Elucidating the role of melatonin or sugar beet pulp pellet in physiological improvement characteristics and promoting the growth of Moringa oleifera under lead stress


  • Marwa F. EL-SAKAAN Mansoura University, Faculty of Science, Botany Department (EG)
  • Mahmoud E. YOUNIS Mansoura University, Faculty of Science, Botany Department (EG)
  • Wafaa M. SHUKRY Mansoura University, Faculty of Science, Botany Department (EG)




electrolyte leakage, lipid peroxidation, mineral content, phytoremediation


Pot experiments were conducted to evaluate the effect of root and foliar uptake of Pb on Moringa oleifera plants. The levels of Pb used in the experiments were 100 and 400 ppm Pb. The lead application affected the growth, photosynthetic pigment, carbohydrates, proline, oxidative stress biomarkers, mineral contents, and Pb accumulation in Moringa plants. The growth parameters, chlorophyll, Na, K, and Ca content declined in the case of soil or foliar Pb application. The foliar lead application revealed a more negative effect on the growth of moringa plants than the soil application. However, Pb-stressed moringa plants increased carbohydrates, proline, H2O2, MDA, electrolyte leakage, Pb, and Mg content. In addition, the possible role of melatonin (MEL) and sugar beet pulp pellets (SBP) in ameliorating lead toxicity and enhancement of phytoremediation was investigated. It was found that supplemental addition of MEL or SBP increases the growth parameters, photosynthetic pigments, carbohydrates, proline, and minerals compared to stressed moringa plants. Moreover, a decrease in hydrogen peroxide, lipid peroxidation, and electrolyte leakage was observed under MEL and SBP treatments. The ameliorating effect of SBP was more pronounced than that of MEL. Furthermore, MEL application enhanced the phytoremediation capacity of moringa plants.


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Abbas G, Murtaza B, Bibi I, Shahid M, Niazi NK, Khan MI, Amjad M, Hussain M (2018). Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. International Journal of Environmental Research and Public Health 15:59. https://doi.org/10.3390/ijerph15010059 DOI: https://doi.org/10.3390/ijerph15010059

Abu-Shahba MS, Mansour MM, Mohamed HI, Sofy MR (2022). Effect of biosorptive removal of cadmium ions from hydroponic solution containing indigenous garlic peel and mercerized garlic peel on lettuce productivity. Scientia Horticulturae 293:110727. https://doi.org/10.1016/j.scienta.2021.110727 DOI: https://doi.org/10.1016/j.scienta.2021.110727

Ahammed GJ, Wu M, Wang Y, Yan Y, Mao Q, Ren J, Ma R, Liu A, Chen S (2020). Melatonin alleviates iron stress by improving iron homeostasis, antioxidant defense and secondary metabolism in cucumber. Scientia Horticulturae 265:109205. https://doi.org/10.1016/j.scienta.2020.109205. DOI: https://doi.org/10.1016/j.scienta.2020.109205

Ahammed GJ, Xu W, Liu A, Chen S (2019). Endogenous melatonin deficiency aggravates high temperature-induced oxidative stress in Solanum lycopersicum L Environmental and Experimental Botany 161:303-311. https://doi.org/10.1016/j.envexpbot.2018.06.006 DOI: https://doi.org/10.1016/j.envexpbot.2018.06.006

Alexieva V, Sergiev I, Mapelli S, Karanov E (2001). The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat Plant, Cell & Environment 24:1337-1344. https://doi.org/10.1046/j.1365-3040.2001.00778.x DOI: https://doi.org/10.1046/j.1365-3040.2001.00778.x

Ali B, Mwamba TM, Gill R A, Yang C, Ali S, Daud MK, Wu Y, Zho W (2014b). Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regulation 74:261-273. https://doi.org/10.1007/s10725-014-9917-9 DOI: https://doi.org/10.1007/s10725-014-9917-9

Alkhatib R, Alkhatib B, Al-Quraan N, Al-Eitan L, Abdo N, Muhaidat R (2016). Impact of exogenous caffeine on morphological, biochemical, and ultrastructural characteristics of Nicotiana tabacum. Biologia Plantarum 60:706-714. https://doi.org/10.1007/s10535-016-0600-z DOI: https://doi.org/10.1007/s10535-016-0600-z

Alkhatib R, Mheidat M, Abdo N, Tadros M, Al‐Eitan L, Al‐Hadid K (2019). Effect of lead on the physiological, biochemical and ultrastructural properties of Leucaena leucocephala. Plant Biology 21:1132-1139. https://doi.org/10.1111/plb.13021 DOI: https://doi.org/10.1111/plb.13021

Anli M, Baslam M, Tahiri A, Raklami A, Symanczik S, Boutasknit A, … Rahou YA (2020). Biofertilizers as strategies to improve photosynthetic apparatus, growth, and drought stress tolerance in the date palm. Frontiers in Plant Science 11. https://doi.org/10.3389/fpls.2020.516818 DOI: https://doi.org/10.3389/fpls.2020.516818

Arnao MB (2014). Phytomelatonin: discovery, content, and role in plants. Advances in Botany 2014:1-11. http://dx.doi.org/10.1155/2014/815769 DOI: https://doi.org/10.1155/2014/815769

Arnao MB, Hernández‐Ruiz J (2007). Melatonin promotes adventitious‐and lateral root regeneration in etiolated hypocotyls of Lupinus albus L. Journal of Pineal Research 42:147-152. https://doi.org/10.1111/j.1600-079X.2006.00396.x DOI: https://doi.org/10.1111/j.1600-079X.2006.00396.x

Arya SK, Basu A, Mukherjee A (2013). Lead induced genotoxicity and cytotoxicity in root cells of Allium cepa and Vicia faba. The Nucleus 56:183-189. https://doi.org/10.1007/s13237-013-0099-z DOI: https://doi.org/10.1007/s13237-013-0099-z

Ashraf M (2009). Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnology Advances 27:84-93. https://doi.org/10.1016/j.biotechadv.2008.09.003 DOI: https://doi.org/10.1016/j.biotechadv.2008.09.003

Ashraf M, Foolad MR (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59:206-216. https://doi.org/10.1016/j.envexpbot.2005.12.006 DOI: https://doi.org/10.1016/j.envexpbot.2005.12.006

Azeez L, Adejumo AL, Lateef A, Adebisi SA, Adetoro RO, Adewuyi SO, Tijani KO, Olaoye S (2019). Zero-valent silver nanoparticles attenuate Cd and Pb toxicities on Moringa oleifera via immobilization and induction of phytochemicals. Plant Physiology and Biochemistry 139:283-292. https://doi.org/10.1016/j.plaphy.2019.03.030 DOI: https://doi.org/10.1016/j.plaphy.2019.03.030

Azooz MM, Abou-Elhamd MF, Al-Fredan MA (2012). Biphasic effect of copper on growth, proline, lipid peroxidation and antioxidant enzyme activities of wheat (Triticum aestivum cv. Hasaawi) at early growing stage. Australian Journal of Crop Science 6:688-694.

Back K, Tan DX, Reiter RJ (2016). Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. Journal of Pineal Research 61:426-437. https://doi.org/10.1111/jpi.12364 DOI: https://doi.org/10.1111/jpi.12364

Balibrea ME, Dell'Amico J, Bolarín MC, Pérez‐Alfocea F (2000). Carbon partitioning and sucrose metabolism in tomato plants growing under salinity. Physiologia Plantarum 110:503-511. https://doi.org/10.1111/j.1399-3054.2000.1100412.x DOI: https://doi.org/10.1111/j.1399-3054.2000.1100412.x

Bates LS, Waldren RP, Teare I (1973). Rapid determination of free proline for water-stress studies. Plant and Soil 39:205-207. https://doi.org/10.1007/BF00018060 DOI: https://doi.org/10.1007/BF00018060

Campos CN, Ávila RG, de Souza KRD, Azevedo LM, Alves JD (2019). Melatonin reduces oxidative stress and promotes drought tolerance in young Coffea arabica L. plants. Agricultural Water Management 211:37-47. https://doi.org/10.1016/j.agwat.2018.09.025 DOI: https://doi.org/10.1016/j.agwat.2018.09.025

Caravaca F, Alguacil M, Azcón R, Parladé J, Torres P, Roldán A (2005). Establishment of two ectomycorrhizal shrub species in a semiarid site after in situ amendment with sugar beet, rock phosphate, and Aspergillus niger. Microbial Ecology 49:73-82. https://doi.org/10.1007/s00248-003-0131-y DOI: https://doi.org/10.1007/s00248-003-0131-y

Chadzinikolau T, Kozłowska M, Mleczek M (2017). Induction of phytochelatins and flavonoids in cadmium polluted Berberis thunbergii. Dendrobiology 77:139-146. https://doi.org/10.12657/denbio.077.011 DOI: https://doi.org/10.12657/denbio.077.011

Chibnall A, Rees M, Williams E (1943). The dicarboxylic and basic amino-acids of edestin, egg albumin and β-lactoglobulin. Biochemical Journal 37:372-388. https://doi.org/10.1042/bj0370372 DOI: https://doi.org/10.1042/bj0370372

Choi GH, Lee HY, Back K (2017). Chloroplast overexpression of rice caffeic acid O‐methyltransferase increases melatonin production in chloroplasts via the 5‐methoxytryptamine pathway in transgenic rice plants. Journal of Pineal Research 63:e12412. https://doi.org/10.1111/jpi.12412 DOI: https://doi.org/10.1111/jpi.12412

Choudhury N, Behera R (2001). Photoinhibition of photosynthesis: role of carotenoids in photoprotection of chloroplast constituents. Photosynthetica 39:481-488. https://doi.org/10.1023/A:1015647708360 DOI: https://doi.org/10.1023/A:1015647708360

Cole IB, Cao J, Alan AR, Saxena PK, Murch SJ (2008). Comparisons of Scutellaria baicalensis, Scutellaria lateriflora and Scutellaria racemosa: genome size, antioxidant potential and phytochemistry. Planta Medica 74:474-481. https://doi.org/10.1055/s-2008-1034358 DOI: https://doi.org/10.1055/s-2008-1034358

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 Physiolgical Biochemistry 118:138-149. https://doi.org/10.1016/j.plaphy.2017.06.014 DOI: https://doi.org/10.1016/j.plaphy.2017.06.014

Dalyan E, Yüzbaşıoğlu E, Akpınar I (2018). Effect of 24-epibrassinolide on antioxidative defence system against lead-induced oxidative stress in the roots of Brassica juncea L. seedlings. Russian Journal of Plant Physiology 65:570-578. https://doi.org/10.1134/S1021443718040118 DOI: https://doi.org/10.1134/S1021443718040118

Dawood MF, Abu-Elsaoud AM, Sofy MR, Mohamed HI, Soliman MH (2022). Appraisal of kinetin spraying strategy to alleviate the harmful effects of UVC stress on tomato plants. Environmental Science and Pollution Research:1-21. https://doi.org/10.1007/s11356-022-19378-6 DOI: https://doi.org/10.1007/s11356-022-19378-6

Dey U, Mondal NK (2016). Ultrastructural deformation of plant cell under heavy metal stress in Gram seedlings Cogent. Environmental Science 2:1196472. https://doi.org/10.1080/23311843.2016.1196472 DOI: https://doi.org/10.1080/23311843.2016.1196472

Dhanapackiam S, Ilyas M (2010). Effect of salinity on chlorophyll and carbohydrate contents of Sesbania grandiflora seedlings Indian Journal of Science and Technology 3:64-66. DOI: https://doi.org/10.17485/ijst/2010/v3i1.20

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. Journal of Pineal Research 18:28-31. https://doi.org/10.1111/j.1600-079X.1995.tb00136.x DOI: https://doi.org/10.1111/j.1600-079X.1995.tb00136.x

El-Sheshtawy HS, Mahdy HM, Sofy AR, Sofy MR (2022). Production of biosurfactant by Bacillus megaterium and its correlation with lipid peroxidation of Lactuca sativa. Egyptian Journal of Petroleum 31:1-6. https://doi.org/10.1016/j.ejpe.2022.03.001 DOI: https://doi.org/10.1016/j.ejpe.2022.03.001

El-Sheshtawy HS, Sofy MR, Ghareeb DA, Yacout GA, Eldemellawy MA, Ibrahim BM (2021). Eco-friendly polyurethane acrylate (PUA)/natural filler-based composite as an antifouling product for marine coating. Applied Microbiology and Biotechnology 105:7023-7034. https://doi.org/10.1007/s00253-021-11501-w DOI: https://doi.org/10.1007/s00253-021-11501-w

Farahat M, Ibrahim MS, Taha LS, El-Quesni EF (2007). Response of vegetative growth and some chemical constituents of Cupressus sempervirens L. to foliar application of ascorbic acid and zinc at Nubaria World. Journal of Agricultural Sciences 3:496-502.

Farouk S, Al-Amri S (2019). Ameliorative roles of melatonin and/or zeolite on chromium-induced leaf senescence in marjoram plants by activating antioxidant defense, osmolyte accumulation, and ultrastructural modification Industrial Crops and Products 142:111823. https://doi.org/10.1016/j.indcrop.2019.111823 DOI: https://doi.org/10.1016/j.indcrop.2019.111823

Figlioli F, Sorrentino MC, Memoli V, Arena C, Maisto G, Giordano S, Capozzi F, Spagnuolo V (2019). Overall plant responses to Cd and Pb metal stress in maize: Growth pattern, ultrastructure, and photosynthetic activity Environmental Science and Pollution Research 26:1781-1790. https://doi.org/10.1007/s11356-018-3743-y DOI: https://doi.org/10.1007/s11356-018-3743-y

Fouda HM, Sofy MR (2022). Effect of biological synthesis of nanoparticles from Penicillium chrysogenum as well as traditional salt and chemical nanoparticles of zinc on canola plant oil productivity and metabolic activity. Egyptian Journal of Chemistry 65:1-2. https://doi.org/10.21608/ejchem.2021.95120.4469 DOI: https://doi.org/10.21608/ejchem.2021.95120.4469

Fuglie L (2000). New uses of Moringa studied in Nicaragua. ECHO Development Notes 68:1-25.

Giannakoula A, Therios I, Chatzissavvidis C (2021). Effect of lead and copper on photosynthetic apparatus in citrus (Citrus aurantium L.) plants. The role of antioxidants in oxidative damage as a response to heavy metal stress. Plants 10:155. https://doi.org/10.3390/plants10010155 DOI: https://doi.org/10.3390/plants10010155

Gilbert GA, Wilson C, Madore MA (1997). Root-zone salinity alters raffinose oligosaccharide metabolism and transport in Coleus. Plant Physiology 115:1267-1276. https://doi.org/10.1104/pp.115.3.1267 DOI: https://doi.org/10.1104/pp.115.3.1267

Gopal R, Rizvi AH (2008). Excess lead alters growth, metabolism and translocation of certain nutrients in radish. Chemosphere 70:1539-1544. https://doi.org/10.1016/j.chemosphere.2007.08.043 DOI: https://doi.org/10.1016/j.chemosphere.2007.08.043

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. Frontiers in Plant Science 6. https://doi.org/doi:10.3389/fpls.2015.00601 DOI: https://doi.org/10.3389/fpls.2015.00601

Hattori A, Migitaka H, Iigo M, Itoh M, Yamamoto K, Ohtani-Kaneko R, … Reiter RJ (1995). Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates. Biochemistry and Molecular Biology International 35:627-634.

Heath RL, Packer L (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125:189-198. https://doi.org/10.1016/0003-9861(68)90654-1 DOI: https://doi.org/10.1016/0003-9861(68)90654-1

Hedge J, Hofreiter B, Whistler R (1962). Carbohydrate chemistry. Academic Press, New York, pp 17.

Hernandez-Ruiz J, Cano A, Arnao MB (2004). Melatonin: a growth-stimulating compound present in lupin tissues. Planta 220:140-144. https://doi.org/10.1007/s00425-004-1317-3 DOI: https://doi.org/10.1007/s00425-004-1317-3

Hiscox J, Israelstam G (1979). A method for the extraction of chlorophyll from leaf tissue without maceration. Canadian Journal of Botany 57:1332-1334. DOI: https://doi.org/10.1139/b79-163

Jackson M (1967). Soil chemical analysis prentice Hall of India Private Limited, New Delhi, pp 498.

Jackson M, Gillette D, Danielsen E, Blifford I, Bryson R, Syers J (1973). Global dustfall during the Quaternary as related to environments Soil Science 116:135-145. DOI: https://doi.org/10.1097/00010694-197309000-00002

Jahan MS, Guo S, Baloch AR, Sun J, Shu S, Wang Y, Ahammed GJ, Kabir K, Roy R (2020). Melatonin alleviates nickel phytotoxicity by improving photosynthesis, secondary metabolism and oxidative stress tolerance in tomato seedlings. Ecotoxicology and Environmental Safety 197:110593. https://doi.org/10.1016/j.ecoenv.2020.110593 DOI: https://doi.org/10.1016/j.ecoenv.2020.110593

Karanatsidis G, Berova M (2009). Effect of organic-N fertilizer on growth and some physiological parameters in pepper plants (Capsicum annum L.). Biotechnology & Biotechnological Equipment 23:254-257. https://doi.org/10.1080/13102818.2009.10818413 DOI: https://doi.org/10.1080/13102818.2009.10818413

Kasim WA, Abokassem EM, Ragab GA, Sewelam NA (2014). Alleviation of lead stress toxicity in Vigna unguiculata by salicylic acid. Egyptian Society of Experimental Biology 10:37-49.

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 225:627-638. https://doi.org/10.1016/j.chemosphere.2019.03.026 DOI: https://doi.org/10.1016/j.chemosphere.2019.03.026

Kolář J, Macháčková I (2005). Melatonin in higher plants: occurrence and possible functions. Journal of Pineal Research 39:333-341. https://doi.org/10.1111/j.1600-079X.2005.00276.x DOI: https://doi.org/10.1111/j.1600-079X.2005.00276.x

Kováčik J, Dresler S, Peterková V, Babula P (2018). Metal-induced oxidative stress in terrestrial macrolichens. Chemosphere 203:402-409. https://doi.org/10.1016/j.chemosphere.2018.03.112 DOI: https://doi.org/10.1016/j.chemosphere.2018.03.112

KrishnaRaj S, Dan TV, Saxena PK (2000). A fragrant solution to soil remediation. International Journal of Phytoremediation 2:117-132. https://doi.org/10.1080/15226510008500034 DOI: https://doi.org/10.1080/15226510008500034

Kushwaha A, Hans N, Kumar S, Rani R (2018). A critical review on speciation, mobilization and toxicity of lead in soil-microbe-plant system and bioremediation strategies. Ecotoxicology and Environmental Safety 147:1035-1045. https://doi.org/10.1016/j.ecoenv.2017.09.049 DOI: https://doi.org/10.1016/j.ecoenv.2017.09.049

Labra M, Gianazza E, Waitt R, Eberini I, Sozzi A, Regondi S, Grassi F, Agradi E (2006). Zea mays L. protein changes in response to potassium dichromate treatments. Chemosphere 62:1234-1244. https://doi.org/10.1016/j.chemosphere.2005.06.062 DOI: https://doi.org/10.1016/j.chemosphere.2005.06.062

Lamhamdi M, El Galiou O, Bakrim A, Nóvoa-Muñoz JC, Arias-Estévez M, Aarab A, Lafont R (2013). Effect of lead stress on mineral content and growth of wheat (Triticum aestivum) and spinach (Spinacia oleracea) seedlings. Saudi Journal of Biological Sciences 20:29-36. https://doi.org/10.1016/j.sjbs.2012.09.001 DOI: https://doi.org/10.1016/j.sjbs.2012.09.001

Li Z, Xiao H, Cheng S, Zhang L, Xie X, Wu Z (2014). A comparison on the phytoremediation ability of triazophos by different macrophytes. Journal of Environmental Sciences 26:315-322. https://doi.org/10.1016/S1001-0742(13)60417-9 DOI: https://doi.org/10.1016/S1001-0742(13)60417-9

Lima LW, Checchio MV, dos Reis AR, de Cássia Alves R, Tezzoto T, Gratão PL (2019). Selenium restricts cadmium uptake and improve micronutrients and proline concentration in tomato fruits. Biocatalysis and Agricultural Biotechnology 18:101057. https://doi.org/10.1016/j.bcab.2019.101057 DOI: https://doi.org/10.1016/j.bcab.2019.101057

Lutts S, Kinet JM, Bouharmont J (1996). NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of Botany 78:389-398. https://doi.org/10.1006/anbo.1996.0134 DOI: https://doi.org/10.1006/anbo.1996.0134

Maksoud MA, Bekhit M, El-Sherif DM, Sofy AR, Sofy MR (2022). Gamma radiation-induced synthesis of a novel chitosan/silver/Mn-Mg ferrite nanocomposite and its impact on cadmium accumulation and translocation in brassica plant growth. International Journal of Biological Macromolecules 194:306-316. https://doi.org/10.1016/j.ijbiomac.2021.11.197 DOI: https://doi.org/10.1016/j.ijbiomac.2021.11.197

Malar S, Manikandan R, Favas PJ, Sahi SV, Venkatachalam P (2014). Effect of lead on phytotoxicity, growth, biochemical alterations and its role on genomic template stability in Sesbania grandiflora: a potential plant for phytoremediation. Ecotoxicology and Environmental Safety 108:249-257. https://doi.org/10.1016/j.ecoenv.2014.05.018 DOI: https://doi.org/10.1016/j.ecoenv.2014.05.018

Malar S, Vikram SS, Favas PJ, Perumal V (2016). Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)] Botanical Studies 55:1-11. https://doi.org/10.1186/s40529-014-0054-6 DOI: https://doi.org/10.1186/s40529-014-0054-6

Medina A, Azcón R (2010). Effectiveness of the application of arbuscular mycorrhiza fungi and organic amendments to improve soil quality and plant performance under stress conditions. Journal of Soil Science and Plant Nutrition 10:354-372. http://dx.doi.org/10.4067/S0718-95162010000100009 DOI: https://doi.org/10.4067/S0718-95162010000100009

Mehta S, Gaur J (1999). Heavy‐metal‐induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris New Phytologist 143:253-259. https://doi.org/10.1046/j.1469-8137.1999.00447.x DOI: https://doi.org/10.1046/j.1469-8137.1999.00447.x

Mohamed HA, Moussa HR, Rgab MHE-DS (2021). Does exogenous application of melatonin ameliorate lead toxicity in Eruca vesicaria plants?. Egyptian Journal of Botany 61:33-40. https://doi.org/10.21608/ejbo.2020.30295.1498 DOI: https://doi.org/10.21608/ejbo.2020.30295.1498

Molinari HBC, Marur CJ, Daros E, De Campos MKF, De Carvalho JFRP, Filho JCB, Pereira LFP, Vieira LGE (2007). Evaluation of the stress‐inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiologia Plantarum 130:218-229. https://doi.org/10.1111/j.1399-3054.2007.00909.x DOI: https://doi.org/10.1111/j.1399-3054.2007.00909.x

Motsara M, Roy R (2008). Guide to Laboratory establishment for plant nutrient analysis. FAO Fertilizer and Plant nutrition bulletin Food and Agriculture Organization, Rome, pp 219.

Mowafy A, Agha M, Haroun S, Abbas M, Elbalkini M (2022). Insights in nodule-inhabiting plant growth promoting bacteria and their ability to stimulate Vicia faba growth. Egyptian Journal of Basic and Applied Sciences 9:51-64. https://doi.org/10.1080/2314808X.2021.2019418 DOI: https://doi.org/10.1080/2314808X.2021.2019418

Mukhopadhyay D, Dasgupta P, Roy DS, Palchoudhuri S, Chatterjee I, Ali S, Dastidar SG (2016). A sensitive in vitro spectrophotometric hydrogen peroxide scavenging assay using 1, 10-phenanthroline. Free Radicals & Antioxidants 6. https://doi.org/10.5530/fra.2016.1.15 DOI: https://doi.org/10.5530/fra.2016.1.15

Nareshkumar A, Krishnappa B, Kirankumar T, Kiranmai K, Lokesh U, Sudhakarbabu O, Sudhakar C (2014). Effect of Pb-stress on growth and mineral status of two groundnut (Arachis hypogaea L.) cultivars. Journal of Plant Sciences 2:304-310. https://doi.org/10.11648/j.jps.20140206.17 DOI: https://doi.org/10.11648/j.jps.20140206.17

Nautiyal N, Sinha P (2012). Lead induced antioxidant defense system in pigeon pea and its impact on yield and quality of seeds. Acta Physiologiae Plantarum 34:977-983. https://doi.org/10.1007/s11738-011-0894-6 DOI: https://doi.org/10.1007/s11738-011-0894-6

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. Journal of Plant Physiology 220:115-127. https://doi.org/10.1016/j.jplph.2017.11.003 DOI: https://doi.org/10.1016/j.jplph.2017.11.003

Nazarian M, Ghanati F (2020). The role of melatonin in reinforcement of antioxidant system of rice plant (Oryza sativa L.) under arsenite toxicity?. Plant Physiology Reports 25:395-404. https://doi.org/10.1007/s40502-020-00523-7 DOI: https://doi.org/10.1007/s40502-020-00523-7

Nouman W, Siddiqui MT, Basra SMA, Farooq H, Zubair M, Gull T (2013). Biomass production and nutritional quality of Moringa oleifera as a field crop Turkish Journal of Agriculture and Forestry 37:410-419. DOI: https://doi.org/10.3906/tar-1206-29

Odjegba V, Fasidi I (2006). Effects of heavy metals on some proximate composition of Eichhornia crassipes. Journal of Applied Sciences and Environmental Management 10:83-87. https://doi.org/10.4314/jasem.v10i1.17309 DOI: https://doi.org/10.4314/jasem.v10i1.17309

Ogundiran MB, Mekwunyei NS, Adejumo SA (2018). Compost and biochar assisted phytoremediation potentials of Moringa oleifera for remediation of lead contaminated soil. Journal of Environmental Chemical Engineering 6:2206-2213. https://doi.org/10.1016/j.jece.2018.03.025 DOI: https://doi.org/10.1016/j.jece.2018.03.025

Okant M, Kaya C (2019). The role of endogenous nitric oxide in melatonin-improved tolerance to lead toxicity in maize plants. Environmental Science and Pollution Research 26:11864-11874. https://doi.org/10.1007/s11356-019-04517-3 DOI: https://doi.org/10.1007/s11356-019-04517-3

Pansu M, Gautheyrou J (2007). Handbook of soil analysis: mineralogical, organic and inorganic methods. Springer Science & Business Media DOI: https://doi.org/10.1007/978-3-540-31211-6

Park S, Lee DE, Jang H, Byeon Y, Kim YS, Back K (2013). Melatonin‐rich transgenic rice plants exhibit resistance to herbicide‐induced oxidative stress. Journal of Pineal Research 54:258-263. https://doi.org/10.1111/j.1600-079X.2012.01029.x DOI: https://doi.org/10.1111/j.1600-079X.2012.01029.x

Pattanagul W, Thitisaksakul M (2008). Effect of salinity stress on growth and carbohydrate metabolism in three rice (Oryza sativa L.) cultivars differing in salinity tolerance. Indian Journal of Experimental Botany 46:736-742. http://nopr.niscair.res.in/handle/123456789/4642

Piper CS (1966). Soil and plant analysis: a laboratory manual of methods for the examination of soils and the determination of the inorganic constituents of plants. Hans, Bombay.

Popoola JO, Obembe OO (2013). Local knowledge, use pattern and geographical distribution of Moringa oleifera Lam.(Moringaceae) in Nigeria Journal of Ethnopharmacology 150:682-691. https://doi.org/10.1016/j.jep.2013.09.043 DOI: https://doi.org/10.1016/j.jep.2013.09.043

Rasool M, Anwar-ul-Haq M, Jan M, Akhtar J, Ibrahim M, Iqbal J (2020). Phytoremedial potential of maize (Zea mays L.) hybrids against cadmium (Cd) and lead (Pb) toxicity. Pure and Applied Biology 9:1932–1945. https://doi: 10.19045/bspab.2020. 90206 DOI: https://doi.org/10.19045/bspab.2020.90206

Reetu K, Maharishi T, Kumari S (2020). Moringa oleifera: a health food for animal and human consumption. Food and Scientific Reports 1:2-5.

Rodriguez E, da Conceição Santos M, Azevedo R, Correia C, Moutinho-Pereira J, de Oliveira JMPF, Dias MC (2015). Photosynthesis light-independent reactions are sensitive biomarkers to monitor lead phytotoxicity in a Pb-tolerant Pisum sativum cultivar. Environmental Science and Pollution Research 22:574-585. https://doi.org/10.1007/s11356-014-3375-9 DOI: https://doi.org/10.1007/s11356-014-3375-9

Romanowska E, Wróblewska B, Drożak A, Zienkiewicz M, Siedlecka M (2008). Effect of Pb ions on superoxide dismutase and catalase activities in leaves of pea plants grown in high and low irradiance. Biologia Plantarum 52:80. https://doi.org/10.1007/s10535-008-0012-9 DOI: https://doi.org/10.1007/s10535-008-0012-9

Sadak MS, Abdalla AM, Abd Elhamid EM, Ezzo M (2020). Role of melatonin in improving growth, yield quantity and quality of Moringa oleifera L. plant under drought stress Bulletin of the National Research Centre 44:1-13. https://doi.org/10.1186/s42269-020-0275-7 DOI: https://doi.org/10.1186/s42269-020-0275-7

Salim R, Al-Subu M, Atallah A (1993). Effects of root and foliar treatments with lead, cadmium, and copper on the uptake distribution and growth of radish plants. Environment International 19:393-404. https://doi.org/10.1016/0160-4120(93)90130-A DOI: https://doi.org/10.1016/0160-4120(93)90130-A

Sami A, Shah F, Abdullah M, Zhou X, Yan Y, Zhu Z, Zhou K (2020). Melatonin mitigates cadmium and aluminium toxicity through modulation of antioxidant potential in Brassica napus L. Plant Biology 22:679-690. https://doi.org/10.1111/plb.13093 DOI: https://doi.org/10.1111/plb.13093

Sarafi E, Tsouvaltzis P, Chatzissavvidis C, Siomos A, Therios I (2017). Melatonin and resveratrol reverse the toxic effect of high boron (B) and modulate biochemical parameters in pepper plants (Capsicum annuum L.). Plant Physiology and Biochemistry 112:173-182. https://doi.org/10.1016/j.plaphy.2016.12.018 DOI: https://doi.org/10.1016/j.plaphy.2016.12.018

Shahid M, Dumat C, Khalid S, Rabbani F, Farooq ABU, Amjad M, Abbas G, Niazi NK (2019). Foliar uptake of arsenic nanoparticles by spinach: an assessment of physiological and human health risk implications. Environmental Science and Pollution Research 26:20121-20131. https://doi.org/10.1007/s11356-018-3867-0 DOI: https://doi.org/10.1007/s11356-018-3867-0

Shahid M, Dumat C, Khalid S, Schreck E, Xiong T, Niazi NK (2017). Foliar heavy metal uptake, toxicity and detoxification in plants: A comparison of foliar and root metal uptake. Journal of Hazardous Materials 325:36-58. https://doi.org/10.1016/j.jhazmat.2016.11.063 DOI: https://doi.org/10.1016/j.jhazmat.2016.11.063

Shahid M, Khalid S (2020). Foliar application of lead and arsenic solutions to Spinacia oleracea: biophysiochemical analysis and risk assessment. Environmental Science and Pollution Research 27. https://doi.org/10.1007/s11356-019-06519-7 DOI: https://doi.org/10.1007/s11356-019-06519-7

Sharma A, Zheng B (2019). Melatonin mediated regulation of drought stress: Physiological and molecular aspects. Plants 8:190. https://doi.org/10.3390/plants8070190 DOI: https://doi.org/10.3390/plants8070190

Sharma P, Dubey RS (2005). Lead toxicity in plants. Brazilian Journal of Plant Physiology 17:35-52. DOI: https://doi.org/10.1590/S1677-04202005000100004

Sharma SS, Dietz K-J (2006). The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany 57:711-726. https://doi.org/10.1093/jxb/erj073 DOI: https://doi.org/10.1093/jxb/erj073

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. International Journal of Molecular Sciences 20:353. https://doi.org/10.3390/ijms20020353 DOI: https://doi.org/10.3390/ijms20020353

Sivasankari B, Anandharaj M, Gunasekaran P (2014). An ethnobotanical study of indigenous knowledge on medicinal plants used by the village peoples of Thoppampatti, Dindigul district, Tamilnadu, India. Journal of Ethnopharmacology 153:408-423. https://doi.org/10.1016/j.jep.2014.02.040 DOI: https://doi.org/10.1016/j.jep.2014.02.040

Sofy AR, Sofy MR, Hmed AA, Dawoud RA, Refaey EE, Mohamed HI, El-Dougdoug NK (2021). Molecular characterization of the Alfalfa mosaic virus infecting Solanum melongena in Egypt and the control of its deleterious effects with melatonin and salicylic acid. Plants 10:459. https://doi.org/10.3390/plants10030459 DOI: https://doi.org/10.3390/plants10030459

Sofy MR, Seleiman MF, Alhammad BA, Alharbi BM, Mohamed HI (2020). Minimizing adverse effects of pb on maize plants by combined treatment with jasmonic, salicylic acids and proline. Agronomy 10:699. https://doi.org/10.3390/agronomy10050699 DOI: https://doi.org/10.3390/agronomy10050699

Soongsombat P, Kruatrachue M, Chaiyarat R, Pokethitiyook P, Ngernsansaruay C (2009). Lead tolerance and accumulation in Pteris vittata and Pityrogramma calomelanos, and their potential for phytoremediation of lead-contaminated soil. International Journal of Phytoremediation 11:396-412. https://doi.org/10.1080/15226510802565634 DOI: https://doi.org/10.1080/15226510802565634

Sorrentino M, Capozzi F, Amitrano C, Giordano S, Arena C, Spagnuolo V (2018). Performance of three cardoon cultivars in an industrial heavy metal-contaminated soil: effects on morphology, cytology and photosynthesis. Journal of Hazardous Materials 351:131-137. https://doi.org/10.1016/j.jhazmat.2018.02.044 DOI: https://doi.org/10.1016/j.jhazmat.2018.02.044

Souza VL, de Almeida A-AF, Souza JdS, Mangabeira PA, de Jesus RM, Pirovani CP, … Loguercio LL (2014). Altered physiology, cell structure, and gene expression of Theobroma cacao seedlings subjected to Cu toxicity. Environmental Science and Pollution Research 21:1217-1230. https://doi.org/10.1007/s11356-013-1983-4 DOI: https://doi.org/10.1007/s11356-013-1983-4

Suarez M, Entenza J, Doerries C, Meyer E, Bourquin L, Sutherland J, … Mermod N (2003). Expression of a plant‐derived peptide harboring water‐cleaning and antimicrobial activities. Biotechnology and Bioengineering 81:13-20. https://doi.org/10.1002/bit.10550 DOI: https://doi.org/10.1002/bit.10550

Tripathi BN, Gaur J (2004). Relationship between copper-and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta 219:397-404. https://doi.org/10.1007/s00425-004-1237-2 DOI: https://doi.org/10.1007/s00425-004-1237-2

Usman K, Al-Ghouti MA, Abu-Dieyeh MH (2019). The assessment of cadmium, chromium, copper, and nickel tolerance and bioaccumulation by shrub plant Tetraena qataranse. Scientific Reports 9:1-11. DOI: https://doi.org/10.1038/s41598-019-42029-9

van Handel E (1968). Direct microdetermination of sucrose. Analytical Biochemistry 22:280-283. DOI: https://doi.org/10.1016/0003-2697(68)90317-5

Wang M, Duan S, Zhou Z, Chen S, Wang D (2019). Foliar spraying of melatonin confers cadmium tolerance in Nicotiana tabacum L. Ecotoxicology and Environmental Safety 170:68-76. https://doi.org/10.1016/j.ecoenv.2018.11.127 DOI: https://doi.org/10.1016/j.ecoenv.2018.11.127

Wang Z, Bao J, Wang T, Moryani HT, Kang W, Zheng J, Zhan C, Xiao W (2021). Hazardous heavy metals accumulation and health risk assessment of different vegetable species in contaminated soils from a typical Mining City, Central China. International Journal of Environmental Research and Public Health 18:2617. https://doi.org/10.3390/ijerph18052617 DOI: https://doi.org/10.3390/ijerph18052617

Winska-Krysiak M, Koropacka K, Gawronski S (2015). Determination of the tolerance of sunflower to lead-induced stress. Journal of Elementology 20. DOI: https://doi.org/10.5601/jelem.2014.19.4.721

Xie C, Xiong X, Huang Z, Sun L, Ma J, Cai S, Yu F, Zhong W, Chen S, Li X (2018). Exogenous melatonin improves lead tolerance of bermudagrass through modulation of the antioxidant defense system. International Journal of Phytoremediation 20:1408-1417. https://doi.org/10.1080/15226514.2018.1488813 DOI: https://doi.org/10.1080/15226514.2018.1488813

Xiong T, Austruy A, Pierart A, Shahid M, Schreck E, Mombo S, Dumat C (2016). Kinetic study of phytotoxicity induced by foliar lead uptake for vegetables exposed to fine particles and implications for sustainable urban agriculture. Journal of Environmental Sciences 46:16-27. https://doi.org/10.1016/j.jes.2015.08.029 DOI: https://doi.org/10.1016/j.jes.2015.08.029

Xiong Z-T (1997). Bioaccumulation and physiological effects of excess lead in a roadside pioneer species Sonchus oleraceus L. Environmental Pollution 97:275-279. https://doi.org/10.1016/S0269-7491(97)00086-9 DOI: https://doi.org/10.1016/S0269-7491(97)00086-9

Yang W-T, Zhou H, Gu J-F, Zeng Q-r, Liao B-H (2017). Influence of rapeseed cake on iron plaque formation and Cd uptake by rice (Oryza sativa L.) seedlings exposed to excess Cd. Bulletin of Environmental Contamination and Toxicology 99:601-606. https://doi.org/10.1007/s00128-017-2151-1 DOI: https://doi.org/10.1007/s00128-017-2151-1

Yemm E, Willis A (1954). The estimation of carbohydrates in plant extracts by anthrone Biochemical Journal 57:508-514. https://doi.org/10.1042/bj0570508 DOI: https://doi.org/10.1042/bj0570508

Yilmaz K, Akinci İE, Akinci S (2009). Effect of lead accumulation on growth and mineral composition of eggplant seedlings (Solarium melongena) New Zealand. Journal of Crop and Horticultural Science 37:189-199. https://doi.org/10.1080/01140670909510264 DOI: https://doi.org/10.1080/01140670909510264

Yoon J, Cao X, Zhou Q, Ma LQ (2006). Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Science of the Total Environment 368:456-464. https://doi.org/10.1016/j.scitotenv.2006.01.016 DOI: https://doi.org/10.1016/j.scitotenv.2006.01.016

Yuan Z, Li C, Xiong S (2005). Effect of Cd and Pb pollution on chlorophyll content, activity of protectiase and cell membrance lipid peroxidation change in tobacco leaves. Journal of Henan Agricultural University 1:15-19.

Zhang R, Sun Y, Liu Z, Jin W, Sun Y (2017). Effects of melatonin on seedling growth, mineral nutrition, and nitrogen metabolism in cucumber under nitrate stress. Journal of Pineal Research 62:e12403. https://doi.org/10.1111/jpi.12403 DOI: https://doi.org/10.1111/jpi.12403

Zhang X, Zhang H, Zhang H, Tang M (2020). Exogenous melatonin application enhances Rhizophagus irregularis symbiosis and induces the antioxidant response of Medicago truncatula under lead stress. Frontiers in Microbiology 11:516. https://doi.org/10.3389/fmicb.2020.00516 DOI: https://doi.org/10.3389/fmicb.2020.00516

Zhao H, Xu L, Su T, Jiang Y, Hu L, Ma F (2015). Melatonin regulates carbohydrate metabolism and defenses against Pseudomonas syringae pv. tomato DC 3000 infection in Arabidopsis thaliana. Journal of Pineal Research 59:109-119. https://doi.org/10.1111/jpi.12245 DOI: https://doi.org/10.1111/jpi.12245

Zhong B, Chen J, Shafi M, Guo J, Wang Y, Wu J, Ye Z, He L, Liu D (2017). Effect of lead (Pb) on antioxidation system and accumulation ability of Moso bamboo (Phyllostachys pubescens). Ecotoxicology and Environmental Safety 138:71-77. https://doi.org/10.1016/j.ecoenv.2016.12.020 DOI: https://doi.org/10.1016/j.ecoenv.2016.12.020



How to Cite

EL-SAKAAN, M. F., YOUNIS, M. E., & SHUKRY, W. M. (2022). Elucidating the role of melatonin or sugar beet pulp pellet in physiological improvement characteristics and promoting the growth of Moringa oleifera under lead stress. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 50(2), 12573. https://doi.org/10.15835/nbha50212573



Research Articles
DOI: 10.15835/nbha50212573