Skip to main content
Log in

Arsenic Toxicity is Counteracted by Exogenous Application of Melatonin to Different Extents in Arsenic-susceptible and Arsenic-tolerant Rice Cultivars

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

Abstract

The current study established the protective effects of exogenous melatonin in ameliorating arsenic toxicity in Khitish (arsenic-sensitive) and Muktashri (arsenic-tolerant) rice cultivars. Melatonin highly improved the overall growth performance of arsenic-treated seedlings, more prominently in the sensitive variety, Khitish. Although the level of arsenic increased in both the cultivars, Khitish accumulated comparatively higher arsenic level. However, melatonin supplementation reduced arsenic bioaccumulation and restored physiological growth attributes, as supported by lowering of electrolyte leakage, chlorophyll loss (by inducing RuBisCo), protein carbonylation, malondialdehyde accumulation, lipoxygenase (LOX), NADPH oxidase (NOX) and protease activity, and improvement of membrane stability index. Isoforms of LOX and NOX showed varietal differences during arsenic stress, both in the presence and absence of melatonin. Melatonin reduced methylglyoxal content during arsenic stress, concomitant with down-regulated gene expression and enzyme activity for glyoxalases. The nitrogen assimilation was improved via induced nitrate reductase (NR) activity and NR expression. The variable accumulation of osmolytes like proline, glycine betaine and total amino acids, concomitant with suppressed P5CS and BADH1 expression, and induced PDH was noteworthy. Antioxidant metabolites like anthocyanins, flavonoids, carotenes, xanthophylls and total phenolics were accumulated upon supplementation of melatonin in arsenic-stressed Khitish, supported by the activation of ANS and PSY genes. Melatonin lowered the ascorbic-acid oxidase activity and restored the ascorbate sink in arsenic-affected seedlings. Overall, the study revealed the potential role of exogenous melatonin in mitigating arsenic-induced injuries by strengthening osmolytes and antioxidative machinery, leading to the restoration of growth and metabolism in rice, especially in the susceptible cultivar.

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

Access this article

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
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Adams MA, Bolger PM, Gunderson EL (1994) Dietary intake and hazards of arsenic. In: Chappell WR, Abernathy CO, Cothern CR (eds) Arsenic: exposure and health. Science and Technology Letters, Northwood, pp 41–49

    Google Scholar 

  • Afreen F, Zobayed SMA, Kozai T (2006) Melatonin in Glycyrrhiza uralensis: response of plant roots to spectral quality of light and UV-B radiation. J Pineal Res 41:108–115

    Article  CAS  PubMed  Google Scholar 

  • 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. Sci Hortic 265:109205

    Article  CAS  Google Scholar 

  • Ahmad P, Alam P, Balawi TH, Altalayan FH, Ahanger MA, Ashraf M (2019) Sodium nitroprusside (SNP) improves tolerance to arsenic (As) toxicity in Vicia faba through the modifications of biochemical attributes, antioxidants, ascorbate-glutathione cycle and glyoxalase cycle. Chemosphere 244:125480

    Article  PubMed  CAS  Google Scholar 

  • Akinbile CO, Haque AMM (2012) Arsenic contamination in irrigation water for rice production in Bangladesh: a review. Trends Appl Sci Res 7:331–349

    Article  CAS  Google Scholar 

  • Arnao MB, Hernández-Ruiz J (2019) Melatonin: a new plant hormone and/or a plant master regulator? Trends Plant Sci 24:38–48

    Article  CAS  PubMed  Google Scholar 

  • Arnao MB, Hernández-Ruiz J (2020) Melatonin as a regulatory hub of plant hormone levels and action in stress situations. Plant Biol. https://doi.org/10.1111/plb.13202

    Article  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Med Cell Longev 2014:1–31

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Roychoudhury A (2019a) Differential regulation of defence pathways in aromatic and non-aromatic indica rice cultivars towards fluoride toxicity. Plant Cell Rep 38:1217–1233

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Roychoudhury A (2019b) Melatonin application reduces fluoride uptake and toxicity in rice seedlings by altering abscisic acid, gibberellin, auxin and antioxidant homeostasis. Plant Physiol Biochem 145:164–173

    Article  PubMed  CAS  Google Scholar 

  • Bano Y, Jayant SK, Sharma J, Shrivastava A (2017) Arsenic effect on morphology and rate limiting step of nitrate assimilation pathway of Phaseolus vulgaris. Int J Adv Res Dev 2:341–344

    Google Scholar 

  • Basu S, Roychoudhury A, Saha PP, Sengupta DN (2010) Differential antioxidative responses of indica rice cultivars to drought stress. Plant Growth Regul 60:51–59

    Article  CAS  Google Scholar 

  • Basu S, Roychoudhury A, Sanyal S, Sengupta DN (2012) Carbohydrate content and antioxidative potential of the seed of three edible indica rice (Oryza sativa L.) cultivars. Ind J Biochem Biophys 49:115–123

    CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Begum MC, Islam MS, Islam M, Amin R, Parvez MS, Kabir AH (2016) Biochemical and molecular responses underlying differential arsenic tolerance in rice (Oryza sativa L.). Plant Physiol Biochem 104:266–277

    Article  CAS  PubMed  Google Scholar 

  • Bhowmick S, Pramanik S, Singh P, Mondal P, Chatterjee D, Nriagu J (2018) Arsenic in groundwater of West Bengal, India: a review of human health risks and assessment of possible intervention options. Sci Total Environ 612:148–169

    Article  CAS  PubMed  Google Scholar 

  • Bidabadi SS, VanderWeide J, Sabbatini P (2020) Exogenous melatonin improves glutathione content, redox state and increases essential oil production in two Salvia species under drought stress. Sci Rep 10:6883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • 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. Agric Water Manage 211:37–47

    Article  Google Scholar 

  • Chandrakar V, Dubey A, Keshavkant S (2016) Modulation of antioxidants enzymes by salicylic acid in arsenic exposed Glycine max L. J Soil Sci Plant Nutr 16:662–676

    CAS  Google Scholar 

  • Chauhan R, Awasthi S, Tripathi P, Mishra S, Dwivedi S, Niranjan A, Mallick S, Tripathi P, Pande V, Tripathi RD (2017) Selenite modulates the level of phenolics and nutrient element to alleviate the toxicity of arsenite in rice (Oryza sativa L.). Ecotoxicol Environ Saf 138:47–55

    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 164:349–363

    Article  CAS  PubMed  Google Scholar 

  • Cheng GW, Breen PJ (1991) Activity of phenylalanine ammonia-lyase (PAL) and concentrations of anthocyanins and phenolics in developing strawberry fruit. J Am Soc Hortic Sci 116:865–869

    Article  CAS  Google Scholar 

  • Christen K (2001) The arsenic threat worsens. Environ Sci Technol 35:286A-291A

    Article  CAS  PubMed  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53

    Article  Google Scholar 

  • Davies BH (1965) Chemistry and biochemistry of plant pigments. Goodwin, London

    Google Scholar 

  • Dikilitas M, Simsek E, Roychoudhury A (2020) Role of proline and glycine betaine in overcoming abiotic stresses. In: Roychoudhury A, Tripathi DK (eds) Protective chemical agents in the amelioration of plant abiotic stress: biochemical and molecular perspectives. Wiley-Blackwell, Hoboken, pp 1–23

    Google Scholar 

  • Dittmar J, Voegelin A, Maurer F, Roberts LC, Hug SJ, Saha GC, Badruzzaman ABM, Kretzschmar R (2010) Arsenic in soil and irrigation water affects arsenic uptake by rice: complementary insights from field and pot studies. Environ Sci Technol 44:8842–8848

    Article  CAS  PubMed  Google Scholar 

  • Dwivedi S, Kumar A, Mishra S, Sharma P, Sinam G, Bahadur L, Goyal V, Jain N, Tripathi RD (2020) Orthosilicic acid (OSA) reduced grain arsenic accumulation and enhanced yield by modulating the level of trace element, antioxidants, and thiols in rice. Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-020-08663-x

    Article  PubMed  Google Scholar 

  • Farooq MA, Islam F, Ali B, Najeeb U, Mao B, Gill RA, Yan G, Siddique KHM, Zhou W (2016) Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism. Environ Exp Bot 132:42–52

    Article  CAS  Google Scholar 

  • Farouk S, Al-Amri SM (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. Ind Crops Prod 142:1823

    Article  CAS  Google Scholar 

  • Farouk S, Al-Amri SM (2019b) Exogenous melatonin-mediated modulation of arsenic tolerance with improved accretion of secondary metabolite production, activating antioxidant capacity and improved chloroplast ultrastructure in rosemary herb. Ecotoxicol Environ Saf 180:333–347

    Article  CAS  PubMed  Google Scholar 

  • Gadi BR, Verma P, Ram A (2012) Influence of NaF on seed germination, membrane stability and some biochemicals content in Vigna seedlings. J Chem Biol Phys Sci 2:1371–1378

    CAS  Google Scholar 

  • Ghosh S, Maiti TK, Basu PS (2008) Bioproduction of ascorbic acid in root nodule and root of the legume pulse Phaseolus mungo. Curr Microbiol 56:495–498

    Article  CAS  PubMed  Google Scholar 

  • Gong B, Yan Y, Wen D, Shi Q (2017) Hydrogen peroxide produced by NADPH oxidase: a novel downstream signaling pathway in melatonin-induced stress tolerance in Solanum lycopersicum. Physiol Plant 160:396–409

    Article  CAS  PubMed  Google Scholar 

  • Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307

    Article  CAS  Google Scholar 

  • Gupta M, Ahmad MA (2014) Arsenate induced differential response in rice genotypes. Ecotoxicol Environ Saf 107:46–54

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Singh EJ (2019) Arsenic-iron relationships in aquifers of north east India: implications for public health and the environment. Environ Manage 63:437–443

    Article  PubMed  Google Scholar 

  • Gupta BK, Sahoo KK, Ghosh A, Tripathi AK, Anwar K, Das P, Singh AK, Pareek A, Sopory SK, Singla-Pareek SL (2017) Manipulation of glyoxalase pathway confers tolerance to multiple stresses in rice. Plant Cell Environ 41:1186–1200

    Article  PubMed  CAS  Google Scholar 

  • Hageman RH, Reed AJ (1980) Nitrate reductase from higher plants. Methods Enzymol 69:270–280

    Article  CAS  Google Scholar 

  • Hasan MK, Ahammed GJ, Yin L, Shi K, Xia X, Zhou Y, Yu Z, Zhou J (2015) Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Front Plant Sci 6:601

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Anee TI, Bhuiyan TF, Nahar K, Fujita M (2019) Emerging role of osmolytes in enhancing abiotic stress tolerance in rice. In: Fujita M, Nahar K, Biswas JK (eds) Advances in rice research for abiotic stress tolerance. Woodhead Publishing, Cambridge, pp 677–708

    Chapter  Google Scholar 

  • He J, Zhuang X, Zhou J, Sun L, Wan H, Li H, Lyu D (2020) Exogenous melatonin alleviates cadmium uptake and toxicity in apple rootstocks. Tree Physiol 40:746–761

    Article  CAS  PubMed  Google Scholar 

  • Hejl AM, Koster KL (2004) Juglone disrupts root plasma membrane H+-ATPase activity and impairs water uptake, root respiration, and growth in soybean (Glycine max) and corn (Zea mays). J Chem Ecol 30:453–471

    Article  CAS  PubMed  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hossain MA, Hossain MZ, Fujita M (2009) Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust J Crop Sci 3:53–64

    CAS  Google Scholar 

  • Hu W, Cao Y, Loka DA, Harris-Shultz KR, Reiter RJ, Ali S, Liu Y, Zhou Z (2020) Exogenous melatonin improves cotton (Gossypium hirsutum L.) pollen fertility under drought by regulating carbohydrate metabolism in male tissues. Plant Physiol Biochem 151:579–588

    Article  CAS  PubMed  Google Scholar 

  • Jha AB, Dubey RS (2004) Arsenic exposure alters activity behaviour of key nitrogen assimilatory enzymes in growing rice plants. Plant Growth Regul 43:259–268

    Article  CAS  Google Scholar 

  • Jia C, Yu X, Zhang M, Liu Z, Zou P, Ma J, Xu Y (2020) Application of melatonin-enhanced tolerance to high-temperature stress in Cherry Radish (Raphanus sativus L. var. radculus pers). J Plant Growth Regul 39:631–640

    Article  CAS  Google Scholar 

  • Jung H, Kong MS, Lee BR, Kim TH, Chae MJ, Lee EJ, Jung GB, Lee CH, Sung JK, Kim YH (2019) Exogenous glutathione increases arsenic translocation into shoots and alleviates arsenic-induced oxidative stress by sustaining ascorbate-glutathione homeostasis in rice seedlings. Front Plant Sci 10:1089

    Article  PubMed  PubMed Central  Google Scholar 

  • Karimi N, Vakilipak F, Souri Z, Farooq MA, Akhtar J (2019) The role of selenium on mitigating arsenic accumulation, enhancing growth and antioxidant responses in metallicolous and non-metallicolous population of Isatis cappadocica Desv. and Brassica oleracea L. Environ Sci Pollut Res Int 26:21704–21716

    Article  CAS  PubMed  Google Scholar 

  • Kaur C, Ghosh A, Pareek A, Sopory SK, Singla-Pareek SL (2014) Glyoxalases and stress tolerance in plants. Biochem Soc Trans 42:485–490

    Article  CAS  PubMed  Google Scholar 

  • Kaur C, Kushwaha HR, Mustafiz A, Pareek A, Sopory SK, Singla-Pareek SL (2015) Analysis of global gene expression profile of rice in response to methylglyoxal indicates its possible role as a stress signal molecule. Front Plant Sci 6:682

    Article  PubMed  PubMed Central  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 225:627–638

    Article  CAS  PubMed  Google Scholar 

  • Khan MN, Zhang J, Luo T, Liu J, Rizwan M, Fahad S, Xu Z, Hu L (2019) Seed priming with melatonin coping drought stress in rapeseed by regulating reactive oxygen species detoxification: antioxidant defense system, osmotic adjustment, stomatal traits and chloroplast ultrastructure perseveration. Ind Crops Prod 140:111597

    Article  CAS  Google Scholar 

  • Khan A, Numan M, Khan AL, Lee I-J, Imran M, Asaf S, Al-Harrasi A (2020) Melatonin: awakening the defense mechanisms during plant oxidative stress. Plants 9:407

    Article  CAS  PubMed Central  Google Scholar 

  • Kim EJ, Jeon E-K, Baek K (2016) Role of reducing agent in extraction of arsenic and heavy metals from soils by use of EDTA. Chemosphere 152:274–283

    Article  CAS  PubMed  Google Scholar 

  • Kumar N, Gautam A, Dubey AK, Ranjan R, Pandey A, Kumari B, Singh G, Mandotra S, Chauhan PS, Srikrishna S, Dutta V, Mallick S (2019) GABA mediated reduction of arsenite toxicity in rice seedling through modulation of fatty acids, stress responsive amino acids and polyamines biosynthesis. Ecotoxicol Environ Saf 173:15–27

    Article  CAS  PubMed  Google Scholar 

  • Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Li X, Wei J-P, Scott E, Liu J-W, Guo S, Li Y, Zhang L, Han W-Y (2018) Exogenous melatonin alleviates cold stress by promoting antioxidant defense and redox homeostasis in Camellia sinensis L. Molecules 23:165

    Article  PubMed Central  CAS  Google Scholar 

  • Li J, Yang Y, Sun K, Chen Y, Chen X, Li X (2019) Exogenous melatonin enhances cold, salt and drought stress tolerance by improving antioxidant defense in tea plant (Camellia sinensis (L.) O. Kuntze). Molecules 24:1826

    Article  CAS  PubMed Central  Google Scholar 

  • Li ZG, Xy Y, Bai LK, Zhang SY, Wang Y (2019) Melatonin enhances thermotolerance of maize seedlings (Zea mays L.) by modulating antioxidant defense, methylglyoxal detoxification, and osmoregulation systems. Protoplasma 256:471–490

    Article  CAS  PubMed  Google Scholar 

  • Li X, Ahammed GJ, Zhang X-N, Zhang L, Yan P, Zhang L-P, Fu J-Y, Han W-Y (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 C, Zheng G, Li W, Wang Y, Hu B, Wang H (2015) Melatonin delays leaf senescence and enhances salt stress tolerance in rice. J Pineal Res 59:91–101

    Article  CAS  PubMed  Google Scholar 

  • Majumder B, Das S, Mukhopadhyay S, Biswas AK (2018) Identification of arsenic-tolerant and arsenic-sensitive rice (Oryza sativa L.) cultivars on the basis of arsenic accumulation assisted stress perception, morpho-biochemical responses, and alteration in genomic template stability. Protoplasma 256:193–211

    Article  PubMed  CAS  Google Scholar 

  • Martinez V, Nieves-Cordones M, Lopez-Delacalle M, Rodenas R, Mestre T, Garcia-Sanchez F, Rubio F, Nortes PA, Mittler R, Rivero R (2018) Tolerance to stress combination in tomato plants: new insights in the protective role of melatonin. Molecules 23:535

    Article  PubMed Central  CAS  Google Scholar 

  • Meharg AA, Rahman MM (2003) Arsenic contamination of Bangladesh paddy field soils: implications for rice contribution to arsenic consumption. Environ Sci Technol 37:229–234

    Article  CAS  PubMed  Google Scholar 

  • Moore S (1968) Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J Biol Chem 243:6281–6283

    Article  CAS  PubMed  Google Scholar 

  • Mousavi SR, Niknejad Y, Fallah H, Barari-Tari D (2020) Methyl jasmonate alleviates arsenic toxicity in rice. Plant Cell Rep 39:1041–1060

    Article  CAS  PubMed  Google Scholar 

  • Nawaz MA, Huang Y, Bie Z, Ahmed W, Reiter RJ, Niu M, Hameed S (2016) Melatonin: current status and future perspectives in plant science. Front Plant Sci 6:1230

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. J Plant Physiol 220:115–127

    Article  CAS  PubMed  Google Scholar 

  • Okant M, Kaya C (2019) The role of endogenous nitric oxide in melatonin-improved tolerance to lead toxicity in maize plants. Environ Sci Pollut Res 26:11864–11874

    Article  CAS  Google Scholar 

  • Olaiya CO (2010) Enzyme activity in bioregulator-treated tomato (Solanum lycopersicon) genotypes. Afr J Biotechnol 9:3264–3271

    CAS  Google Scholar 

  • Parvin K, Nahar K, Hasanuzzaman M, Bhuyan MHMB, Mohsin SM, Fujita M (2020) Exogenous vanillic acid enhances salt tolerance of tomato: insight into plant antioxidant defense and glyoxalase systems. Plant Physiol Biochem 150:109–120

    Article  CAS  PubMed  Google Scholar 

  • Paul S, Roychoudhury A (2018) Transcriptome profiling of abiotic stress-responsive genes during cadmium chloride-mediated stress in two indica rice varieties. J Plant Growth Regul 37:657–667

    Article  CAS  Google Scholar 

  • Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poeggeler B, Thuermann S, Dose A, Schoenke M, Burkhardt S, Hardeland R (2002) Melatonin’s unique radical scavenging properties—roles of its functional substituents as revealed by a comparison with its structural analogs. J Pineal Res 33:20–30

    Article  CAS  PubMed  Google Scholar 

  • Principato GB, Rosi G, Talesa V, Govannini E, Uolila L (1987) Purification and characterization of two forms of glyoxalase II from rat liver and brain of wistar rats. Biochem Biophys Acta 911:349–355

    CAS  PubMed  Google Scholar 

  • Qiu Y, An K, Sun J, Chen X, Gong X, Ma L, Wu S, Jiang S, Zhang Z, Wang Y (2019) Investigating the effect of methyl jasmonate and melatonin on resistance of Malus crabapple “Hong Jiu” to ozone stress. Environ Sci Pollut Res Int 26:27761–27768

    Article  CAS  PubMed  Google Scholar 

  • Rady MM (2011) Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium 496 content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Sci Hortic 129:232–237

    Article  CAS  Google Scholar 

  • Rahman MA, Hasegawa H, Rahman MM, Islam MN, Miah MAM, Tasmen A (2007) Effect of arsenic on photosynthesis, growth and yield of five widely cultivated rice (Oryza sativa L.) varieties in Bangladesh. Chemosphere 67:1072–1079

    Article  CAS  Google Scholar 

  • Richards LA, Kumar A, Shankar P, Gaurav A, Ghosh A, Polya DA (2020) Distribution and geochemical controls of arsenic and uranium in groundwater-derived drinking water in Bihar, India. Int J Environ Res Public Health 17:E2500

    Article  PubMed  CAS  Google Scholar 

  • Roychoudhury A, Roy C, Sengupta DN (2007) Transgenic tobacco plants overexpressing the heterologous lea gene Rab16A from rice during high salt and water deficit display enhanced tolerance to salinity stress. Plant Cell Rep 26:1839–1859

    Article  CAS  PubMed  Google Scholar 

  • Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma P, Dubey RS (2005) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity an water stress: role of osmolytes as enzyme protectant. J Plant Physiol 162:854–864

    Article  CAS  PubMed  Google Scholar 

  • Sharma J, Subhadra AV (2010) The effect of mercury on nitrate reductase activity in bean leaf segments (Phaseolus vulgaris) and its chelation by phytochelatin synthesis. Life Sci Med Res 13:1–8

    Google Scholar 

  • Shi H, Jiang C, Ye T, Tan DX, Reiter RJ, Zhang H et al (2015) Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. J Exp Bot 66:681–694

    Article  CAS  PubMed  Google Scholar 

  • Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui MH, Alamri S, Alsubaie QD, Ali HM, Ibrahim AA, Alsadon A (2019) Potential roles of melatonin and sulfur in alleviation of lanthanum toxicity in tomato seedlings. Ecotoxicol Environ Saf 180:656–667

    Article  CAS  PubMed  Google Scholar 

  • Singh AP, Dixit G, Kumar A, Mishra S, Singh PK, Dwivedi S, Trivedi PK, Chakrabarty D, Mallick S, Pandey V, Dhankher OP, Tripathi RD (2016) Nitric oxide alleviated arsenic toxicity by modulation of antioxidants and thiol metabolism in rice (Oryza sativa L.). Front Plant Sci 6:1272

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh R, Parihar P, Prasad SM (2018) Simultaneous exposure of sulphur and calcium hinder as toxicity: up-regulation of growth, mineral nutrients uptake and antioxidants system. Ecotoxicol Environ Saf 161:318–331

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Prasad SM, Singh VP (2020) Additional calcium and sulfur manages hexavalent chromium toxicity in Solanum lycopersicum L. and Solanum melongena L. seedlings by involving nitric oxide. J Hazard Mater 398:1607

    Article  CAS  Google Scholar 

  • Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava S, Sharma YK (2013) Arsenic phytotoxicity in black gram (Vigna mungo L. var. PU19) and its possible amelioration by phosphate application. J Plant Physiol Pathol 1:3

    Google Scholar 

  • Srivastava S, Akkarakaran JJ, Sounderajan S, Shrivastava M, Suprasanna P (2016) Arsenic toxicity in rice (Oryza sativa L.) is influenced by sulfur supply: impact on the expression of transporters and thiol metabolism. Geoderma 270:33–42

    Article  CAS  Google Scholar 

  • Stoeva N, Berova M, Zlatev Z (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Plant 49:293–296

    Article  CAS  Google Scholar 

  • Sun C, Lv T, Huang L, Liu X, Jin C, Lin X (2020) Melatonin ameliorates aluminum toxicity through enhancing aluminum exclusion and reestablishing redox homeostasis in roots of wheat. J Pineal Res 68:e12642

    Article  CAS  PubMed  Google Scholar 

  • Sun C, Liu L, Wang L, Li B, Jin C, Lin X (2021) Melatonin: a master regulator of plant development and stress responses. J Integr Plant Biol. https://doi.org/10.1111/jipb.12993

    Article  PubMed  Google Scholar 

  • Tripathi RD, Tripathi P, Dwivedi S, Dubey S, Chatterjee S, Chakrabarty D, Trivedi PK (2012) Arsenomics: omics of arsenic metabolism in plants. Front Physiol 3:275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma PK, Verma S, Pande V, Mallick S, Tripathi RD, Dhankher OP, Chakrabarty D (2016) Overexpression of rice glutaredoxin OsGrx_C7 and OsGrx_C2.1 reduces intracellular arsenic accumulation and increases tolerance in Arabidopsis thaliana. Front Plant Sci 7:740

    PubMed  PubMed Central  Google Scholar 

  • Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Yin L, 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

    Article  PubMed  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 (2014) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66:695–707

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wei Z, Li C, Gao T, Zhang Z, Liang B, Lv Z, Zou Y, Ma F (2019) Melatonin increases the performance of Malus hupehensis after UV-B exposure. Plant Physiol Biochem 139:630–641

    Article  CAS  PubMed  Google Scholar 

  • Wild R, Ooi L, Srikanth V, Münch G (2012) A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: the N-acetyl-l-cysteine assay. Anal Bioanal Chem 403:2577–2581

    Article  CAS  PubMed  Google Scholar 

  • Xie C, Xiong X, Huang Z, Sun L, Ma J, Cai S, Yu F, Zhong W, Li X (2018) Exogenous melatonin improves lead tolerance of bermudagrass through modulation of the antioxidant defense system. Int J Phytoremediation 20:1408–1417

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Wang A, Li X, Kou M, Wang W, Chen X, Xu T, Zhu M, Ma D, Li Z, Sun Z (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 

  • Yuan L, Zhu S, Li S, Shu S, Sun J, Guo S (2014) 24-epibrassinolide regulates carbohydrate metabolism and increases polyamine content in cucumber exposed to Ca(NO3)2 stress. Acta Physiol Plant 36:2845–2852

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed Central  Google Scholar 

  • Zhang L, Jia J, Xu Y, Wang Y, Hao J, Li T (2012) Production of transgenic Nicotiana sylvestris plants expressing melatonin synthetase genes and their effect on UV-B-induced DNA damage. Vitro Cell Dev Biol Plant 48:275–282

    Article  CAS  Google Scholar 

  • Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S, Guo Y-D (2015) Roles of melatonin in abiotic stress resistance in plants. J Exp Bot 66:647–656

    Article  CAS  PubMed  Google Scholar 

  • Zhang N, Sun Q, Li H, Li X, Cao Y, Zhang H, Li S, Zhang L, Qi Y, Ren S, Zhao B, Guo YD (2016) Melatonin improved anthocyanin accumulation by regulating gene expressions and resulted in high reactive oxygen species scavenging capacity in cabbage. Front Plant Sci 7:197

    PubMed  PubMed Central  Google Scholar 

  • 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. J Pineal Res 62:e12403

    Article  CAS  Google Scholar 

  • Zhang J, Li D, Wei J, Ma W, Kong X, Rengel Z, Chen Q (2019) Melatonin alleviates aluminum-induced root growth inhibition by interfering with nitric oxide production in Arabidopsis. Environ Exp Bot 161:157–165

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Financial assistance from Science and Engineering Research Board, Government of India through the Grant [EMR/2016/004799] and Department of Higher Education, Science and Technology and Biotechnology, Government of West Bengal, through the Grant [264(Sanc.)/ST/P/S&T/1G-80/2017] to Dr. Aryadeep Roychoudhury is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Contributions

ARC designed the experimental plan. SS and AB performed the experiments and generated data. SS, AB and ARC drafted the manuscript. ARC supervised the entire work, provided critical comments and incorporated necessary corrections or modifications within the manuscript.

Corresponding author

Correspondence to Aryadeep Roychoudhury.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest in publication of the manuscript.

Research Involving Human and Animal Participants

The present work does not involve any human subject or animal model.

Additional information

Handling Editor: Golam jalal Ahammed.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Samanta, S., Banerjee, A. & Roychoudhury, A. Arsenic Toxicity is Counteracted by Exogenous Application of Melatonin to Different Extents in Arsenic-susceptible and Arsenic-tolerant Rice Cultivars. J Plant Growth Regul 41, 2210–2231 (2022). https://doi.org/10.1007/s00344-021-10432-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-021-10432-0

Keywords

Navigation