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Nickel accumulation and its effect on growth, physiological and biochemical parameters in millets and oats

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Abstract

With the boom in industrialization, there is an increase in the level of heavy metals in the soil which drastically affect the growth and development of plants. Nickel is an essential micronutrient for plant growth and development, but elevated level of Ni causes stunted growth, chlorosis, nutrient imbalance, and alterations in the defense mechanism of plants in terms of accumulation of osmolytes or change in enzyme activities like guiacol peroxidase (POD), catalase (CAT), and superoxide dismutase (SOD). Ni-induced toxic response was studied in seedlings of finger millet, pearl millet, and oats in terms of seedling growth, lipid peroxidation, total chlorophyll, proline content, and enzymatic activities. On the basis of germination and growth parameters of the seedling, finger millet was found to be the most tolerant. Nickel accumulation was markedly lower in the shoots as compared to the roots, which was the highest in finger millet and the lowest in shoots of oats. Plants treated with a high concentration of Ni showed significant reduction in chlorophyll and increase in proline content. Considerable difference in level of malondialdehyde (MDA) content and activity of antioxidative enzymes indicates generation of redox imbalance in plants due to Ni-induced stress. Elevated activities of POD and SOD were observed with high concentrations of Ni while CAT activity was found to be reduced. It was observed that finger millet has higher capability to maintain homeostasis by keeping the balance between accumulation and ROS scavenging system than pearl millet and oats. The data provide insight into the physiological and biochemical changes in plants adapted to survive in Ni-rich environment. This study will help in selecting the more suitable crop species to be grown on Ni-rich soils.

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References

  • Adrees M, Ali S, Rizwan M, Ibrahim M, Abbas F, Farid M, Zia-ur-Rehman M, Irshad MK, Bharwana SA (2015) The effect of excess copper on growth and physiology of important food crops: a review. Environ Sci Pollut Res 22:8148–8162

    Article  CAS  Google Scholar 

  • Afshan S, Ali S, Bharwana SA, Rizwan M, Farid M, Abbas F, Ibrahim M, Mehmood MA, Abbasi GH (2015) Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L. Environ Sci Pollut Res 22:11679–11689

    Article  CAS  Google Scholar 

  • Ahmad MSA, Ashraf M (2012) Essential roles and hazardous effects of nickel in plants. Rev Environ Contam Toxicol 214:pp125–pp167

    Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress. J Exp Bot 53:1331–1341

    Article  CAS  Google Scholar 

  • Amadou I, Gounga ME, Le G-W (2013) Millets: nutritional composition, some health benefits and processing—a review. Emirates J Food Agric 25:501

    Article  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1

    Article  CAS  Google Scholar 

  • Arshad M, Ali S, Noman A, Ali Q, Rizwan M, Farid M, Irshad MK (2016) Phosphorus amendment decreased cadmium (Cd) uptake and ameliorates chlorophyll contents, gas exchange attributes, antioxidants, and mineral nutrients in wheat (Triticum aestivum L.) under Cd stress. Arch Agron Soil Sci 62:533–546

    Article  CAS  Google Scholar 

  • Asada K (1992) Ascorbate peroxidase—a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241

    Article  CAS  Google Scholar 

  • Asopa PP, Bhatt R, Sihag S, Kothari S, Kachhwaha S (2016) Effect of cadmium on physiological parameters of cereal and millet plants—a comparative study. Int J Phytoremediation, 00-00

  • Assche FV, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206

    Article  Google Scholar 

  • Baccouch S, Chaoui A, El Ferjani E (2001) Nickel toxicity induces oxidative damage in Zea mays roots. J Plant Nutr 24:1085–1097

    Article  CAS  Google Scholar 

  • Bai C, Liu L, Wood BW (2013) Nickel affects xylem Sap RNase A and converts RNase A to a urease. BMC Plant Biol 13:1

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  Google Scholar 

  • Ben Halima N, Khemakhem B, Fendri I, Ogata H, Baril P, Pichon C, Abdelkafi S (2016) Identification of a new oat β amylase by functional proteomics. Biochim Biophys Acta 1864:52–61

    Article  CAS  Google Scholar 

  • Ben Halima N, Borchani M, Fendri I, Khemakhem B, Gosset D, Baril P, Pichon C, Ayadi MA, Abdelkafi S (2015a) Optimized amylases extraction from oat seeds and its impact on bread properties. Int J Biol Macromol 72:1213–1221

    Article  CAS  Google Scholar 

  • Ben Halima N, Ben Saad R, Khemakhem B, Fendri I, Abdelkafi S (2015b) Oat (Avena sativa L.): oil and nutriment compounds valorization for potential use in industrial applications. J Oleo Sci 64:915932

    Google Scholar 

  • Bhaduri AM, Fulekar M (2012) Antioxidant enzyme responses of plants to heavy metal stress. Rev Environ Sci Biotechnol 11:55–69

    Article  CAS  Google Scholar 

  • Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. New Phytol 156:205–215

    Article  CAS  Google Scholar 

  • Clarkson DT, Luttge U (1989) Mineral nutrition: divalent cations, transport and compartmentation. Prog Bot 51:93–112

    Google Scholar 

  • Echevarria G, Massoura ST, Sterckeman T, Becquer T, Schwartz C, Morel JL (2006) Assessment and control of the bioavailability of nickel in soils. Environ Toxicol Chem 25:643–651

    Article  CAS  Google Scholar 

  • Edreva AM, Georgieva ID, Cjholakova NI (1989) Pathogenic and non-pathogenic stress effects on peroxidases in leaves of tobacco. Environ Exp Bot 29:365–377

    Article  CAS  Google Scholar 

  • EFSA CONTAM Panel (EFSA Panel on Contaminants in the Food Chain) (2015) Scientific opinion on the risks to public health related to the presence of nickel in food and drinking water. EFSA J 13:202 http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32016H1111, http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32016H1110

    Google Scholar 

  • Elstner EF (1982) Oxygen activation and oxygen toxicity. Ann Rev Plant Physiol 33:73–96

    Article  CAS  Google Scholar 

  • FAO (Food and Agriculture Organization) (2014) http://www.fao.org/faostat/en/#data/QC Accessed 10 November 2016

  • Fendri I, Ben Saad R, Khemakhem B, Ben Halima N, Gdoura R, Abdelkafi S (2013) Effect of treated and untreated domestic wastewater on seed germination, seedling growth, amylase and lipase activities in Avena sativa L. J Sci Food Agric 93:1568–1574

    Article  CAS  Google Scholar 

  • Flora S, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res 128:501

    CAS  Google Scholar 

  • Gabbrielli R, Pandolfini T, Vergnano O (1987) Peroxidase involvement in tolerance mechanisms. G Bot Ital 21:200–201

    Google Scholar 

  • Gajewska E, Skłodowska M (2005) Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 27:329–340

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M, Słaba M (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50:653–659

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M (2007a) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20:27–36

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M (2007b) Relations between tocopherol, chlorophyll and lipid peroxides contents in shoots of Ni-treated wheat. J Plant Physiol 164:364–366

    Article  CAS  Google Scholar 

  • Ghasemi F, Heidari R, Jameii R, Purakbar L (2012) Effects of Ni2+ toxicity on Hill reaction and membrane functionality in maize. J Stress Physiol Biochem, 8

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

    Article  CAS  Google Scholar 

  • Gimeno-García E, Andreu V, Boluda R (1996) Heavy metals incidence in the application of inorganic fertilizers and pesticides to rice farming soils. Environ Pollut 92:19–25

    Article  Google Scholar 

  • Gupta N, Srivastava A, Pandey V (2012) Biodiversity and nutraceutical quality of some indian millets. Proceed Natl Acad Sci India Section B: Biological Sci 82:265–273

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicles in biology and medicine, 4th edn. Oxford University Press, New York

    Google Scholar 

  • Hanif MA, Nadeem R, Rashid U, Zafar MN (2005) Assessing pollution levels in effluents of industries in city zone of Faisalabad, Pakistan. J Appl Sci 5:1713–1717

    Article  CAS  Google Scholar 

  • Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266

    Article  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation Archives of biochemistry and biophysics. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Hossein Khoshgoftarmanesh A, Bahmanziari H (2012) Stimulating and toxicity effects of nickel on growth, yield, and fruit quality of cucumber supplied with different nitrogen sources. J Plant Nutr Soil Sci 175:474–481

    Article  CAS  Google Scholar 

  • Ishtiaq S, Mahmood S (2012) Phytotoxicity of nickel and its accumulation in tissues of three Vigna species at their early growth stages. J Appl Bot Food Qual 84:223

    Google Scholar 

  • Izosimova A (2005) Modelling the interaction between calcium and nickel in the soil-plant system. Bundesforschungsanstalt für Landwirtschaft (FAL), German

    Google Scholar 

  • Kaul S, Sharma S, Mehta I (2008) Free radical scavenging potential of L-proline: evidence from in vitro assays. Amino Acids 34:315–320

    Article  CAS  Google Scholar 

  • Khan MR, Khan MM (2010) Effect of varying concentration of nickel and cobalt on the plant growth and yield of chickpea. Aust J Basic Appl Sci 4:1036–1046

    CAS  Google Scholar 

  • Khellaf N, Zerdaoui M (2010) Growth response of the duckweed Lemna gibba L. to copper and nickel phytoaccumulation. Ecotoxicology 19:1363–1368

    Article  CAS  Google Scholar 

  • Küpper H, Kroneck PM (2007) Nickel in the environment and its role in the metabolism of plants and cyanobacteria. Met Ions Life Sci 2:31–62

    Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    Article  CAS  Google Scholar 

  • Lin CC, Kao CH (2000) Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul 30:151–155

    Article  CAS  Google Scholar 

  • Ling W, Shen Q, Gao Y, Gu X, Yang Z (2007) Use of bentonite to control the release of copper from contaminated soils. Aust J Soil Res 45:618–623

    Article  CAS  Google Scholar 

  • Maheshwari R, Dubey R (2009) Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 59:37–49

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Zarcinas BA, Stevens DP, Cook N (2000a) Soil testing for heavy metals. Commun Soil Sci Plant Anal 31:1661–1700

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Hamon RE, McLaren RG, Speir TW, Rogers SL (2000b) Review: a bioavailability-based rationale for controlling metal and metalloid contamination of agricultural land in Australia and New Zealand. Aust J Soil Res 38:1037–1086

    Article  CAS  Google Scholar 

  • Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Botany 61(15):4197–4220. doi:10.1093/jxb/erq282

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  Google Scholar 

  • Nagajyoti P, Lee K, Sreekanth T (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216

    Article  CAS  Google Scholar 

  • Nouairi I, Ammar WB, Youssef NB, Miled DDB, Ghorbal MH, Zarrouk M (2009) Antioxidant defense system in leaves of Indian mustard (Brassica juncea) and rape (Brassica napus) under cadmium stress. Acta Physiol Plant 31:237–247

    Article  CAS  Google Scholar 

  • Pandey N, Sharma CP (2002) Effect of heavy metals Co 2+, Ni 2+ and Cd 2+ on growth and metabolism of cabbage. Plant Sci 163:753–758

    Article  CAS  Google Scholar 

  • Pietrini F, Iori V, Cheremisina A, Shevyakova NI, Radyukina N, Kuznetsov VV, Zacchini M (2015) Evaluation of nickel tolerance in Amaranthus paniculatus L. plants by measuring photosynthesis, oxidative status, antioxidative response and metal-binding molecule content. Environ Sci Pollut Res 22:482–494

    Article  CAS  Google Scholar 

  • Poonkothai M, Vijayavathi BS (2012) Nickel as an essential element and a toxicant. Int J Environ Sci 1:285–288

    Google Scholar 

  • Racusen D, Foote M (1965) Protein synthesis in dark-grown bean leaves. Can J Bot 43:817–824

    Article  CAS  Google Scholar 

  • Rahman H, Sabreen S, Alam S, Kawai S (2005) Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution. J Plant Nutr 28:393–404

    Article  CAS  Google Scholar 

  • Rao KM, Sresty T (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  Google Scholar 

  • Raskin I, Kumar PBAN, Dushenkov S, Salt DE (1994) Bioconcentration of heavy metals by plants. Curr Opin Biotechnol 5:285–290

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Saleh AS, Zhang Q, Chen J, Shen Q (2013) Millet grains: nutritional quality, processing, and potential health benefits. Compr Rev Food Sci Food Saf 12:281–295

    Article  CAS  Google Scholar 

  • Schat H, Sharma SS, Vooijs R (1997) Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiol Plant 101:477–482

    Article  CAS  Google Scholar 

  • Schickler H, Caspi H (1999) Response of antioxidative enzymes to nickel and cadmium stress in hyperaccumulator plants of the genus Alyssum. Physiol Plant 105:39–44

    Article  CAS  Google Scholar 

  • Seregin I, Kozhevnikova A (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277

    Article  CAS  Google Scholar 

  • 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. J Exp Bot 57:711–726

    Article  CAS  Google Scholar 

  • Shen Z, Li X, Wang C, Chen H, Chua H (2002) Lead phytoextraction from contaminated soil with high biomass plant species. J Environ Qual 31:1893–1900

    Article  CAS  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Ali HM, Sakran AM, Basalah MO, AlKhaishany MY (2013) Mitigation of nickel stress by the exogenous application of salicylic acid and nitric oxide in wheat. Aust J Crop Sci 7:1780

    Google Scholar 

  • Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847

    Article  CAS  Google Scholar 

  • Sreekanth T, Nagajyothi P, Lee K, Prasad T (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Technol 10:1129–1140

    Article  CAS  Google Scholar 

  • Teranishi Y, Tanaka A, Osumi M, Fukui S (1974) Catalase activities of hydrocarbon-utilizing Candida yeasts. Agric Biol Chem 38:1213–1220

    Article  CAS  Google Scholar 

  • Thakur S, Sharma SS (2016) Characterization of seed germination, seedling growth, and associated metabolic responses of Brassica juncea L. cultivars to elevated nickel concentrations. Protoplasma 253:571–580

    Article  CAS  Google Scholar 

  • Van Assche F, Cardinaels C, Clijsters H (1988) Induction of enzyme capacity in plants as a result of heavy metal toxicity: dose-response relations in Phaseolus vulgaris L., treated with zinc and cadmium. Environ Pollut 52:103–115

    Article  Google Scholar 

  • Vigouroux Y, Barnaud A, Scarcelli N, Thuillet A-C (2011) Biodiversity, evolution and adaptation of cultivated crops. Comptes rendus biologies 334:450–457

    Article  Google Scholar 

  • Yan R, Gao S, Yang W, Cao M, Wang S, Chen F (2008) Nickel toxicity induced antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. cotyledons. Plant Soil Environ 54:294–300

    CAS  Google Scholar 

  • Yusuf M, Fariduddin Q, Hayat S, Ahmad A (2011) Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86:1–17

    Article  CAS  Google Scholar 

  • Zurayk R, Sukkariyah B, Baalbaki R, Ghanem DA (2002) Ni phytoaccumulation in Mentha aquatica L. and Mentha sylvestris L. Water Air Soil Pollut 139:355–364

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to the Council of Scientific and Industrial Research (CSIR), the Indian Council of Medical Research (ICMR), and the Rajiv Gandhi National Fellowship (RGNF) for financial support. We also express sincere thanks to DBT-IPLS facility and DRS Phase II, Department of Botany, University of Rajasthan, for providing research facilities.

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  1. Department of Botany, University of Rajasthan, Jaipur, 302004, India

    Vibha Gupta, Pradeep Kumar Jatav, Raini Verma & Sumita Kachhwaha

  2. Amity Institute of Biotechnology, Amity University Rajasthan, Jaipur, 302006, India

    Shanker Lal Kothari

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  1. Vibha Gupta
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Gupta, V., Jatav, P.K., Verma, R. et al. Nickel accumulation and its effect on growth, physiological and biochemical parameters in millets and oats. Environ Sci Pollut Res 24, 23915–23925 (2017). https://doi.org/10.1007/s11356-017-0057-4

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