Abstract
Melatonin (MT) and salicylic acid (SA) are known to improve plant tolerance to environmental stresses; however, no reports have evaluated the effect of their combined treatment on plants under both normal and stressful conditions. For the first time, the present study aimed to investigate MT and SA’s potential role in regulating polyamine and nitrogen metabolism in wheat plants subjected to salty soils, and counterbalancing oxidative damage induced by salt stress. Moreover, this research aimed to elucidate a possible link between melatonin, salicylic acid, nitrogen and polyamine levels. Wheat (Triticum aestivum L. cv. Sids 14) plants were grown under non-saline or saline conditions (6.0 and 12.0 dS m–1) and were foliar sprayed with 70 µM MT and/or 75 mg l−1 SA. The injury impacts of salt stress on wheat growth and production were significantly alleviated by exogenous MT and/or SA treatments. This was evidenced by increasing polyamines content through accelerating the metabolic flow from the precursor amino acids arginine and methionine to polyamines, decreasing the polyamines degradation, and enhancing the polyamines biosynthesis. Furthermore, MT and/or SA are involved in promoting nitrogen metabolism through up-regulating the activities of N uptake and metabolism related enzymes (nitrate reductase, nitrite reductase, glutamine synthetase, glutamate synthase) as well as enhancing the content of nitrogen, nitrate and protein in salt-stressed plants. The mitigation was also detected in reduced lipid peroxidation, hydrogen peroxide content, carbonyl content, and protease activity in stressed treated plants. Notably, the best response was registered for the combined treatment of MT and SA. Therefore, the co-application of MT and SA is a promising way for ameliorating salt toxicity in sustainable agricultural systems.
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References
Aghdam MS, Luo ZS, Jannatizadeh A, Sheikh-Assadi M, Sharafi Y, Farmani B, Fard JR, Razavi F (2019) Employing exogenous melatonin applying confers chilling tolerance in tomato fruits by upregulating ZAT2/6/12 giving rise to promoting endogenous polyamines, proline, and nitric oxide accumulation by triggering arginine pathway activity. Food Chem 275:549–556. https://doi.org/10.1016/j.foodchem.2018.09.157
Ahmad S, Cui W, Kamran M, Ahmad I, Meng X, Wu X, Su W, Javed T, El-Serehy HA, Jia Z, Han Q (2021) 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. https://doi.org/10.1007/s00344-020-10187-0
Albacete A (2020) Get together: the interaction between melatonin and salicylic acid as a strategy to improve plant stress tolerance. Agronomy 10:1486. https://doi.org/10.3390/agronomy10101486
Arnao MB, Hernández-Ruiz J (2019) 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
Asthir B, Duffus CM, Smith RC, Spoor W (2002) Diamine oxidase is involved in H2O2 production in the chalazal cells during barley grain filling. J Exp Bot 53:677–682. https://doi.org/10.1093/jexbot/53.369.677
Bose SK, Howlader P (2020) Melatonin plays multifunctional role in horticultural crops against environmental stresses: a review. Environ Exp Bot 176:104063. https://doi.org/10.1016/j.envexpbot.2020.104063
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 7:248–254. https://doi.org/10.1006/abio.1976.9999
Bukhat S, Manzoor H, Athar H, Zafar ZU, Azeem F, Rasul S (2020) Salicylic acid induced photosynthetic adaptability of Raphanus sativus to salt stress is associated with antioxidant capacity. J Plant Growth Regul 39:809–822. https://doi.org/10.1007/s00344-019-10024-z
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. https://doi.org/10.1016/j.hpj.2019.01.002
Cottenie A, Verloo M, Kiekens L, Velghe G, Camerlynck R (1982) Chemical analysis of plants and soils. In: Laboratory of analytical and agrochemistry. State University, Ghent, pp 14–24. https://lib.ugent.be/catalog/rug01:000239299
Drapeau G (1974) Protease from Staphylococcus aureus. In: Lorand L (ed) Methods in enzymology, vol 45b. Academic Press, New York
Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635. https://doi.org/10.1016/j.jplph.2007.11.006
Es-sbihi FZ, Hazzoumi Z, Aasfar A, Joutei KA (2021) Improving salinity tolerance in Salvia officinalis L. by foliar application of salicylic acid. Chem Biol Technol Agric 8:25. https://doi.org/10.1186/s40538-021-00221-y
Faraz A, Faizan M, Sami F, Siddiqui H, Hayat S (2020) Supplementation of salicylic acid and citric acid for alleviation of cadmium toxicity to Brassica juncea. J Plant Growth Regul 39:641–655. https://doi.org/10.1007/s00344-019-10007-0
Fuertes-Mendizábal T, Bastías EI, González-Murua C, González-Moro M (2020) Nitrogen assimilation in the highly salt- and boron-tolerant ecotype Zea mays L. Amylacea. Plants 9:322. https://doi.org/10.3390/plants9030322
Gao Q, Jia S, Miao Y, Lu X, Li H (2016) Effects of exogenous melatonin on nitrogen metabolism and osmotic adjustment substances of melon seedlings under sub-low temperature. Chin J Appl Ecol 27:519–524. https://doi.org/10.13287/j.1001-9332.201602.016
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 20:1176. https://doi.org/10.3390/ijms20051176
Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F, Raza A, Mohsin SM, Al Mahmud J, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9:681. https://doi.org/10.3390/antiox9080681
Hoang HL, de Guzman CC, Cadiz NM, Hoang TTH, Tran DH, Rehman H (2020) Salicylic acid and calcium signaling induce physiological and phytochemical changes to improve salinity tolerance in red amaranth (Amaranthus tricolor L.). J Soil Sci Plant Nutr 20:1759–1769. https://doi.org/10.1007/s42729-020-00248-4
Högberg P, Granström A, Johansson T, LundmarkThelin A, Näsholm T (1986) Plant nitrate reductase activity as an indicator of availability of nitrate in forest soils. Can J For Res 16:1165–1169. https://doi.org/10.1139/x86-207
Hussain SJ, Khan NA, Anjum NA, Masood A, Khan MIR (2021) Mechanistic elucidation of salicylic acid and sulphur–induced defence systems, nitrogen metabolism, photosynthetic, and gowth potential of mungbean (Vigna radiata) under salt stress. J Plant Growth Regul 40:1000–1016. https://doi.org/10.1007/s00344-020-10159-4
Igarashi K, Kashiwagi K (2019) The functional role of polyamines in eukaryotic cells. Int J Biochem Cell Biol 107:104–115. https://doi.org/10.1016/j.biocel.2018.12.012
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
Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020) The role of endogenous nitric oxide in salicylic acid-induced up-regulation of ascorbate-glutathione cycle involved in salinity tolerance of pepper (Capsicum annuum L.) plants. Plant Physiol Biochem 147:10–20. https://doi.org/10.1016/j.plaphy.2019.11.040
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
Khan A, Numan M, Khan AL, Lee I, Imran M, Asaf S, Al-Harrasi AA (2020) Melatonin: awakening the defense mechanisms during plant oxidative stress. Plants 9:407. https://doi.org/10.3390/plants9040407
Liang B, Ma C, Zhang Z, Wei Z, Gao T, Zhao Q, Ma F, Li C (2018) Long-term exogenous application of melatonin improves nutrient uptake fluxes in apple plants under moderate drought stress. Environ Exp Bot 155:650–661. https://doi.org/10.1016/j.envexpbot.2018.08.016
Lin CC, Kao CH (1996) Disturbed ammonium assimilation is associated with growth inhibition of roots in rice seedlings caused by NaCl. Plant Growth Regul 18:233–238. https://doi.org/10.1007/BF00024387
Lowry OH, Rosenbrough NJ, Aarr AL, Randaal RJ (1951) Protein measurement with Folin phenol reagent. J Biol Chem 193:265–275. https://doi.org/10.1016/S0021-9258(19)52451-6
Ma L, Huang Z, Li S, Ashraf U, Yang W, Liu H, Xu D, Li W, Mo Z (2021) Melatonin and nitrogen applications modulate early growth and related physio-biochemical attributes in maize under Cd stress. J Soil Sci Plant Nutr 21:978–990. https://doi.org/10.1007/s42729-021-00415-1
Morton JL, Awila M, Al-Tamimi N, Saade S, Pailles Y, Negrão S, Tester M (2019) Salt stress under the scalpel-dissecting the genetics of salt tolerance. Plant J 97:148–163. https://doi.org/10.1111/tpj.14189
Naka Y, Watanabe K, Sagor GHM, Niitsu M, Pillai MA, Kusano T, Takahashi Y (2010) Quantitative analysis of plant polyamines including thermospermine during growth and salinity stress. Plant Physiol Biochem 48:527–533. https://doi.org/10.1016/j.plaphy.2010.01.013
Nawaz MA, Jiao Y, Chen C, Shireen F, Zheng Z, Imtia M, Bie Z, Huang Y (2018) Melatonin pretreatment improves vanadium stress tolerance of watermelon on 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
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279. https://doi.org/10.1146/annurev.arplant.49.1.249
Pregl F (1945) Quantitative organic microanalysis, 4th edn. A. Churchill Ltd., London
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
Rady MM, Talaat NB, Abdelhamid MT, Shawky BT, Desoky EM (2019) Maize (Zea mays L.) grains extract mitigates the deleterious effects of salt stress on common bean (Phaseolus vulgaris L.) growth and physiology. J Hortic Sci Biotech 94:777–789. https://doi.org/10.1080/14620316.2019.1626773
Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363. https://doi.org/10.1016/S0076-6879(94)33041-7
Seith B, Setzer B, Flaig H, Mohr H (2010) Appearance of nitrate reductase, nitrite reductase and glutamine synthetase in different organs of the Scots pine (Pinus sylvestris) seedling as affected by light, nitrate and ammonium. Physiol Plant 91:419–426. https://doi.org/10.1111/j.1399-3054.1994.tb02969.x
Shafi A, Singh AK, Zahoor I (2021) Melatonin: role in abiotic stress resistance and tolerance. In: Aftab T, Hakeem KR (eds) Plant growth regulators. Springer, Cham, pp 239–273
Shamili M, Ghalati RE, Samari F (2021) The impact of foliar salicylic acid in salt-exposed guava (Psidium Guajava L.) seedlings. Int J Fruit Sci 21:323–333. https://doi.org/10.1080/15538362.2021.1887050
Sharma A, Sidhu GPS, Araniti F, Bali AS, Shahzad B, Tripathi DK, Brestic M, Skalicky M, Landi M (2020) The role of salicylic acid in plants exposed to heavy metals. Molecules 25:540. https://doi.org/10.3390/molecules25030540
Singh JP (1988) A rapid method for determination of nitrate in soil and plant extracts. Plant Soil 110:137–139. https://doi.org/10.1007/BF02143549
Takahashi Y, Tahara M, Yamada Y, Mitsudomi Y, Koga K (2018) Characterization of the polyamine biosynthetic pathways and salt stress response in Brachypodium distachyon. J Plant Growth Regul 37:625–634. https://doi.org/10.1007/s00344-017-9761-z
Talaat NB (2015) Effective microorganisms modify protein and polyamine pools in common bean (Phaseolus vulgaris L.) plants grown under saline conditions. Sci Hortic 190:1–10. https://doi.org/10.1016/j.scienta.2015.04.005
Talaat NB (2019a) Role of reactive oxygen species signaling in plant growth and development. In: Hasanuzzaman M, Fotopoulos V, Nahar K, Fujita M (eds) Reactive oxygen, nitrogen and sulfur species in plants: production, metabolism, signaling and defense mechanisms. Wiley, Oxford, pp 225–266. https://doi.org/10.1002/9781119468677.ch10
Talaat NB (2019b) Abiotic stresses-induced physiological alteration in wheat. In: Hasanuzzaman M, Nahar K, Hossain A (eds) Wheat production in changing environments—responses, adaptation and tolerance. Springer, Singapore, pp 1–30. https://doi.org/10.1007/978-981-13-6883-7_1
Talaat NB, Shawky BT (2013) Modulation of nutrient acquisition and polyamine pool in salt-stressed wheat (Triticum aestivum L.) plants inoculated with arbuscular mycorrhizal fungi. Acta Physiol Plant 35:2601–2610. https://doi.org/10.1007/s11738-013-1295-9
Talaat NB, Shawky BT (2016) Dual application of 24-epibrassinolide and spermine confers drought stress tolerance in maize (Zea mays L.) by modulating polyamine and protein metabolism. J Plant Growth Regul 35:518–533. https://doi.org/10.1007/s00344-015-9557-y
Talaat NB, Ghoniem AE, Abdelhamid MT, Shawky BT (2015) Effective microorganisms improve growth performance, alter nutrients acquisition and induce compatible solutes accumulation in common bean (Phaseolus vulgaris L.) plants subjected to salinity stress. Plant Growth Regul 75:281–295. https://doi.org/10.1007/s10725-014-9952-6
Todorova D, Talaat NB, Katerova Z, Alexieva V, Shawky BT (2016) Polyamines and brassinosteroids in drought stress responses and tolerance in plants. In: Ahmad P (ed) Water stress and crop plants: a sustainable approach, vol 2. Wiley, Oxford, pp 608–627
Wang L, Zhou Q, Ding L, Sun Y (2008) Effect of cadmium toxicity on nitrogen metabolism in leaves of Solanum nigrum L. as a newly found cadmium hyperaccumulator. J Hazard Mater 154:818–825. https://doi.org/10.1016/j.hazmat.2007.10.097
Wang D, Li L, Xu YQ, Limwachiranon J, Li D, Ban ZJ, Luo ZS (2017) Effect of exogenous nitro oxide on chilling tolerance, polyamine, proline and γ-aminobutyric acid in bamboo shoots (Phyllostachys praecox f. prevernalis). J Agric Food Chem 65:5607–5613. https://doi.org/10.1021/acs.jafc.7b02091
Yan F, Wei H, Ding Y, Li W, Liu Z, Chen L, Tang S, Ding C, Jiang Y, Li G (2021) Melatonin regulates antioxidant strategy in response to continuous salt stress in rice seedlings. Plant Physiol Biochem 165:239–250. https://doi.org/10.1016/j.plaphy.2021.05.003
Zahedi SM, Hosseini MS, Abadia 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. https://doi.org/10.1016/j.plaphy.2020.02.021
Zhang Q, Liu X, Zhang Z, Liu N, Li D, Hu L (2019) 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
Zörb C, Geilffus CM, Dietz KJ (2019) Salinity and crop yield. Plant Biol 21:31–38. https://doi.org/10.1111/plb.12884
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This research was supported by the Academy of Scientific Research and Technology in Egypt and the Bulgaria-Egypt Joint Research Project.
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NBT: conceived the idea, designed the experiment, carried out the experiments, generated the data, analyzed the data and wrote the manuscript.
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Talaat, N.B. Polyamine and nitrogen metabolism regulation by melatonin and salicylic acid combined treatment as a repressor for salt toxicity in wheat (Triticum aestivum L.) plants. Plant Growth Regul 95, 315–329 (2021). https://doi.org/10.1007/s10725-021-00740-6
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DOI: https://doi.org/10.1007/s10725-021-00740-6