J Arid Environ 92:14–25
Byeon Y, Back K (2014) Melatonin synthesis in rice seedlings in vivo is enhanced at high temperatures and under dark conditions due to increased serotonin N-acetyltransferase and N-acetylserotonin me. J Pineal Res 56:189–195
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227
Carmen R, Juan CM, Rosa MS, Isaac A, Russel JR (2004) Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 36:1–9
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. https://doi.org/10.1093/aob/mcn125
Chen YE, Jun-Mei C, Yan-Qiu S, Shu Y, Ming Y, Huai-Yu Z (2015) Influence of stripe rust infection on the photosynthetic characteristics and antioxidant system of susceptible and resistant wheat cultivars at the adult plant stage. Front Plant Sci 6:779
Chen Z, Xie Y, Gu Q, Zhao G, Zhang Y, Cui W, Xu S, Wang R, Shen W (2017) The AtrbohF -dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radic Biol Med 108:465–477
Cui G, Zhao X, Liu S, Sun F, Zhang C, Xi Y (2017) Beneficial effects of melatonin in overcoming drought stress in wheat seedlings. Plant Physiol Biochem 118:138–149
Cuin TA, Shabala S (2007) Compatible solutes reduce ROS-induced potassium efflux in Arabidopsis roots. Plant Cell Environ 30:875–885
Fariduddin Q, Mir BA, Yusuf M, Ahmad A (2014) 24-epibrassinolide and/or putrescine trigger physiological and biochemical responses for the salt stress mitigation in Cucumis sativus L. Photosynthetica 52:464–474
Giannopolitis CN, Ries SK (1977) Superoxide Dismutases: II: purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 59:315–318
Hao L, Jingjing C, Hejie C, Zhongyuan W, Xiurong G, Chunhua W, Yong Z, Jianxiang M, Jianqiang Y, Xian Z (2016) Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis. Front Plant Sci 8:295
Hardeland R, Madrid JA, Tan D-X, Reiter RJ (2012) Melatonin, the circadian multioscillator system and health: the need for detailed analyses of peripheral melatonin signaling. J Pineal Res 52:139–166
Havir EA, Mchale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455
Hernández-Ruiz J, Cano A, Arnao MB (2004) Melatonin: a growth-stimulating compound present in lupin tissues. Planta 220:140–144
Jiang C, Cui Q, Feng K, Xu D, Li C, Zheng Q (2016) Melatonin improves antioxidant capacity and ion homeostasis and enhances salt tolerance in maize seedlings. Acta Physiol Plant 38:82
Jiang C, Zu C, Lu D, Zheng Q, Shen J, Wang H, Li D (2017) Effect of exogenous selenium supply on photosynthesis, Na (+) accumulation and antioxidative capacity of maize (Zea mays L.) under salinity stress. Sci Rep 7:42039
Kamran M, Wennan S, Ahmad I, Xiangping M, Wenwen C, Xudong Z, Siwei M, Khan A, Qingfang H, Tiening L (2018) Application of paclobutrazol affect maize grain yield by regulating root morphological and physiological characteristics under a semi-arid region. Sci Rep 8:4818
Katarzyna S, Reiter RJ, Posmyk MM (2016) 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 7:1663
Lerner AB, Case JD, Takahashi Y, Lee TH, Mori W (1958) Isolation of melatonin, the pineal gland factor that lightens melanocytess. J Am Chem Soc 80:2587–2587
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
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 8:1–9. https://doi.org/10.3389/fpls.2017.00295
Liu J, Yue R, Si M, Wu M, Cong L, Zhai R, Yang C, Wang Z, Ma F, Xu L (2019) Effects of exogenous application of melatonin on quality and sugar metabolism in ‘Zaosu’ pear fruit. J Plant Growth Regul 38:1161–1169
Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76
Mishima K (2012) Melatonin as a regulator of human sleep and circadian systems. Nihon rinsho. Jpn J Clin Med 70:1139–1144
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Mukherjee S, David A, Yadav S, Baluška F, Bhatla SC (2014) Salt stressinduced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiol Plant 152:714–728. https://doi.org/10.1111/ppl.12218
Naeem M, Naeem MS, Ahmad R, Ahmad R, Ashraf MY, Ihsan MZ, Nawaz F, Athar H, Ashraf M, Abbas HT, Abdullah M (2018) Improving drought tolerance in maize by foliar application of boron: water status, antioxidative defense and photosynthetic capacity. Arch Agron Soil Sci 64:626–639
Nakano Y, Asada K (1980) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nuss ET, Tanumihardjo SA (2010) Maize: a paramount staple crop in the context of global nutrition. Compr Rev Food Sci Food Saf 9:417–436
Pandolfi C, Mancuso S, Shabala S (2012) Physiology of acclimation to salinity stress in pea (Pisum sativum). Environ Exp Bot 84:44–55
Posmyk Mg M, Janas KM (2009) Melatonin in plants. Acta Physiol Plant 31:1–11
Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi: a review. Agron Sustain Dev 32:181–200. https://doi.org/10.1007/s13593-011-0029-x
Polesskaya OG, Kashirina EI, Alekhina ND (2004) Changes in the Activity of antioxidant enzymes in wheat leaves and roots as a function of nitrogen source and supply. Russ J Plant Physiol 51:615–620
Posmyk MM, Kontek R, Janas KM (2008) Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicol Environ Saf 72:592–602
Szafrańska K, Reiter RJ, Posmyk MM (2016) 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 7:1–12. https://doi.org/10.3389/fpls.2016.01663
Qingbo K, Jun Y, Bomei W, Jianhong R, Lina Y, Xiping D, Shiwen W (2018) Melatonin mitigates salt stress in wheat seedlings by modulating polyamine metabolism. Front Plant Sci 9:914
Sarropoulou V, Dimassi-Theriou K, Therios I, Koukourikou-Petridou M (2012) Melatonin enhances root regeneration, photosynthetic pigments, biomass, total carbohydrates and proline content in the cherry rootstock PHL-C (Prunus avium×Prunus cerasus). Plant Physiol Biochem 61:162–168
Shi H, Wang X, Tan DX, Reiter RJ, Chan Z (2015) 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
Suriya-arunroj D, Supapoj N, Toojinda T, Vanavichit A (2004) Relative leaf water content as an efficient method for evaluating rice cultivars for tolerance to salt stress. Sci Asia 30:411–415
Tan DX, Manchester LC, Korkmaz A, Ma S, Rosales-Corral S, Reiter RJ (2012) Fundamental issues related to the origin of melatonin and melatonin isomers during evolution: relation to their biological functions. Int J Mol Sci 15:15858–15890
Tiwari JK, Munshi AD, Kumar R, Pandey RN, Arora A, Bhat JS, Sureja AK (2010) Effect of salt stress on cucumber: Na+–K+ ratio, osmolyte concentration, phenols and chlorophyll content. Acta Physiol Plant 32:103–114
Turk H, Erdal S (2015) Melatonin alleviates cold-induced oxidative damage in maize seedlings by up-regulating mineral elements and enhancing antioxidant activity. J Plant Nutr Soil Sci 178:433–439
Turk H, Erdal S, Genisel M, Atici O, Demir Y, Yanmis D (2014) The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul 74:139–152
Uchendu EE, Shukla MR, Reed BM, Saxena PK (2013) Melatonin enhances the recovery of cryopreserved shoot tips of American elm (Ulmus americana L.). J Pineal Res 55:435–442
Wang LY, Liu JL, Wang WX, Sun Y (2016) Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress. Photosynthetica 54:19–27
Wang P, Sun X, Li C, Wei Z, Liang D, Ma F (2013) Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. J Pineal Res 54:292–302
Wang PYL, 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
Wei W, Li QT, Chu YN, Reiter RJ, Yu X-M, Zhu D-H, Zhang W-K, Ma B, Lin Q, Zhang J-S (2015a) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66:695–707
Yang X, Lu C (2005) Photosynthesis is improved by exogenous glycinebetaine in saltstressed maize plants. Physiol Plant 124:343–352
Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217:523–539
Ye J, Wang S, Deng X, Yin L, Xiong B, Wang X (2016) Melatonin increased maize (Zea mays L.) seedling drought tolerance by alleviating drought-induced photosynthetic inhibition and oxidative damage. Acta Physiol Plant. https://doi.org/10.1007/s11738-015-2045-y
Yin L, Wang P, Li M, Ke X, Li C, Liang D, Wu S, Ma X, Li C, Zou Y (2013) Exogenous melatonin improves Malus resistance to Marssonina apple blotch. J Pineal Res 54:426–434
Zeng L, Cai JS, Jing-Jing LI, Guang-Yuan LU, Chun-Sheng LI, Gui-Ping FU, Zhang XK, Hai-Qing MA, Liu QY, Zou XL (2018) Exogenous application of a low concentration of melatonin enhances salt tolerance in rapeseed (Brassica napus L.) seedlings. J Integr Agric 17:328–335
Zhang H, Chen T, Wang Z, Yang J, Zhang J (2010) Involvement of cytokinins in the grain filling of rice under alternate wetting and drying irrigation. J Exp Bot 61:3719–3733
Zhang HJ, 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
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71
Acknowledgements
This study was supported by funding from High Technology Research and Development Program of China (863 Program, No. 2013AA102902), the special fund for Agro-scientific Research in the Public Interest (201303104), the 111 Project of Chinese Education Ministry (B12007). The author would like to extend their sincere appreciation to the Researchers Supporting Project number (RSP-2020/19), King Saud University, Riyadh, Saudi Arabia.
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H.Q., Z.J., and S.A. designed the experiment. S.A. performed the experiment and wrote the manuscript. W.C. helped in manuscript revision. M.K. helped in data analysis and review the MS. I.A., M.X., W.X., and W.S. T.J. helped in data collection. H. A. El-S. Revised the MS for language. All the authors have read and approved the final manuscript.
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Shakeel Ahmad and Wenwen Cui have contributed equally to this study.
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Ahmad, S., Cui, W., Kamran, M. et al. 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 40, 1270–1283 (2021). https://doi.org/10.1007/s00344-020-10187-0
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DOI: https://doi.org/10.1007/s00344-020-10187-0