Skip to main content

Advertisement

Log in

Exogenous Melatonin Improves the Growth of Rice Seedlings by Regulating Redox Balance and Ion Homeostasis Under Salt Stress

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

This study evaluated the effects of foliar spraying melatonin (MT) on the growth of salt-stressed rice. Seedlings were treated with 50 and 100 mM of NaCl and different concentrations of MT (25, 50, 100, 200, 300, and 400 μM) for 14 days. Different concentrations of MT could promote plant growth significantly under salt stress, particularly at concentrations of 200, 300, and 400 μM. A concentration of 200 μM MT was considered as optimal and used in a subsequent experiment on biomass, water content, antioxidation, mineral nutrition, salt absorption, and distribution of salt-stressed rice seedlings. Results showed that MT’s promoting effect on plant growth under salt stress was evident with time, particularly under high salt stress. MT improved the activities of antioxidant enzymes, reduced membrane lipid peroxidation, alleviated cell injury in plant leaves, and increased N content and Si accumulation in the leaves and roots under salt stress, particularly under high salinity. This compound also inhibited Na uptake and upward transport, but it promoted or maintained the uptake and upward transport of K and Ca in salt-stressed rice. Thus, MT improved the ion homeostasis of K/Na and Ca/Na in plants, particularly in the leaves. Foliar spraying of MT alleviated salt stress on rice by promoting nutrient accumulation or translocation, improving ion homeostasis, which is evident in the leaves, and consequently enhancing its salt resistance. The antioxidative improvement caused by MT might also be related to the improved ion homeostasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Ahanger MA, Aziz U, Alsahli AA, Alyemeni MN, Ahmad P (2020) Influence of exogenous salicylic acid and nitric oxide on growth, photosynthesis, and ascorbate-glutathione cycle in salt stressed vigna angularis. Biomolecules 10(1):42

    Article  CAS  Google Scholar 

  • Ahmad P, Ahanger MA, Alam P, Alyemeni MN, Wijaya L, Ali S, Ashraf M (2018) Silicon (Si) supplementation alleviates NaCl toxicity in mung bean [Vigna radiata (L.) Wilczek] through the modifications of physio-biochemical attributes and key antioxidant enzymes. J Plant Growth Regul. https://doi.org/10.1007/s00344-018-9810-2

    Article  Google Scholar 

  • Ahmad S, Cui WW, Kamran M, Ahmad I, Meng XP, Wu XR, Su WN, Javed T, ElSerehy HA, Jia ZK, Han QF (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. https://doi.org/10.1007/s00344-020-10187-0

    Article  Google Scholar 

  • 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 Biol Med 106:315–328

    Article  CAS  PubMed  Google Scholar 

  • Castañares JL, Bouzo CA (2019) Effect of exogenous melatonin on seed germination and seedling growth in melon (Cucumis melo L.) under salt stress. Hortic Plant J 5:79–87

    Article  Google Scholar 

  • Cen HF, Wang TT, Liu HY, Tian DY, Zhang YW (2020) Melatonin application improves salt tolerance of alfalfa (Medicago sativa L.) by enhancing antioxidant capacity. Plants 9(2):220

    Article  CAS  PubMed Central  Google Scholar 

  • Cheeseman JM (2006) Hydrogen peroxide concentrations in leaves under natural conditions. J Exp Bot 57:2435–2444

    Article  CAS  PubMed  Google Scholar 

  • 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(3):349–363

    Article  CAS  PubMed  Google Scholar 

  • El-Katony TM, Deyab MA, El-Adl MF, Ward MFE (2020) The aqueous extract and powder of the brown alga Dictyota dichotoma (Hudson) differentially alleviate the impact of abiotic stress on rice (Oryza sativa L.). Physiol Mol Biol Plant 26(6):1155–1171

    Article  CAS  Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxyl ammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  CAS  PubMed  Google Scholar 

  • Erdal S (2019) Melatonin promotes plant growth by maintaining integration and coordination between carbon and nitrogen metabolisms. Plant Cell Rep 38(8):1001–1012

    Article  CAS  PubMed  Google Scholar 

  • Farouk S, Elhindi KM, Alotaibi MA (2020) Silicon supplementation mitigates salinity stress on Ocimum basilicum L. via improving water balance, ion homeostasis, and antioxidant defense system. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2020.111396

    Article  PubMed  Google Scholar 

  • Formentin E, Barizza E, Stevanato P, Falda M, Massa F, Tarkowska D, Novák O, Lo Schiavo F (2018) Fast regulation of hormone metabolism contributes to salt tolerance in rice (Oryza sativa spp. Japonica, L.) by inducing specific morpho-physiological responses. Plants 7(3):75

    Article  CAS  PubMed Central  Google Scholar 

  • Gao W, Feng Z, Bai Q, HeWang JY (2019) Melatonin-mediated regulation of growth and antioxidant capacity in salt-tolerant naked oat under salt stress. Int J Mol Sci 20:1176

    Article  CAS  PubMed Central  Google Scholar 

  • Hasan MK, Ahammed GJ, Sun SC, Li MQ, Yin HQ, Zhou J (2019) Melatonin inhibits cadmium translocation and enhances plant tolerance by regulating sulfur uptake and assimilation in Solanum lycopersicum L. J Agric Food Chem 67(38):10563–10576

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Huang YX, Zhou SX, Zhang YQ, Cheng RS, Guo JF, Ling Y (2020) Traditional rice landraces in Lei-Qiong area of South China tolerate salt stress with strong antioxidant activity. Plant Signal Behav 15(4):1740466

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hussain S, Zhang JH, Zhong C, Zhu LF, Cao XC, Yu SM, Allen BJ, Hu JJ, Jin QY (2017) Effects of salt stress on rice growth, development characteristics, and the regulating ways: a review. J Integr Agric 16:235–2374

    Article  Google Scholar 

  • Hussain M, Ahmad S, Hussain S, Lal R, Ul-Allah S, Nawaz A (2018a) Rice in saline soils: physiology, biochemistry, genetics, and management. Adv Agron 148:231–287

    Article  Google Scholar 

  • Hussain S, Khaliq A, Tanveer M, Matloob A, Hussain HA (2018b) Aspirin priming circumvents the salinity-induced effects on wheat emergence and seedling growth by regulating starch metabolism and antioxidant enzyme activities. Acta Physiol Plant 40:68

    Article  CAS  Google Scholar 

  • Islam MA, Shelia V, Ludwig F, de Bruyn LL, Rahman MHU, Hoogenboom G (2021) Bringing farmers’ perceptions into science and policy: understanding salinity tolerance of rice in southwestern Bangladesh under climate change. Land Use Policy 101:105159

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jouve L, Jacques D, Douglas GC, Hoffmann L, Hausman JF (2007) Biochemical characterization of early and late bud flushing in common ash (Fraxinus excelsior L.). Plant Sci 172:962–969

    Article  CAS  Google Scholar 

  • Kaya C, Okant M, Ugurlar F, Alyemeni MN, Ashraf M, Ahmad P (2019) Melatonin-mediated nitric oxide improves tolerance to cadmium toxicity by reducing oxidative stress in wheat plants. Chemosphere. https://doi.org/10.1016/j.chemosphere.2019.03.026

    Article  PubMed  Google Scholar 

  • Kaya C, Higgs D, Ashraf M, Alyemeni MN, Ahmad P (2020) Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) plants to iron deficiency and salt stress alone or in combination. Physiol Plant 168(2):256–277

    CAS  PubMed  Google Scholar 

  • Khan MHU, Khattak JZK, Jamil M, Malook I, Khan SU, Jan M, Din I, Saud S, Kamran M, Alharby H, Fahad S (2017) Bacillus safensis with plant-derived smoke stimulates rice growth under saline conditions. Environ Sci Pollut Res 24:23850–23863

    Article  CAS  Google Scholar 

  • Khan I, Raza MA, Awan SA, Shah GA, Rizwan M, Ali B, Tariq R, Hassan MJ, Alyemeni MN, Brestic M, Zhang XQ, Ali S, Huang LK (2020) Amelioration of salt induced toxicity in pearl millet by seed priming with silver nanoparticles (AgNPs): the oxidative damage, antioxidant enzymes and ions uptake are major determinants of salt tolerant capacity. Plant Physiol Biochem 156:221–232

    Article  CAS  PubMed  Google Scholar 

  • Li J, Jia H, Wang J, Cao Q, Wen Z (2014) Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na+/H+ antiporter system in the hydrogen peroxide-dependent manner in salt-stress Arabidopsis thaliana root. Protoplasma 251:899–912

    Article  CAS  PubMed  Google Scholar 

  • Li C, Liang B, Chang C, Wei Z, Zhou S, Ma F (2016) Exogenous melatonin improved potassium content in Malus under different stress conditions. J Pineal Res 61:218–229

    Article  PubMed  CAS  Google Scholar 

  • Li H, Chang JJ, Chen HJ, Wang ZY, Gu XR, Wei CH, Zhang Y, Ma JF, Yang JQ, Zhang X (2017a) Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00295

    Article  PubMed  PubMed Central  Google Scholar 

  • Li X, Yu B, Cui Y, Yin Y (2017b) Melatonin application confers enhanced salt tolerance by regulating Na+ and Cl accumulation in rice. Plant Growth Regul 83:441–454

    Article  CAS  Google Scholar 

  • Li J, Liu J, Zhu T, Zhao C, Li L, Chen M (2019) The role of melatonin in salt stress responses. Int J Mol Sci 20(7):1735

    Article  CAS  PubMed Central  Google Scholar 

  • Li X, Ahammed GJ, Zhang XN, Zhang L, Yan P, Zhang LP, Fu JY, Han WY (2021) Melatonin- mediated regulation of anthocyanin biosynthesis and antioxidant defense confer tolerance to arsenic stress in Camellia sinensis L. J Hazard Mater 403:123922

    Article  CAS  PubMed  Google Scholar 

  • Liang CZ, Zheng GY, Li WZ, Wang YQ, Hu B, Wang HR, Wu HK, Qian YW, Zhu XG, Tan DX, Chen SY, Chu CC (2015) Melatonin delays leaf senescence and enhances salt stress tolerance in rice. J Pineal Res 59:91–101

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Li DQ, Chen YX, Cheng JP, Zhao G, Fahima T, Yan J (2020) Selenium mitigates salt-induced oxidative stress in durum wheat (Triticum durum Desf.) seedlings by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. 3 Biotech 10(8):368

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu N, Gong B, Jin Z, Wang X, Wei M, Yang F, Li Y, Shi QH (2015) Sodic alkaline stress mitigation by exogenous melatonin in tomato needs nitric oxide as a downstream signal. J Plant Physiol 186:68–77

    Article  PubMed  CAS  Google Scholar 

  • Nawaz K, Chaudhary R, Sarwar A, Ahmad B, Gul A, Hano C, Abbasi BH, Anjum S (2021) Melatonin as master regulator in plant growth, development and stress alleviator for sustainable agricultural production: current status and future perspectives. Sustainability 13(1):294

    Article  Google Scholar 

  • Qi ZY, Wang KX, Yan MY, Kanwar MK, Li DY, Wijaya L, Alyemeni MN, Ahamd P, Zhou J (2018) Melatonin alleviates high temperature-induced pollen abortion in Solanum lycopersicum. Molecules 23:386

    Article  PubMed Central  CAS  Google Scholar 

  • Rattan A, Kapoor D, Kapoor N, Bhardwaj R, Sharma A (2020) Brassinosteroids regulate functional components of antioxidative defense system in salt stressed maize seedlings. J Plant Growth Regul 39(4):1465–1475

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui MH, Alamri S, Al-Khaishany MY, Khan MN, Al-Amri A, Ali HM, Alaraidh IA, 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

    Article  PubMed Central  CAS  Google Scholar 

  • Siddiqui MH, Alamri S, Khan MN, Corpas FJ, Ahmad P (2020) Melatonin and calcium function synergistically to promote the resilience through ROS metabolism under arsenic-induced stress. J Hazard Mater 398:122882

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66:695–707

    Article  CAS  PubMed  Google Scholar 

  • Wen C, Dong A, Li G, Lei S, Lei Y (2005) Determination of total sugar and reducing sugar in Viola Philippicassp Munda W. Becker by anthrone colorimetry. Mod Food Sci Technol 21:122–124

    Google Scholar 

  • Wu Y, Gao Q, Huang S, Jia S (2019) Enhancing salt tolerance in melon by application of exogenous melatonin and Ca2+. Pak J Bot 51:781–787

    Article  CAS  Google Scholar 

  • Yan GC, Fan XP, Peng M, Yin C, Xiao ZX, Liang YC (2020) Silicon improves rice salinity resistance by alleviating ionic toxicity and osmotic constraint in an organ-specific pattern. Front Plant Sci 11:260

    Article  PubMed  PubMed Central  Google Scholar 

  • Yasmeen A, Basra SMA, Wahid A, Nouman W, Rehman H (2013) Exploring the potential of Moringa oleifera leaf extract (MLE) as a seed priming agent in improving wheat performance. Turk J Bot 37:512–520

    CAS  Google Scholar 

  • Yi Z, Li S, Liang Y, Zhao H, Hou L, Yu S, Ahammed GJ (2018) Effects of exogenous spermidine and elevated CO2 on physiological and biochemical changes in tomato plants under iso-osmotic salt stress. J Plant Growth Regul 37:1222–1234

    Article  CAS  Google Scholar 

  • Yu YC, Wang AM, Li X, Kou M, Wang WJ, ChenXY XuT, Zhu MK, Ma DF, Li ZY, 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. Front Plant Sci 9:256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zafar S, Hasnain Z, Anwar S, Perveen S, Iqbal N, Noman A (2019) Influence of melatonin on antioxidant defense system and yield of wheat (Triticum aestivum L.) genotypes under saline condition. Pak J Bot 51:1987–1994

    CAS  Google Scholar 

  • 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 Physiol Biochem 149:313–323

    Article  CAS  PubMed  Google Scholar 

  • Zellener W, Tubana B, Rodrigues FA, Datnoff LE (2021) Silicon’s role in plant stress reduction and why this element is not used routinely for managing plant health. Plant Dis. https://doi.org/10.1094/PDIS-08-20-1797-FE

    Article  Google Scholar 

  • Zeng L, CaiJS LJJ, 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 Integr Agric 17:328–335

    Article  CAS  Google Scholar 

  • Zhang HJ, Zhang N, Yang RC, Wang L, Sun QQ, Li DB, Cao YY, Weeda S, Zhao B, Ren SX, Guo YD (2014) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA(4) interaction in cucumber (Cucumis sativus L.). J Pineal Res 57:269–279

    Article  CAS  PubMed  Google Scholar 

  • Zhang N, ZhangHJ SQQ, Cao YY, Li XS, Zhao B, Wu P, Guo YD (2017) Proteomic analysis reveals a role of melatonin in promoting cucumber seed germination under high salinity by regulating energy production. Sci Rep 7:503

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao G, Yu XL, Lou W, Wei SQ, Wang R, Wan Q, Shen WB (2019) Transgenic Arabidopsis overexpressing MsSNAT enhances salt tolerance via the increase in autophagy, and the reestablishment of redox and ion homeostasis. Environ Exp Bot 164:20–28

    Article  CAS  Google Scholar 

  • Zheng QS, Liu L, Liu ZP, Chen JM, Zhao GM (2009) Comparison of the response of ion distribution in the tissues and cells of the succulent plants Aloe vera and Salicornia europaea to saline stress. J Plant Nutr Soil Sci 172:875–883

    Article  CAS  Google Scholar 

  • Zhu YX, Gong HJ, Yin J (2019) Role of silicon in mediating salt tolerance in plants: a review. Plants 8:147

    Article  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by Grants from the “National Natural Science Foundation of China (31672141),” “Open Foundation of Key Laboratory of Crop Genetics and Physiology of Jiangsu Province (YCSL201902),” “Key Research and Development Projects of Jiangsu Province (BE2018680),” “Research and Development Projects of Taizhou Science and Technology (SNY20190077),” and “Training Programs of Innovation and Entrepreneurship for Undergraduates of Nanjing Agricultural University (1913C19).”

Author information

Authors and Affiliations

Authors

Contributions

Long Wei, Baoxiang Wang, Chaoqiang Jiang and Qingsong Zheng planned and designed the research. Long Wei, Haiyan Zhao, Xinyi Wu, Rujia Lan, Xu Huang, Bo Chen, Jinlan Wang and Yan Liu performed the experiments and data analysis. Gang Chen reviewed and edited the manuscript and procured funding. Long Wei, Haiyan Zhao, Xinyi Wu and Baoxiang Wang wrote the manuscript. Qingsong Zheng performed project administration, execution of the experiment, reviewed and edited the manuscript, and procured funding.

Corresponding author

Correspondence to Qingsong Zheng.

Additional information

Handling Editor: Mikihisa Umehara.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, L., Zhao, H., Wang, B. et al. Exogenous Melatonin Improves the Growth of Rice Seedlings by Regulating Redox Balance and Ion Homeostasis Under Salt Stress. J Plant Growth Regul 41, 2108–2121 (2022). https://doi.org/10.1007/s00344-021-10417-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-021-10417-z

Keywords

Navigation