Growth and antioxidant responses in plants induced by heavy metals present in fly ash

Abstract

Fly ash (FA) is a solid waste generated from coal combustion processes every year from thermal power plant. FA was considered as a problem for the environment, but also proves to be beneficial for the agricultural crops. This review begins with the utilization of FA as a soil ameliorant, its role in enhancing the plant growth and impact of elemental uptake from FA on plant growth. FA improves the physical, chemical and biological property of the soil which thereby enhances the crop productivity. Then, it focusses on phytotoxicity of various heavy metals in plants such as chromium, arsenic, lead, zinc, etc., followed by analyzing the defense mechanism of the plants against these heavy metal stresses which is due to the presence of toxic heavy metals present in FA resulting in the generation of reactive oxygen species which further causes oxidative stress. Finally, the review analyzes the influence of heavy metals on the antioxidative system of various plant species which helps in understanding the usage of optimum concentration of FA amendment in the soil for plant cultivation and to further explore the key features regulating the heavy metal damage and utilization of FA in agriculture.

Keywords

Anti-oxidation system / Fly ash / Heavy metal stress / Plant growth / Plant defense mechanism / Reactive oxygen species / Oxidative stress

References

[1] Abhilash PC, Tripathi V, Edrisi SA Sustainability of crop production from polluted lands. Energy Ecol Environ, 2016, 1: 54-65

[2] Adriano DC, Wenzel WW, Vangronsveld J, Bolan NS. Role of assisted natural remediation in environmental cleanup. Geoderma, 2004, 122: 121-142

[3] Aggarwal M, Sharma S, Kaur N, Pathania D, Bhandhari K, Kaushal N, Kaur R, Singh K, Srivastava A, Nayyar H. Exogenous proline application reduces phytotoxic effects of selenium by minimizing oxidative stress and improves growth in bean (Phaseolus vulgaris L.) seedlings. Biol Trace Elem Res, 2011, 140(3): 354-367

[4] Aggrawal B, Czymmek KJ, Sparks DL, Bais HP. Transient influx of nickel in root mitochondria modulates organic acid and reactive oxygen species production in nickel hyperaccumulators Alyssum murale. J Biol Chem, 2013, 288(10): 7351-7362

[5] Ahmad R, Tehsin Z, Malik ST. Phytoremediation potential of hemp (Cannabis sativa L.): identification and characterization of heavy metals responsive genes. Clean-Soil Air Water., 2016, 44(2): 195-201

[6] Ansari FA, Gupta AK, Yunus M. Fly ash from coal fed thermal power plants: bulk utilization in horticulture—a long term risk management option. Int J Environ Res, 2011, 5(1): 101-108

[7] Ashraf M, Foolad MR. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot, 2007, 59: 206-216

[8] Bakkaus E, Gouget B, Gallien JP, Khodja H, Carrot H, Morel JL, Collins R. Concentration and distribution of cobalt in higher plants: the use of micro-PIXE spectroscopy. Nucl Instrum Methods B, 2005, 231: 350-356

[9] Barceloux DG, Barceloux D. Cobalt. J Toxicol Clin Toxicol, 1999, 37: 201-216

[10] Basu M, Pande M, Bhadoria PBS, Mahapatra SC. Potential fly-ash utilization in agriculture: a global review. Progre Nat Sci, 2009, 19: 1173-1186

[11] Belen Marquez-Garcıa M, Fernandez-Recamales A, Cordoba F. Effects of cadmium on phenolic composition and antioxidant activities of Erica andevalensis. J Bot, 2012

[12] Benekos K, Kissoudis C, Nianiou-Obeidat I, Labrou N, Madesis P, Kalamaki M, Makris A, Tsaftaris A. Overexpression of a specific soybean GmGSTU4 isoenzyme improves diphenyl ether and chloroacetanilide herbicide tolerance of transgenic tobacco plants. J Biotechnol, 2010, 150: 195-201

[13] Brake SS, Jensen RR, Mattox JM. Effects of coal fly ash amended soils on trace element uptake in plants. Environ Geol, 2004, 45: 680-689

[14] CEA (Central Electricity Authority) (2018) Annual Report on Fly-ash utilization, Report on Fly Ash Generation at Coal/Lignite Based Thermal Power Stations and its Utilization in the Country, New Delhi

[15] Cestone B, Cuypers A, Vangronsveld J, Sgherri C, Navari-Izzo F. The influence of EDDS on the metabolic and transcriptional responses induced by copper in hydroponically grown Brassica carinata seedlings. Plant Physiol Biochem, 2012, 55: 43-51

[16] Chandrakar JD, Dash AK, Jena SN, Panda N, Monica M. Soil microbial activity as influenced by application of fly ash and soil amendments to maize crop in acidic alfisols. Int Res J Agric Sci Soil Sci, 2015, 5(4): 120-128

[17] Chatterjee J, Chatterjee C. Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut, 2000, 109: 69-74

[18] Chinmayee MD, Anu MS, Mahesh B, Sheeba MA, Mini I, Swapna TS. A comparative study of heavy metal accumulation and antioxidant responses in Jatropha curcas L. IOSR. J Environ Sci Toxicol Food Technol, 2014, 8(7): 58-67

[19] Ciupa MK, Ciepał R, Socha AN, Barczyk G. A comparative study of heavy metal accumulation and antioxidant responses in Vaccinium myrtillus L. leaves in polluted and non-polluted areas. Environ Sci Pollut Res Int, 2013, 20(7): 4920-4932

[20] Ciupa MK, Ciepał R, Socha AN, Barczyk G. Accumulation of heavy metals and antioxidant responses in Pinus sylvestris L. needles in polluted and non-polluted sites. Ecotoxicology, 2016, 25: 970-981

[21] Cohu CM, Pilon M. Regulation of superoxide dismutase expression by copper availability. Physiol Plant, 2007, 129(4): 747-755

[22] Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, Horemans N, Vanhoudt N, Van Sanden S, Van Belleghem F, Yvese G, Jana C, Jacoa V. The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol, 2011, 168: 309-316

[23] Dahiya P, Manglik A. Evaluation of antibacterial, antifungal and antioxidant potential of essential oil from Amyris balsamifera against multi drug resistant clinical isolates. Asian J Pharm Clin Res, 2013, 6(5): 57-60

[24] Dalvi AA, Bhalerao SA. Response of plants towards heavy metal toxicity: an overview of avoidance, tolerance and uptake mechanism. Ann Plant Sci, 2013, 2(9): 362-368

[25] Demirevska-kepova K, Simova-Stoilova L, Stoyanova Z, Holzer R, Feller U. Biochemical changes in barley plants after successive supply of copper and manganese. Environ Exp Bot, 2004, 52: 253-266

[26] De-Vries W, Lofts S, Tipping E, Meili M, Groenenberg JE, Schütze G. Impact of soil properties on critical concentrations of cadmium, lead, copper, zinc, and mercury in soil and soil solution in view of ecotoxicological effects. Rev Environ Contam Toxicol, 2002, 191: 47-89

[27] Dimkpa CHO, Merten D, Svatos A, Buchel G, Kothe E. Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem, 2009, 41(1): 154-162

[28] Dwivedi S, Tripathi RD, Srivastava S, Mishra S, Shukla MK, Tiwari KK, Singh R, Rai UN. Growth performance and biochemical responses of three rice (Oryza sativa L.) cultivars grown in fly-ash amendment soil. Chemosphere, 2007, 67: 140-151

[29] Farmer EE, Mueller MJ. ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol, 2013, 64: 429-450

[30] Freeman JL, Garcia D, Ki D, Hopf A, Salt DE. Constitutively elevated salicyclic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol, 2005, 137(3): 1082-1091

[31] Freeman JL, Tamaoki M, Stushnoff C. Molecular mechanisms of selenium tolerance and hyper accumulation in Stanleya pinnata. Plant Physiol, 2010, 153(4): 1630-1652

[32] Gajewska E, Sklodowska M, Slaba M, Mazur J. Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant, 2006, 50: 653-659

[33] Gajic G Ecological potential of plants for phytoremediation and ecorestoration of fly ash deposits and mine wastes. Front Environ Sci, 2018, 6: 124

[34] Gangolff WJ, Ghodrati M, Sims JT, Vasilas BL. Impact of fly ash amendments and incorporation method of hydraulic properties of sandy soil. Water Air Soil Pollut, 2010, 119(1–4): 231-245

[35] Gautam S, Singh A, Singh J, Shikha Effect of fly ash amended soil on growth and yield of Indian Mustard (Brassica juncea). Adv Biores, 2012, 3(4): 39-45

[36] Georgiadou EC, Kowalska E, Patla K, Kulbat K, Smolinska B, Leszczynska J, Fotopoulos V. Influence of heavy metals (Ni, Cu, and Zn) on nitro-oxidative stress responses, proteome regulation and allergen production in Basil (Ocimum basilicum L.) plants. Front. Plant Sci., 2018, 9(862): 1-16

[37] Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem, 2010, 48(12): 909-930

[38] Gjorgieva D, Kadifkova T, Tatjana R, Ruskovska T, BaIeva K, Stafilov T. Influence of heavy metal stress on antioxidant status and DNA damage in Urtica dioica. Biomed Res Int, 2013

[39] Gond DP, Pal A, Singh S. Growth performance and biochemical responses of tomato (Lycopersicon esculentum Mill.) grown in fly ash amended soil. J Ecophysiol Occup Health, 2011, 11: 123-130

[40] Gratão PL, Polle A, Lea PJ, Azevedo RA. Making the life of heavy metal stressed plants a little easier. Funct Plant Biol, 2005, 32: 481-494

[41] Gupta AK, Sinha S. Role of Brassica juncea L. Czern. (var. vaibhav) in the phytoextraction of Ni from soil amended with fly-ash, selection of extractant for metal bioavailability. J Hazard Mater, 2006, 136: 371-378

[42] Gupta AK, Sinha S. Decontamination and/or revegetation of fly ash dykes through naturally growing plants. J Hazard Mater, 2008, 153: 1078-1087

[43] Gupta AK, Sinha S. Growth and metal accumulation response of Vigna radiate L. var PDM 54 (mung bean) grown on fly ash- amended soil: effect on dietary intake. Environ Geochem Health, 2009, 31: 463-473

[44] Gupta AK, Mishra RK, Sinha S, Lee BK. Growth, metal accumulation and yield performance of Brassica campestris L. (cv. Pusa Jaikisan) grown on soil amended with tannery sludge/fly ash mixture. Ecol Eng, 2010, 36(8): 981-991

[45] Hall JL. Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot, 2002, 53(366): 1-11

[46] Hamid N, Bukhari N, Jawaid F. Physiological responses of Phaseolus vulgaris in different lead concentration. Pak J Bot, 2010, 42: 239-246

[47] Hassan Z, Aarts MGM. Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot, 2011, 72: 53-63

[48] He J, Qin J, Long L, Ma Y, Li H, Li K, Jiang X, Liu T, Polle A, Liang Z. Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus × canescens. Physiol Plant, 2011, 143: 50-63

[49] Hechmi N, Ben Aissa N, Abdenaceur H, Jedidi N. Uptake and bioaccumulation of pentachlorophenol by emergent wetland plant Phragmites australis (common reed) in cadmium co-contaminated soil. Int J Phytoremediation., 2015, 17: 109-116

[50] Henrique F, Rabêlo S, Borgo L. Changes caused by heavy metals in micronutrient content and antioxidant system of forage grasses used for phytoremediation: an overview. Ciência Rural., 2016, 46(8): 1368-1375

[51] Honghua H, Dong Z, Peng Q, Wang X, Fan C, Zhang X. Impact of coal fly ash on plant growth and accumulation of essential nutrients and trace elements by alfalfa (Medicago sativa) grown in a losessial soil. J Environ Manag, 2017, 197: 428-439

[52] Howladar MF, Islam MR. A study on physico-chemical properties and uses of coal ash of Barapukuria coal fired thermal power plant, Dinajpur, for environmental sustainability. Energy Ecol Environ, 2016, 1(4): 233-247

[53] Islam MM, Hoque M, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y. Exogenous proline and glycine betaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol, 2009, 166: 1587-1597

[54] Jambhulkar HP, Shaikh SMS, Kumar S. Fly ash toxicity, emerging issues and possible implications for its exploitation in agriculture; Indian scenario: a review. Chemosphere, 2018, 213: 333-344

[55] Jiang W, Liu D. Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biol, 2010, 10: 40

[56] Jukny R, Vitkauskaite G, Racaite M, Vencloviene J. The impacts of heavy metals on oxidative stress and growth of spring barley. Cent Eur J Biol, 2012, 7(2): 299-306

[57] Junaid M, Adnan M, Khan N, Khan N, Rahman M, Ali N. Plant growth, biochemical, characteristics and heavy metals contents of Medicago sativa L., Brassica juncea (L.) Czern and Cicer arietinum. Fuuast J Biol, 2013, 3(2): 5-103

[58] Kachout SS, Mansoura AB, Leclerc JC, Mechergui R, Rejeb MN, Ouerghi Z. Effects of heavy metal on antioxidant activities of Atriplex hortensis and A. rosea. J. Food Agricul Environ., 2009, 7(4): 938-945

[59] Kafel A, Nadgorska-Socha A, Gospodarek J, Babczyńska A, Skowronek M, Kandziora M, Rozpedek K. The effects of Aphis fabae infestation on the antioxidant response and heavy metal content in field grown Philadelphus coronarius plants. Sci Total Environ, 2010, 408(5): 1111-1119

[60] Karthik S, Kumar AE, Gowtham P, Elango G, Gokul D, Thangaraj S. Soil stabilization by using fly ash. IOSR- J Mech Civ Eng, 2014, 10(6): 20-26

[61] Kim YH, Lee HS, Kwak SS. Differential responses of sweet potato peroxidases to heavy metals. Chemosphere, 2010, 81: 79-85

[62] Kim S-H, Jung M-Y, Lee Y-M. Effect of heavy metals on the antioxidant enzymes in the marine ciliate Euplotes crassus. Toxicol Environ Health Sci, 2012, 3(4): 213-219

[63] Kisa D. The responses of antioxidant system against the heavy metal-induced stress in tomato. J Nat Appl Sci, 2018, 22(1): 1-6

[64] Kishor P, Ghosh AK, Kumar D. Use of flyash in agriculture: a way to improve soil fertility and its productivity. Asian J Agric Res, 2010, 4: 1-14

[65] Krzesłowska M, Lenartowska M, Mellerowicz EJ, Samardakiewicz S, Woźny A. Pectinous cell wall thickenings formation—A response of moss protonemata cells to lead. Environ Exp Bot, 2009, 65: 119-131

[66] Krzesłowska M, Lenartowska M, Samardakiewicz S, Bilski WA. Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable–a remobilization can occur. Environ Pollut, 2010, 158: 325-338

[67] Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ. The effect of pH on metal accumulation in two Alyssum species. J Environ Qual, 2004, 33: 2090-2102

[68] Kulbat K, Leszczyńska J. Antioxidants as a defensive shield in thyme (Thymus vulgaris L.) grown on the soil contaminated with heavy metals. Biotechnol Food Sci., 2016, 80(2): 109-117

[69] Kumar A, Vajpayee P, Ali MB, Tripathi RD, Singh N, Rai UN, Singh SN. Biochemical responses of Cassia siamea Lamk. grown on coal combustion residue (Fly-ash). Bull Environ Contam Toxicol, 2002, 68: 675-683

[70] Lee S, Moon JS, Domier LL, Korban SS. Molecular characterization of phytochelatin synthase expression in transgenic Arabidopsis. Plant Physiol Biochem, 2002, 40(9): 727-733

[71] Lewis S, Donkin ME, Depledge MH. Hsp70 expression in Enteromorpha intestinalis (Chlorophyta) exposed to environmental stressors. Aquat Toxicol, 2001, 51: 277-291

[72] Li HF, Gray C, Mico C, Zhao FJ, McGrath SP. Phytotoxicity and bioavailability of cobalt to plants in a range of soils. Chemosphere, 2009, 75: 979-986

[73] Li N, Liu R, Chen J, Wang J, Hou L, Zhou Y. Enhanced phytoremediation of PAHs and cadmium contaminated soils by a Mycobacterium. Sci Total Environ, 2020

[74] Liang HM, Lin TH, Chiou JM, Yeh KC. Model evaluation of the phytoextraction potential of heavy metal hyperaccumulators and non-hyperaccumulators. Environ Pollut, 2009, 157(6): 1945-1952

[75] Lin M, Ning XA, An T, Zhang J, Chen C, Ke Y, Liu J Degradation of polycyclic aromatic hydrocarbons (PAHs) in textile dyeing sludge with ultrasound and Fenton processes: effect of system parameters and synergistic effect study. J Hazard Mater, 2016, 307: 7-16

[76] Lomonte C, Sgherri C, Baker AJM, Kolev SD, Navari-Izzo F. Antioxidative response of Atriplex codonocarpa to mercury. Environ Exp Bot, 2010, 69: 9-16

[77] Majer BJ, Tscherko D, Paschke A. Effects of heavy metal contamination of soils on micronucleus induction in Tradescantia and on microbial enzyme activities: a comparative investigation. Mutat Res, 2002, 515(1–2): 111-124

[78] Malecka A, Piechalak A, Mensinger A, Hanć A, Barałkiewicz D, Tomaszewska B. Antioxidative defense system in Pisum sativum roots exposed to heavy metals (Pb, Cu, Cd, Zn). Pol J Environ Stud, 2012, 21(6): 1721-1730

[79] Manan FA, Mamat DD, Samad AA, Ong YS, Ooh KF, Chai TT. Heavy metal accumulation and antioxidant properties of Nephrolepis biserrata growing in heavy metal-contaminated soil. Glob Nest J, 2015, 17(1): 1-11

[80] Martins LL, Mourato MP, Cardoso AI, Pinto AP, Mota AM, Goncalves MLS, De Varennes A. Oxidative stress induced by cadmium in Nicotiana tabacum L.: effects on growth parameters, oxidative damage and antioxidant responses in different plant parts. Acta Physiol Plant, 2011, 33(4): 1375-1383

[81] Michalak A. Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud, 2006, 15(4): 523-530

[82] Mishra M, Sahu RK, Padhy RN. Growth, yield and elemental status of rice (Oryza sativa) grown in fly ash amended soils. Ecotoxicology, 2007, 16: 271-278

[83] Mithofer A, Schulze B, Boland W. Bio tic and heavy metal stress response in plants: evidence for common signals. FEBS Lett, 2004, 566: 1-5

[84] Mourato M, Reis R, Martins LL. Montanaro G, Dichio B. Characterization of plant antioxidative system in response to abiotic stresses: a focus on heavy metal toxicity. Advances in selected plant physiology aspects, 2012 Vienna InTech 23-44

[85] Muthusaravanan S, Sivarajasekar N, Vivek JS, Paramasivan T, Naushad M, Prakashmaran J, Gayathri V, Al Duaij OK. Phytoremediation of heavy metals: mechanisms, methods and enhancements. Environ Chem Lett, 2018, 16(4): 1339-1359

[86] Nadgorska-Socha A, Kafel A, Kandziora-Ciupa M, Gospodarek J, Zawisza-Raszka A. Accumulation of heavy metals and antioxidant responses in Vicia faba plants grown on non-metallic contaminated soil. Environ Sci Pollut Res, 2013, 20: 1124-1134

[87] Neves SB, Soares C, Sousa A, Martins V, Azenha M, Geros H, Fidalgo F. An efficient antioxidant system and heavy metal exclusion from leaves make Solanum cheesmaniae more tolerant to Cu than its cultivated counterpart. Food Energy Security., 2017, 6(3): 123-133

[88] Panda D, Tikadar P. Effect of fly ash incorporation in soil on germination and seedling characteristics of rice (Oryza sativa L.). Int Q J Biol Life Sci, 2014, 2(3): 800-807

[89] Panda SK, Chaudhary I, Khan MH. Heavy metals induce lipid peroxidation and affect antioxidants in wheat leaves. Biol Plant, 2003, 2: 289-294

[90] Panda D, Mandal L, Barik J. Phytoremediation potential of naturally growing weed plants grown on fly ash-amended soil for restoration of fly ash deposit. Int J Phytorem, 2020

[91] Pandey N, Pathak GC, Pandey DK, Pandey R. Heavy metals Co, Ni, Cu, Zn and Cd, produces oxidative damage and evoke differential antioxidant responses in Spinach. Braz J Plant Physiol, 2009, 21(2): 103-111

[92] Pandey VC, Abhilash PC, Upadhayay RN, Tewari DD. Application of fly ash on the growth performance and translocation of toxic heavy metals within Cajanus cajan L. Implication for safe utilization of fly ash for agricultural production. J Hazard Mater, 2009, 166: 255-259

[93] Pandey VC, Singh JS, Kumar Tiwari DD. Accumulation of heavy metals by Chickpea grown in fly ash treated soil: effect on antioxidants. CLEAN Soil Air Water, 2010, 38(12): 1116-1123

[94] Pani NK, Samal P, Das R, Sahoo S. Effect of fly ash on growth and yield of sunflower (Helianthus annus L.). Int. J. agro and Agricult. Res., 2015, 7(2): 64-74

[95] Pant PP, Tripathi AK. Impact of heavy metals on morphological and biochemical parameters of Shorea robusta plant. Ekológia (Bratislava), 2014, 33(2): 116-126

[96] Parida AK, Das AB. Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf, 2005, 60: 324-349

[97] Parlak KU. Effect of Nickel on growth and biochemical characteristics of wheat (Triticum sativum L.) seedlings. Wagening J Life Sci, 2016, 76: 1-5

[98] Pascual JA, Garcia C, Hernandez T, Moreno JL, Ros M. Soil microbial activity as a biomarker of degradation and remediation processes. Soil Biol Biochem, 2000, 32: 1877-1883

[99] Pathan SM, Aylmore LAG, Colmer TD. Soil properties and turf growth on a sandy soil amended with fly ash. Plant Soil, 2003, 256(1): 103-114

[100] Pati SS, Sahu SK. CO₂ evaluation and enzyme activities (dehydrogenase, protease and amylase) of fly ash amended soil in presence and absence of earthworms (under laboratory condition). Geo Derma, 2004, 118: 289-301

[101] Patra M, Bhowmik N, Bandopadhyay B, Sharma A. Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Indian Acad Sci, 2004, 3: 199-223

[102] Plackova A, Geneva M, Markovska Y, Salamon I, Stancheva I. Antioxidant potential of Marigold (Calendula officinalis Linn.) flowers grown in Slovakia and Bulgaria. Eur J Plant Sci Biotechnol, 2010, 4(1): 145-149

[103] Pohanka M. Alzheimer’s disease and oxidative stress. A review. Curr Med Chem, 2014, 21(3): 356-364

[104] Pohanka M. Copper, aluminum, iron and calcium inhibit human acetyl cholinesterase in vitro. Environ Toxicol Pharmacol, 2014, 37(1): 455-459

[105] Pourrut B, Pohu AL, Pruvot C, Garcon G, Verdin A, Waterlot C, Bidar G, Shirali P, Douay F. Assessment of fly ash-aided phytostabilisation of highly contaminated soils after an 8-year field trial Part 2. Influence on plants. Sci Total Environ, 2011, 409: 4504-4510

[106] Prabhakar J, Dendorkar N, Morchhale RK. Influence of fly ash on strength behavior of typical soils. Constr Build Mater, 2004, 18: 263-267

[107] Prasad SM, Dwivedi R, Zeeshan M. Growth, photosynthetic electron transport, and antioxidant responses of young soybean seedlings to simultaneous exposure of nickel and UV-B stress. Photosynthetica, 2005, 2: 177-185

[108] Prasad SSD, Raju AVRG, Mallikarjuna K, Hephzibah G, Kumar NV. Impact of thermal fly ash and cow dung on growth, yield and metal residues in Solanum melongena. Asian J Plant Sci Res, 2016, 6(5): 1-4

[109] Rahman H, Sabreen S, Alam S, Kawai S. Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution. J Plant Nutr, 2005, 28: 393-404

[110] Rahmawati NUS, Sutopo NR, Yulia N, Eko H. Phytotoxicity of coal fly ash on plant growth and heavy metal uptake by plant in an acid soil. J Degrad Min Land Manag, 2020, 7(3): 2233-2240

[111] Raj S, Mohan S. Impact on proline content of Jatropha curcas in fly ash amended soil with respect to heavy metals. Int J Pharm Sci, 2016, 8(5): 244-247

[112] Raj S, Mohan S. Influence of metal uptake from fly ash on the growth of Jatropha curcas plant: bulk utilization approach. Int J Pharma Biosci, 2018, 9(2): 154-159

[113] Raj S, Dahiya P, Mohan S. Physico-chemical analysis and in vivo antibacterial activity of Jatropha curcas grown in fly ash amended soil. Int J Appl Environ Sci, 2015, 10(4): 1375-1383

[114] Rao SN. Effect of fly ash of on certain biochemical parameters of Coleus forskohlii. Int J Appl Pure Sci Agric, 2015, 1(12): 81-84

[115] Rastgoo L, Alemzadeh A, Afsharifar A. Isolation of two novel isoforms encoding zinc- and copper-transporting P1B-ATPase from Gouan (Aeluropus littoralis). Plant Omics J, 2011, 4(7): 377-383

[116] Rautaray SK, Ghosh BC, Mittra BN. Effect of fly ash, organic wastes and chemical fertilizers on yield, nutrient uptake, heavy metal content and residual fertility in a rice-mustard cropping sequence under acid lateritic soils. Bioresour Technol, 2003, 90: 275-283

[117] Rawat K, Pathak B, Fulekar MH. Enzymatic mechanism during phytoextraction of heavy metals from fly ash amended soil. Int J Sci Ind Res, 2015, 6(4): 1041-1055

[118] Reddy AM, Kumar SG, Jyonthsnakumari G, Thimmanaik S, Sudhakar C. Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum L.). Chemosphere, 2005, 60: 97-104

[119] Rees F, Germain C, Sterckean T, Morel JL. Plant growth and metal uptake by a non-hyper accumulating species (Lolium perenne) and a Cd-Zn hyperaccumulator (Noceaea caerulescens) in contaminated soils amended with biochar. Plant Soil, 2015, 395(1–2): 57-73

[120] Ruan X, Luo F, Li D, Zhang J, Liu Z, Xu W, Huang G, Li X. Cotton BCP genes encoding putative blue copper-binding proteins are functionally expressed in fiber development and involved in response to high-salinity and heavy metal stresses. Physiol Plant, 2011, 141: 71-83

[121] Sampaio CJS, de Souza JRB, Damiao AO Biodegradation of polycyclic aromatic hydrocarbons (PAHs) in a diesel oil-contaminated mangrove by plant growth- promoting rhizobacteria. 3 Biotech, 2019, 9: 155

[122] Sangwan P, Kumar V, Joshi U. Effect of Chromium (VI) Toxicity on enzymes of nitrogen metabolism in cluster beans (Cyamopsis tetragonoloba L.). Enzyme Res, 2014, 7: 836-840

[123] Sao S, Sahu PK. Influence of fly ash and growth regulator with soil for determination of chlorophyll in Arachis hypogea L. Am J Plant Sci, 2013, 4: 1744-1749

[124] Saraswat PK, Chaudhary K. Effect of fly ash (FA) to improving soil quality and increase the efficiency of crop productivity. Eur J Biotechnol Biosci, 2014, 2(6): 72-78

[125] Schutzendubel A, Polle A. Plants response to abiotic stresses: heavy metal induced oxidative stress and protection by mycorrhization. J Exp Bot, 2001, 53(372): 1351-1365

[126] Shahid M, Dumat C, Pourrut B, Silvestre J, Laplanche C, Pinelli E. Influence of EDTA and citric acid on lead-induced oxidative stress to Vicia faba roots. J Soils Sediments, 2013

[127] Shahid M, Dumat C, Pourrut B, Sabir M, Pinelli E. Assessing the effect of metal speciation on lead toxicity to Vicia faba pigment contents. J Geochem Explor, 2014, 144: 290-297

[128] Shakeel A, Khan AA, Hakeem KR. Growth, biochemical, and antioxidant response of beetroot (Beta vulgaris L.) grown in fly ash-amended soil. SN Appl Sci, 2020, 2: 1378

[129] Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S. Chromium toxicity in plants. Environ Int, 2005, 31: 739-753

[130] Sharma P, Dubey RS. Lead toxicity in plants. Braz J Plant Physiol, 2005, 17: 35-52

[131] Sharma SK, Kalra N, Singh GR. Soil physical and chemical properties as influenced by fly ash addition in soil and yield of wheat. J Sci Ind Res, 2002, 61(8): 617-620

[132] Sharma DC, Sharma CP, Tripathi RD. Phytotoxic lesions of zinc in maize. Chemosphere, 2003, 51: 63-68

[133] Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot, 2012

[134] Singh DK, Gupta T. Effect through inhalation on human health of PM1 bound polycyclic aromatic hydrocarbons collected from foggy days in northern part of India. J Hazard Mater, 2016, 306: 257-268

[135] Singh S, Prasad SM. Growth, photosynthesis and oxidative responses of Solanum melongena L. seedlings to cadmium stress: mechanism of toxicity amelioration by kinetin. Sci Hortic, 2014, 176: 1-10

[136] Singh M, Kumar J, Singh S, Singh VP, Prasad SM, Singh MPVVB. Adaptation strategies of plants against heavy metal toxicity: a short review. Biochem Pharmacol, 2015, 4(2): 1-7

[137] Sinha S, Gupta AK. Translocation of metals from fly ash amended soil in the plant of Sesbania cannabina L. Ritz: effect on antioxidants. Chemosphere, 2005, 61(8): 1204-1214

[138] Sinha D, Sharma S, Dwivedi MK. The impact of fly ash on photosynthetic activity and medicinal property of plants. Int J Curr Microbiol Appl Sci, 2013, 2(8): 382-388

[139] Smeets K, Ruytinx J, Semane B, Van Belleghem F, Remans T, Van Sanden S, Vangronsveld J, Cuypers A. Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot, 2008, 63: 1-8

[140] Stankovic S, Kalaba P, Stankovic AR. Biota as toxic metal indicators. Environ Chem Lett, 2014, 12(1): 63-84

[141] Swaminathan MS. Biodiversity: an effective safety net against environmental pollution. Environ Pollut, 2003, 126(3): 287-291

[142] Thakare PB, Chaudhary MD, Pokale WK. Physico-chemical characterization of fly ash and its effect on the growth of soyabean plant (Glycine max). Int J Res Biosci Agric Technol, 2014, 2(1): 1262-1270

[143] Tiwari S, Kumari B, Singh SN. Evaluation of metal mobility/immobility in fly ash induced by bacterial strains isolated from the rhizospheric zone of Typha latifolia growing on fly ash dumps. Bioresour Technol, 2008, 99: 1305-1310

[144] Vajpayee P, Tripathi RD, Rai UN, Ali MB, Singh SN. Chromium accumulation reduces chlorophyll biosynthesis, nitrate reductase activity and protein content in Nympaea alba L. Chemosphere, 2000, 41: 1075-1082

[145] Van Bussel CGJ, Schroeder JP, Mahlmann L, Schulz C. Aquatic accumulation of dietary metals (Fe, Zn, Cu Co, Mn) in recirculating aquaculture systems (RAS) changes body composition but not performance and health of juvenile turbot (Psetta maxima). Aquacult Eng, 2014, 61: 35-42

[146] Vanhoudt N, Vandenhove H, Horemans N, Remans T, Opdenakker K, Smeets K, Bello DM, Wannijn J, Van Hees M, Vangronsveld J. Unraveling uranium induced oxidative stress related responses in Arabidopsis thaliana seedlings. Part I: responses in the roots. J Environ Radioact, 2011, 102: 630-637

[147] Varshney A, Dahiya P, Singh N, Mohan S. Variations in morphological parameters and pigment content of Calendula officinalis grown in fly ash amended soil. Plant Archives, 2019, 19(2): 2959-2963

[148] Velickovic JM, Dimitrijevic DS, Mitic SS, Mitic MN. The determination of phenolic composition, antioxidative activity and the heavy metals in the extracts of Calendula officinalis L. Adv Technol, 2014, 3(2): 46-51

[149] Viehweger K. How plants cope with heavy metals. Bot Stud, 2014, 55(35): 1-12

[150] Vijayalakshmi VK, Revathi K, Sudha PN. Comparative studies on the effect of antioxidant properties of the plants Helianthus annus and Solanum nigrum exposed to the heavy metal chromium. J Pharm Sci Res, 2010, 2(12): 889-895

[151] Winquist E, Jorklof K, Schultz E, Rasanen M, Salonen K, Anasonye F, Cajthaml T, Steffen KT, Jorgensen KS, Tuomela M. Bioremediation of PAH-contaminated soil with fungi- From laboratory to field scale. Int Biodeterior Biodegrad, 2013, 86: 238-247

[152] Wojas S, Clemens S, Skodowska A, Antosiewicz DM. Arsenic response of AtPCS1- and CePCS-expressing plants—effects of external As (V) concentration on As-accumulation pattern and NPT metabolism. J Plant Physiol, 2010, 167: 169-175

[153] Yadav SK. Heavy metal toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South Afr J Bot, 2010, 76: 167-179

[154] Yadav VK, Fulekar MH. The current scenario of thermal power plants and fly ash: production and utilization with a focus in India. Int J Adv Eng Res Dev, 2018, 5(4): 2348-6406

[155] Yadav B, Bajaj A, Saxena M. Impact of fly ash on physical properties of waterlogged soil, plant growth and root yield of Withania somnifera (L.) Dunal (Ashwagandha). Int J Curr Res Biosci Plant Biol, 2014, 1(5): 58-70

[156] Zenk MH. Heavy metal detoxification in higher plants -a review. Gene, 1996, 179(21): 30

[157] Zhang X, Gao B, Xia H. Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of bana grass and vetiver grass. Ecotoxicol Environ Saf, 2014, 106: 102-108

[158] Zhang XF, Zhang XH, Gao B, Zhian L, HanPing X, HaiFang L, Jian L. Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of an energy crop, king grass (Pennisetum americanum x P. purpureum). Biomass Bioenerg, 2014, 67: 179-187

[159] Zhou ZS, Huang SQ, Guo K, Mehta SK, Zhang PC, Yang ZM. Metabolic adaptations to zinc-induced oxidative stress in roots of Medicago sativa L. J Inorg Biochem, 2007, 101: 1-9

Funding

Council for Science and Technology Policy(CST/AAS/D-4995)