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Nickel toxicity in plants: reasons, toxic effects, tolerance mechanisms, and remediation possibilities—a review

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Abstract

Nickel (Ni) is a naturally occurring metal, but anthropogenic activities such as industrialization, use of fertilizers, chemicals, and sewage sludge have increased its concentration in the environment up to undesirable levels. Ni is considered to be essential for plant growth at low concentration; however, Ni pollution is increasing in the environment, and therefore, it is important to understand its functional roles and toxic effects on plants. This review emphasizes the environmental sources of Ni, its essentiality, effects, tolerance mechanisms, possible remediation approaches, and research direction that may help in interdisciplinary studies to assess the significance of Ni toxicity. Briefly, Ni affects plant growth both positively and negatively, depending on the concentration present in the growth medium. On the positive side, Ni is essential for normal growth, enzymatic activities (e.g., urease), nitrogen metabolism, iron uptake, and specific metabolic reactions. On the negative side, Ni reduces seed germination, root and shoot growth, biomass accumulation, and final production. Moreover, Ni toxicity also causes chlorosis and necrosis and inhibits various physiological processes (photosynthesis, transpiration) and cause oxidative damage in plants. The threat associated with Ni is increased as Ni concentration increases day by day in the environment, particularly in soils; therefore, it would be hazardous for crop production in the near future. Additionally, the lack of information regarding the mechanisms of Ni tolerance in plants further intensifies this situation. Therefore, future research should be focused on approachable and prominent solutions in order to minimize the entry of Ni into our ecosystems.

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References

  • Aamer M, Muhammad UH, Li Z, Abid A, Su Q, Liu Y, Adnan R, Muhammad AUK, Tahir AK, Huang G (2018) Foliar application of glycinebetaine (GB) alleviates the cadmium toxicity in spinach through reducing Cd uptake and improving the activity of anti-oxidant system. Appl Ecol Environ Res 16:7575–7583

    Google Scholar 

  • Ahmad MSA, Hussain M, Saddiq R, Alvi AK (2007) Mungbean: a nickel indicator, accumulator or excluder. Bull Environ Contam Toxicol 78:319–324

    CAS  Google Scholar 

  • Ahmad MS, Ashraf M, Hussain M (2010) Phytotoxic effects of nickel on yield and concentration of macro- and micro-nutrients in sunflower (Helianthus annuus L.) achenes. J Hazard Mater 10:234–240

    Google Scholar 

  • Alam MM, Hayat S, Ali B, Ahmad A (2007) Effect of 28-homobrassinolide treatment on nickel toxicity in Brassica juncea. Photosynthetica 45:139–142

    Google Scholar 

  • Alexandrovn R, Costisor O, Patron I (2006) Nickel. Exp Pathol Parasitol 911:64–74

    Google Scholar 

  • Ali MA, Ashraf M, Athar HR (2009) Influence of nickel stress on growth and some important physiological/biochemical attributes in some diverse canola (Brassica napus L.) cultivars. J Hazard Mater 172:964–969

    CAS  Google Scholar 

  • Alloway BJ (1995) In heavy metal in soils (Ed: B. J. Alloway), 2nd edn. Blackie Academic and Professional, London, pp 25–34

    Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ehsanullah, Samad RA, Tung SA, Shahzad B (2015) Cadmium toxicity in maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and vcadmium accumulation. Environ Sci Pollut Res 22:17022–17030

    CAS  Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Shahzad B, Ashraf U, Fahad S, Hassan S, Jan W, Saleem MF, Khan I, Bajwa AA, Wang L, Mehmood A, Samad RA, Tung SA (2016) Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. Environ Sci Pollut Res 23(12):11864–11875

    CAS  Google Scholar 

  • Arefifars M, Mahdieh M, Mirjani M (2014) Study of the effect of nickel heavy metals on some physiological parameters of Catharanthus roseus. Nat Prod Res 28(18):1499–1502

    Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    CAS  Google Scholar 

  • Atta-Aly MA (1999) Effect of nickel addition on the yield and quality of parsley leaves. Sci Hortic 82:9–24

    CAS  Google Scholar 

  • Audet P, Charest C (2008) Allocation plasticity and plant–metal partitioning: metal-analytical perspectives in phytoremediation. Environ Pollut 156:290–296

    CAS  Google Scholar 

  • Aziz H, Sabir M, Ahmad HR, Aziz T, Rehman MZ, Hakeen KR, Ozturk M (2015) Alleviating effect of calcium on nickel toxicity in rice. Clean Soil Air Water 42(9999):1–9

    Google Scholar 

  • Baccouch S, Chaoui A, Ferjani EE (1998) Nickel-induced oxidative damage and antioxidant responses in Zea mays shoots, Plant Physiol. Biochem 36:689–694

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Bai C, Reilly CC, Wood BW (2006) Nickel deficiency disrupts metabolism of ureids, amino acids and organic acids of young pecan foliage. Plant Physiol 140:433–443

    CAS  Google Scholar 

  • Barcan V, Kovnatsky E (1998) Soil surface geochemical anomaly around the copper-nickel metallurgical smelter. Water Air Soil Pollut 103:197–218

    CAS  Google Scholar 

  • Barcelo J, Poschenrieder CH (2004) Structural and ultrastructural changes in heavy metal exposed plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystem. Springer, Berlin, pp 223–248

    Google Scholar 

  • Barceloux DG (1999) Nickel. J Toxicol Clin Toxicol 37:239–258

    CAS  Google Scholar 

  • Barker AV (2006) Nickel. In: Barker AV, Pilbeam DJ (eds) Handbook of Plant Nutrition. CRC Press

  • Barman SC, Sahu RK, Bhargava SK, Chaterjee C (2000) Distribution of heavy metals in wheat, mustard, and weed grown in field irrigated with industrial effluents. Bull Environ Contam Toxicol 64:489–496

    CAS  Google Scholar 

  • Bazihizina N, Redwan M, Taiti C, Giordano C, Monetti E, Masi E, Azzarello E, Mancuso S (2015) Root based responses account for Psidium guajava survival at high nickel concentration. J Plant Physiol 174:137–146

    CAS  Google Scholar 

  • Bhalerao SA, Amit SS, Anukthi CP (2015) Toxicity of nickel in plants. Int J Pure App Biosci 3(2):345–355

    Google Scholar 

  • Bhardwaj R, Arora N, Sharma P, Arora HK (2007) Effects of 28-homobrassinolide on seedling growth, lipid peroxidation and antioxidative enzyme activities under nickel stress in seedlings of Zea mays. Asian J Plant Sci 6:765–772

    CAS  Google Scholar 

  • Bhatia NP, Orlic I, Siegele R, Ashwath N, Baker AJM, Walsh KB (2003) Elemental mapping using PIXE shows the main pathway of nickel movement is principally symplastic within the fruit of the hyperaccumulator Stackhousia tryonii. New Phytol 160:479–488

    CAS  Google Scholar 

  • Bhatia NP, Walsh KB, Baker AJM (2005) Detection and quantification of ligands involved nickel detoxification in the herbaceous Ni hyperaccumulator Stackhousia tryonii Bailey. J Exp Bot 56:1343–1349

    CAS  Google Scholar 

  • Bishnoi NR, Sheoran IS, Singh R (1993a) Effect of cadmium and nickel on mobilization of food reserves and activities of hydrolytic enzymes in germinating pigeon pea seeds. Biol Plant 35:583–589

    CAS  Google Scholar 

  • Bishnoi NR, Sheoran IS, Singh R (1993b) Influence of cadmium and nickel on photosynthesis and water relations in wheat leaves of differential insertion levels. Photosynthetica 28:473–479

    CAS  Google Scholar 

  • Boisvert S, Joly D, Leclerc S, Govindachary S, Harnois J, Carpentier R (2007) Inhibition of the oxygen-evolving complex of photosystem-II and depletion of extrinsic polypeptides by nickel. Biometals 20:879–889

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Boyd RS, Wall MA, Jaffre T (2006) Nickel levels in arthropods associated with Ni hyperaccumulator plants from an ultramafic site in New Caledonia. Insect Sci 13(4):271–277

    CAS  Google Scholar 

  • Briat JF, Lebrun M (1999) Plant responses to metal toxicity. C R Acad Sci 322:43–54

    CAS  Google Scholar 

  • Brooks RR, Shaw S, Marfil AA (1981) The chemical form and physiological function of nickel in some Iberian Alyssum species. Physiol Plant 51:167–170

    CAS  Google Scholar 

  • Brown PH (2006) “Nickel.” In Handbook of Plant Nutrition, edited by A. V. Barker and D. J. Pilbeam, pp 395–410

  • Brown PH, Welch RM, Cary EE (1987) Nickel: a micronutrient essential for higher plants. Plant Physiol 85:801–803

    CAS  Google Scholar 

  • Brune A, Deitz KJ (1995) A comparative analysis of element composition of roots and leaves of barley seedlings grown in the presence of toxic cadmium, molybdenum, nickel and zinc concentrations. J Plant Nutr 18:853–868

    CAS  Google Scholar 

  • Cataldo DA, Garland TR, Wildung RW (1978) Nickel in plants: I. Uptake kinetics using intact soybean seedlings. Plant Physiol 62:563–565

    CAS  Google Scholar 

  • Cempel M, Nikel G (2006) Nickel: a review of its sources and environmental toxicology. Pol J Environ Stud 15(3):375–382

    CAS  Google Scholar 

  • Chaney RL, Angle JS, McIntosh MS, Reeves RD, Li YM, Brewer EP, Chen KY, Roseberg RJ, Perner H, Synkowski EC, Broadhurst CL, Wang S, Baker AJ (2005) Using hyperaccumulator plants to phytoextract soil Ni and Cd. Z Naturforsch 60:190–198

    CAS  Google Scholar 

  • Chawan DD (1995) Environment and adaptive biology of plants. Scientific Publishers, Jodhpur

    Google Scholar 

  • Chen ZS, Tsai CC, Tsui CC (1999) Proposed regulation of soil pollutants in Taiwan soils. Proceedings of 6th workshop on Soil pollution and prevention: soil remediation techniques on soils contaminated by organic pollutants. Taipei, Taiwan, pp 169–207

  • Chen Y, Li X, Shen Z (2004) Leaching and uptake of heavy metals by ten different species of plants during an EDT Aassisted phytoextraction process. Chemosphere 57(3):187–196

    CAS  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    CAS  Google Scholar 

  • Colpas GJ, Hausinger RP (2000) In vivo and in vitro kinetics of metal transfer by the Klebsiella aerogenes urease nickel metallochaperone, urea. J Biol Chem 275:10731–10737

    CAS  Google Scholar 

  • Dalton DA, Evans HJ, Hanus FJ (1985) Stimulation by nickel of soil microbial urease activity and urease and hydrogenase activities in soybeans grown in a low-nickel soil. Plant Soil 88:245–258

    CAS  Google Scholar 

  • DEPA (2005) Draft risk assessment. Nickel (CAS No: 7440-02-0), EINECS No: 231–111- 4. Copenhagen: Danish Environmental Protection Agency

  • Dietz KJM, Baier M, Kramer U (1999) In: Prasad MNV, Hagemeyer J (eds) In heavy metal stress in plants: from molecules to ecosystems, vol 1999. Springer- Verlag, Berlin, pp 73–97

    Google Scholar 

  • Dixon NE, Hinds JA, Fihelly AK, Gozala C, Winzor DJ, Blakeley RL, Zerner B (1980) Jack bean urease (EC 3.5.1.5). IV. The molecular size and mechanism of inhibition by hydroxamic acids. Spectrophotometric fixation of enzymes with reversible inhibitors. Can J Biochem 58:1323–1334

    CAS  Google Scholar 

  • Doganlar ZB, Cakmak S, Yanik T (2012) Metal uptake and physiological changes in Lemna gibba exposed to manganese and nickel. Int J Biol 4:148–157

    CAS  Google Scholar 

  • Duarte B, Delgado M, Caador I (2007) The role of citric acid in cadmium and nickel uptake and translocation, in Halimione portulacoides. Chemosphere 69:836–840

    CAS  Google Scholar 

  • Dubey D, Pandey A (2011) Effect of nickel (ni) on chlopophyll, lipid peroxidation andantioxidant enzymes activities in black gram (Vigna mungo) leaves. Int J Sci Nat 2(2):395–401

    CAS  Google Scholar 

  • Duda-Chodak A, Baszczyk U (2008) The impact of nickel on human health. J Elementol 13(4):685–696

    Google Scholar 

  • Duman F, Ozturk F (2010) Nickel accumulation and its effect on biomass, protein content and antioxidative enzymes in roots and leaves of watercress. J Environ Sci 22(4):526–532

    CAS  Google Scholar 

  • Elson, M (2006) Nickel: staying healthy with nutrition the complete guide to diet and nutritional medicine, September

  • Eskew DL, Welch RM, Cary EE (1983) Nickel: an essential micronutrient for legumes and possibly all higher plants. Science 222:691–693

    Google Scholar 

  • European Food Safety Authority (EFSA) (2015) Scientific opinion on the risks to public health related to the presence of nickel in food and drinking water. In; EFSA Panel on Contaminants in the Food Chain (CONTAM). EFSA J 13(2):4002

  • Ewais EA (1997) Effects of cadmium, nickel and lead on growth, chlorophyll content and proteins of weeds. Biol Plant 39:403–410

    CAS  Google Scholar 

  • Feleafel MN, Mirdad ZM (2013) Hazard and effects of pollution by lead on vegetable crops. J Agric Environ Ethics 26:547–567

    Google Scholar 

  • Feng X, Melander AP, Klaue B (2000) Contribution of municipal waste incineration to trace metal deposition on the vicinity. Water Air Soil Pollut 119:295–316

    CAS  Google Scholar 

  • Fismes J, Echevarria G, Leclerc-Cessac E, Morel JL (2005) Uptake and transport of radioactive nickel and cadmium into three vegetables after wet aerial contamination. J Environ Qual 34:1497–1507

    CAS  Google Scholar 

  • Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191

    CAS  Google Scholar 

  • Gabbrielli A, Pandolfini T, Vergnano O, Palandri MR (1990) Comparison of two serpentine species with different nickel tolerance strategies. Plant Soil 122:271–277

    CAS  Google Scholar 

  • Gajewska E, Sklodowska M (2005) Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 27:329–339

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Gajewska E, Sklodowska M (2008) Differential biochemical responses of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Regul 54:179–188

    CAS  Google Scholar 

  • Gajewska E, Skłodowska M (2009) Nickel-induced changes in nitrogen metabolism in wheat shoots. J Plant Physiol 166:1034–1044

    CAS  Google Scholar 

  • Gajewska E, Skłodowska M, Słaba M, Mazur J (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50(4):653–659

    CAS  Google Scholar 

  • Gerendas J, Sattelmacher B (1999) Influence of Ni supply on growth and nitrogen metabolism of Brassica napus L. grown with NH4NO3 or urea as N source. Ann Bot 83:65–71

    CAS  Google Scholar 

  • Gray CW, Mclaren RG (2006) Soil factors affecting heavy metal solubility in some New Zealand soils. Water Air Soil Pollut 175:3–14

    CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    CAS  Google Scholar 

  • Hao F, Wang X, Chen J (2006) Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci 170:151–158

    CAS  Google Scholar 

  • Harada E, Kim JA, Meyer AJ, Hell R, Clemens S, Choi YE (2010) Expression profiling of tobacco leaf trichomes identifies genes for biotic and abiotic stresses. Plant Cell Physiol 51:1627–1637

    CAS  Google Scholar 

  • Hasinur R, Shamima S, Shigenao KW (2005) Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution. J Plant Nutr 28:393–404

    Google Scholar 

  • Hassanpour ES, Rezayatmand Z (2015) Evaluation of some physiological and biochemical parameters of variety of sunflower sanbero (Helianthus annuus L.) under nickel toxicity. Ind J Fundam Appl Life Sci 5(4):88–99

    Google Scholar 

  • Hauser MT (2014) Molecular basis of natural variation and environmental control of trichome patterning. Front Plant Sci 5:1–7

    Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Ahmad A (2013) Proline enhances antioxidative enzyme activity, photosynthesis and yield of Cicer arietinum L. exposed to cadmium stress. Acta Bot Croat 2:323–335

    Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    CAS  Google Scholar 

  • Heath SM, Southworth D, Allura A (1997) Localization of nickel in epidermal subsidiary cells of leaves of Thlaspi montanum var. Siskiyouense (Brassicaceae) using energy-dispersive X-ray microanalysis. Int J Plant Sci 158:184–188

    CAS  Google Scholar 

  • Hedfi A, Mahmoudi E, Boufahja F, Beyrem H, Aissa P (2007) Effects of increasing levels of nickel contamination on structure of offshore nematode communities in experimental microcosms. Bull Environ Contam Toxicol 79:345–349

    CAS  Google Scholar 

  • Hermle S, Vollenweider P, Gunthardt-Goerg MS, Mcquattie CJ, Matyssek M (2007) Leaf responsiveness of Populus tremula and Salix viminalis to soil contaminated with heavy metals and acidic rainwater. Tree Physiol 27:1517–1531

    CAS  Google Scholar 

  • Hirai M, Kawai-Hirai R, Hirai T, Ueki T (1993) Structural change of Jack Bean urease induced by addition of surfactants studied with synchrotron-radiation small-angle X-ray scattering. Eur J Biochem 215:55–61

    CAS  Google Scholar 

  • IARC (International Agency for Research on Cancer) (1990) IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Chromium, nickel, and welding. World Health Organization. Lyon. 49:257–445

    Google Scholar 

  • IPCS (1991) Nickel. Geneva, World Health Organization, International Programme on Chemical Safety (Environmental Health Criteria 108)

  • Jagetiya B, Akash S, Saroj Y (2013) Effect of nickel on plant water relations and growth in green gram. Indian J Plant Physiol 18:372–376

    Google Scholar 

  • Kabata-Pendias A, Mukherjee AB (2007) Trace elements in soils and plants. Springer, Berlin

    Google Scholar 

  • Kalac P (2010) Trace element contents in European species of wild growing edible mushrooms: a review for the period 2000–2009. Food Chem 122:2–15

    CAS  Google Scholar 

  • Karaca A (2004) Effect of organic wastes on the extractability of cadmium, copper, nickel, and zinc in soil. Geoderma 122(4):297–303

    CAS  Google Scholar 

  • Kastori R, Petrovi M, Petrovi N (1992) Effect of excess lead, cadmium, copper, and zinc on water relations in sunflower. J Plant Nutr 15:2427–2439

    CAS  Google Scholar 

  • Keeling SM, Stewart RB, Anderson CWN, Robinson BH (2003) Nickel and cobalt phytoextraction by the hyperaccumulator Berkheya coddii implications for polymetallic phytomining and phytoremediation. Int J Phytoremed 5:235–244

    CAS  Google Scholar 

  • Kevresan S, Petrovic N, Popovic M, Kandrac J (1998) Effect of heavy metals on nitrate and protein metabolism in sugar beet. Biol Plant 41:235–240

    CAS  Google Scholar 

  • Kovacevic G, Kastori R, Merkulov RJ (1999) Dry matter and leaf structure in young wheat plants as affected by Cd, lead, and nickel. Biol Plant 42:119–123

    CAS  Google Scholar 

  • Kozlow MV (2005) Pollution resistance of mountain birch, Betula pubescens subsp. czerepanovii, near the copper-nickel smelter: natural selection or phenotypic acclimation. Chemosphere 59:189–197

    Google Scholar 

  • Krupa Z, Baszynski T (1995) Some aspects of heavy metals toxicity towards photosynthetic apparatus direct and indirect effects on light and dark reactions. Acta Physiol Plant 17:177–190

    CAS  Google Scholar 

  • Krupa Z, Siedleka A, Maksymiec W, Baszynski T (1993) In vivo response of photosynthetic apparatus of Phaseolus vulgaris L. to nickel toxicity. J Plant Physiol 142:664–668

    CAS  Google Scholar 

  • Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. J Environ Qual 33:2090–2102

    CAS  Google Scholar 

  • Kupper H, Kroneck PMH (2007) Nickel in the environment and its role in the metabolism of plants and cyanobacteria. In: Sigel A, Sigel H, Sigel RKO (eds) Metal Ions in Life Sciences. Wiley, Chichester, pp 31–62

    Google Scholar 

  • Kupper H, Kupper F, Spiller M (1996) Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. J Exp Bot 47:259–266

    Google Scholar 

  • Kupper H, Lombi E, Zhao FG, Wieshammer G, McGrath SP (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300

    CAS  Google Scholar 

  • Lee S, Moon JS, Domier LL, Korban SS (2002) Molecular characterization of phytochelatin synthase expression in transgenic arabidopsis. Plant Physiol Biochem 40:727–733

    CAS  Google Scholar 

  • Lin YC, Kao CH (2005) Nickel toxicity of rice seedlings: cell wall peroxidase, lignin, and NiSO4-inhibited root growth. Crop Environ Bioinform 2:131–136

    CAS  Google Scholar 

  • Lin YC, Kao CH (2007) Proline accumulation induced by excess nickel in detached rice leaves. Biol Plant 51:351–354

    CAS  Google Scholar 

  • Lipismita S, Mishra C (2011) Significance of nickel in livestock health and production. IJAVMS 5(3):349–361

    Google Scholar 

  • Liu WX (2008) Accumulation and translocation of toxic heavy metals in winter wheat (Triticum aestivum L.) growing in agricultural soil of Zhengzhou, China. Bull Environ Contam Toxicol 82:343–347

    Google Scholar 

  • Llamas A, Ullrich CI, Sanz A (2008) Ni2+ toxicity in rice: effect on membrane functionality and plant water content. Plant Physiol Biochem 46:905–910

    CAS  Google Scholar 

  • Lu Y, Li X, He M, Wang Z, Tan H (2010) Nickel effects on growth and anti-oxidative enzymes activities in desert plant Zygophyllum xanthoxylon (Bunge). Sci Cold Arid Reg 2:436–444

    Google Scholar 

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

    CAS  Google Scholar 

  • Maksimović I, Kastori R, Krstic L, Lukovic J (2007) Steady presence of cadmium and nickel affects root anatomy, accumulation and distribution of essential ions in maize seedlings. Biol Plant 51:589–592

    Google Scholar 

  • Malkin R, Niyogi K (2000) Photosynthesis. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, MD, pp 568–628

    Google Scholar 

  • Maraghy SA, Gad MZ, Fahim AT, Hamdy MA (2001) Effect of cadmium and aluminum intake on the antioxidant status and lipid peroxidation in rat tissues. J Biochem Mol Toxicol 15:207–214

    Google Scholar 

  • Marschner H (2002) Mineral nutrition of higher plants, 3rd edn. Academic Press, London, pp 364–369

    Google Scholar 

  • Matraszek R, Szymanska M, Wroblewska M (2002) Effect of nickel on yielding and mineral composition of the selected vegetables. Acta Sci Pol Tech Agr 1:3–22

    Google Scholar 

  • McGrath SP (1995) Chromium and Nickel. In: In heavy metals in soils (Ed: B. J. Alloway), 2nd edn. Blackie Academic and Professional, London, pp 152–174

    Google Scholar 

  • McIlveen WD, Negusantil JJ (1994) Nickel in the terrestrial environment. Sci Total Environ 148:109–138

    CAS  Google Scholar 

  • Meagher RB, Rugh CL, Kandasamy MK, Gragson G, Wang NJ (2000) Engineered phytoremediation of mercury pollution in soil and water using bacterial genes. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. Lewis Publishers, Boca Raton, FL, pp 201–219

    Google Scholar 

  • Menon MSH, Abbaspour KC, Gunthardt-Goerg MS, Oswald SE, Schulin R (2005) Water regime of metal-contaminated soil under juvenile forest vegetation. Plant Soil 271:227–241

    CAS  Google Scholar 

  • Molas J (1997) Changes in morphological and anatomical structure of cabbage (Brassica oleracea L.) outer leaves and in ultrastructure of their chloroplasts caused by an in vitro excess of nickel. Photosynthetica 34:513–522

    CAS  Google Scholar 

  • Molas J (2002) Changes of chloroplast ultrastructure and total chlorophyll concentration in cabbage leaves caused by excess of organic Ni II complexes. Environ Exp Bot 47:115–126

    CAS  Google Scholar 

  • Mulrooney SB, Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27:239–261

    CAS  Google Scholar 

  • Munne-Bosch S, Penuelas J (2003) Photo and antioxidative protection, and a role for salicylic acid during drought and recovery in fieldgrown Phillyrea angustifolia plants. Planta 217:758–766

    CAS  Google Scholar 

  • Nakazawa R, Kameda Y, Ito T, Ogita Y, Michihata R, Takenaga H (2004) Selection and characterization of nickel-tolerant tobacco cells. Biol Plant 48:497–502

    CAS  Google Scholar 

  • Namgay T, Singh B, Singh BP (2010) Influence of biochar application to soil on the availability of As, Cd, Cu, Pb, and Zn to maize (Zea mays L.). Soil Res 48(6–7):638–647

    CAS  Google Scholar 

  • Nedhi A, Singh LJ, Singh SI (1990) Effect of cadmium and nickel on germination, early seedling growth and photosynthesis of wheat and pigeon pea. Int J Trop Agric 8:141–147

    Google Scholar 

  • Neumann PM, Chamel A (1986) Comparative phloem mobility of nickel in nonsenescent plants. Plant Physiol 81:689–691

    CAS  Google Scholar 

  • Nielson FH, Ollerich DA (1973) Nickel: a new essential trace element. Presented at 57th annual federation of American Societies for experimental biology, meeting, Atlantic city

  • Nieminen TM, Ukonmaanaho L, Rausch N, Shotyk W (2007) Biogeochemistry of nickel and its release into the environment. Met Ions Life Sci 2:1–30

    CAS  Google Scholar 

  • Novak JM, Busscher WJ, Laird DL, Ahmedna M, Watts DW, Niandou MAS (2009) Impact of biochar amendment on fertility of a southeastern coastal plain soil. Soil Sci 174(2):105–112

    CAS  Google Scholar 

  • Page V, Feller U (2005) Selective transport of zinc, manganese, nickel, cobalt and cadmium in the root system and transfer to the leaves in young wheat plants. Ann Bot 96:425–434

    CAS  Google Scholar 

  • Page V, Weisskof L, Feller U (2006) Heavy metals in white Lupin: uptake, root-to-shoot transfer and redistribution within the plant. New Phytol 171:329–341

    CAS  Google Scholar 

  • Pandey N, Pathak GC (2006) Nickel alters antioxidative defense and water status in green gram. Indian J Plant Physiol 11:113–118

    CAS  Google Scholar 

  • Pandey N, Sharma CP (2002) Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci 163:753–758

    CAS  Google Scholar 

  • Pandolfini T, Gabbrielli R, Comparini C (1992) Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant Cell Environ 15(6):719–725

    CAS  Google Scholar 

  • Papadopoulos A, Prochaska C, Papadopoulos F, Gantidis N, Metaxa E (2007) Determination and evaluation of cadmium, copper, nickel, and zinc in agricultural soils of western Macedonia, Greece. Environ Manag 40:719–726

    CAS  Google Scholar 

  • Papazogloua EG, Serelisb KG, Bouranisc DL (2007) Impact of high cadmium and nickel soil concentration on selected physiological parameters of Arundo donax L. Eur J Soil Biol 911:64–74

    Google Scholar 

  • Parlak KU (2016) Effect of nickel on growth and biochemical characteristicsof wheat (Triticum aestivum L.) seedlings. Wageningen J Life Sci 76:1–5

    Google Scholar 

  • Parmar P, Mandakini J, Bhaumik D, Subramanian RB (2012) Nickel accumulation by Colocassia esculentum and its impact on plant growth and physiology. Afr J Agric Res 7:3579–3587

    Google Scholar 

  • Pendias A, Mukherjee AB (2007) Trace elements from soil to human. Springer- Verlag, Berlin

    Google Scholar 

  • Peralta-Videaa JR, Gardea-Torresdey JL, Gomezc EL, Tiemanna KJ, Parsonsa JG, Carrillod G (2002) Effect of mixed cadmium, copper, nickel and zinc at different pHs upon alfalfa growth and heavy metal uptake. Environ Pollut 119:291–301

    Google Scholar 

  • Prasad MNV (1997) Trace elements. In: Prasad MNV (ed) Plant ecophysiology. Wiley, New York, pp 207–249

    Google Scholar 

  • Prasad MNV (2005) Nickelophilous plants and their significance in phytotechnologies. Braz J Plant Physiol 17:113–128

    CAS  Google Scholar 

  • Psaras GK, Manetas Y (2001) Nickel localization in seeds of metal hyper accumulator Thlaspi pindicum. Ann Bot 88:513–516

    CAS  Google Scholar 

  • Ragsdale SW (1998) Nickel biochemistry. Curr Opin Chem Biol 2:208–215

    CAS  Google Scholar 

  • Rajni S, Rajeev G (2009) Excess nickel alters growth, metabolism, and translocation of certain nutrients in potato. J Plant Nutr 32:10051014

    Google Scholar 

  • Rao KVM, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajnus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Google Scholar 

  • Rathor G, Neelam C, Tapan A (2014) Effect of variation in nickel concentration on growth of maize plant: a comparative over view for pot and hoagland culture. Res J Chem Sci 4(10):30–32

    CAS  Google Scholar 

  • Rauser WE, Dumbroff EB (1981) Effects of excess cobalt, nickel and zinc on the water relations of Phaseolus vulgaris. Environ Exp Bot 21:249–255

    CAS  Google Scholar 

  • Rautaray SK, Ghosh BC, Mittra BN (2003) 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 90(3):275–283

    CAS  Google Scholar 

  • Reddy SR (2004) Principles of crop production: growth regulators and growth analysis, 2nd edn. Kalyani Publishers, Ludhiana

    Google Scholar 

  • Riesen O, Feller U (2005) Redistribution of nickel, cobalt, manganese, zinc and cadmium via the phloem in young and in maturing wheat. J Plant Nutr 28:421–430

    CAS  Google Scholar 

  • Rooney CP, Zhao FJ, McGrath SP (2007) Phytotoxicity of nickel in a range of Europian soils: influence of soil properties, Ni solubility and speciation. Environ Pollut 145:596–605

    CAS  Google Scholar 

  • Ros R, Cooke DT, Martinez-Cortina C, Picazo I (1992) Nickel and cadmium related changes in growth, plasma membrane lipid composition, ATPase hydrolytic activity and proton-pumping of rice (Oryza sativa L.) shoots. J Exp Bot 43:1475–1481

    CAS  Google Scholar 

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

    Google Scholar 

  • Sabir M, Ghafoor A, Saifullah RMZU, Ahmand HR, Aziz T (2011) Growth and metal ionic composition of Zea mays as affected by nickel supplementation in the nutrient solution. Int J Agric Biol 13:186–190

    CAS  Google Scholar 

  • Sajwan KS, Ornes WH, Youngblood TV, Alva AK (1996) Uptake of soil applied cadmium, nickel and selenium by bush beans. Water Air Soil Pollut 91:209–217

    CAS  Google Scholar 

  • Sakamoto T, Bryant DA (2001) Requirement of nickel as an essential micronutrient for the utilization of urea in the marine cyanobacterium Synechococcus sp. PCC 7002. Microbes Environ 16:177–184

    Google Scholar 

  • Salt DE, Kramer U (2000) Mechanisms of metal hyperaccumulation in plants. In: Ensley BD, Raskin I (eds) Phytoremediation of toxic metals: using plants to clean-up the environment. Wiley, New York, pp 231–246

    Google Scholar 

  • Samantaray S, Rout GR, Das P (1997) Tolerance of rice to nickel in nutrient solution. Biol Plant 40:295–298

    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

    CAS  Google Scholar 

  • Scott FJJ (1997) Toxicity of nickel to soil organisms in Denmark. Rev Environ Contam Toxicol 148:1

    Google Scholar 

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

    CAS  Google Scholar 

  • Seregin IV, Kozhevnikova AD, Kazyumina EM, Ivanov VB (2003) Nickel toxicity and distribution in maize roots. Russ J Plant Physiol 50:711–717

    CAS  Google Scholar 

  • Shalygo NV, Kolensikova NY, Voronetskaya VV, Averina NG (1999) Effects of Mn Fe, Co and Ni on chlorophyll accumulation and early stages of chlorophyll formation of greening barley seedling. Russ J Plant Physiol 46:496–501

    CAS  Google Scholar 

  • Sharma P, Bhardwaj R, Arora N, Arora HK, Kumar A (2008) Effects of 28-homobrassinolide on nickel uptake, protein content and antioxidative defense system in Brassica juncea. Biol Plant 52:767–770

    Article  CAS  Google Scholar 

  • Sheng X, Xia J (2006) Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere 64(6):1036–1042

    CAS  Google Scholar 

  • Sheoran IS, Singal HR, Singh R (1990a) Effect of cadmium and nickel on photosynthesis and the enzymes of the photosynthetic carbon reduction cycle in pigeonpea (Cajanus cajan L.). Photosynth Res 23:345–351

    CAS  Google Scholar 

  • Sheoran IS, Aggarwal N, Singh R (1990b) Effect of cadmium and nickel on in vivo carbon dioxide exchange rate of pigeon pea (Cajanus cajan L.). Plant Soil 129:243–249

    CAS  Google Scholar 

  • Shi GR, Cai QS (2008) Photosynthetic and anatomic responses of peanut leaves to cadmium stress. Photosynthetica 46(4):627–630

    CAS  Google Scholar 

  • Shukla R, Gopal R (2009) Excess nickel alters growth, metabolism, and translocation of certain nutrients in potato. J Plant Nutr 32:1005–1014

    CAS  Google Scholar 

  • Shukla D, Tiwari M, Tripathi RD, Nath P, Trivedi PK (2013) Synthetic phytochelatins complement a phytochelatin deficient Arabidopsis mutant and enhance the accumulation of heavy metal(loid)s. Biochem Biophys Res Commun 434:664–669

    CAS  Google Scholar 

  • Singh P, Nayyar K (2001) Influence of lime on nickel availability to plants and its toxic level in cowpea. J Res Punjab Agri Univ 38:10–13

    CAS  Google Scholar 

  • Singh K, Panday SA (2010) Effect of nickel-stresses on uptake, pigments and antioxidative responses of water lettuce (Pistia stratiotes L). J Environ Biol 32:391–394

    Google Scholar 

  • Smith RM, Martell AE (1989) Stability Constants, Vol. 6: Second Supplement, Plenum Press, New York.

  • Sobkowiak RR (2016) Water relations in plants subjected to heavy metal stresses. Acta Physiol Plant 38:1–13

    Google Scholar 

  • Solomons NW, Viteri F, Shuler TR, Niels FH (1982) Bioavailabilty of nickel in man: effects of foods and chemically-defined dietary constituents on the absorption of inorganic nickel. J Nutr 112(1):39–44

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Tatrai E, Zuzana K, Hudak A, Adamis Z, Ungvary G (2001) Comparative in vitro toxicity of cadmium and lead on redox cycling in type II pneumocytes. J Appl Toxicol 21:479–483

    CAS  Google Scholar 

  • Taylor GJ, Stadt KJ (1990) Interactive effects of cadmium, copper, manganese, nickel and zinc on root growth of wheat (Triticum aestivum) in solution culture. Plant Soil Sci 4:317–322

    Google Scholar 

  • Tripathy BC, Bhatia B, Mohanty P (1981) Inactivation of chloroplast photosynthetic electron transport activity by Ni2+. Biochim Biophys Acta 638:217–224

    CAS  Google Scholar 

  • U.S. Public Health Service USPHS (1977) Criteria for a recommended standard occupational exposure to inorganic nickel. U. S. Department of Health, Education and Welfare, Public Health Service, Center for Disease Control, National Institute for Occupational Safety and Health. DHEW (NIOSH) Publication No. 77–164, p 282

  • Veeranjaneyulu K, Das VSR (1982) Intrachloroplast localization of 65Zn and 63Ni in a Zn-tolerant plant Ocimum basilicum Benth. J Exp Bot 33:1161–1165

    Google Scholar 

  • Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655

    CAS  Google Scholar 

  • Vernay P, Gauthier-Moussard C, Hitmi A (2007) Interaction of bioaccumulation of heavy metal chromium with water relation, mineral nutrition and photosynthesis in developed leaves of Lolium perenne L. Chemosphere 68:1563–1575

    CAS  Google Scholar 

  • Vogel-Mikus K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonization of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242

    CAS  Google Scholar 

  • Walker CD, Graham RD, Madison JT, Cary EE, Welch RM (1985) Effects of Ni deficiency on some nitrogen metabolites in cowpeas (Vigna unguiculata L. Walp). Plant Physiol 79:474–479

    CAS  Google Scholar 

  • Wang Z, Zhang Y, Huang Z, Huang L (2008) Antioxidative response of metal-accumulator and non-accumulator plants under cadmium stress. Plant Soil 310:137–149

    CAS  Google Scholar 

  • Wang ST, He XJ, An AD (2010) Responses of growth and antioxidant metabolism to nickel toxicity in Luffa cylindrica seedlings. J Animal Plant Sci 7:810–821

    Google Scholar 

  • Wang Y, Wang S, Nan J, Ma F, Zang Y, Chen Y, Li L, Zhang Q (2015) Effects of Ni stress on the uptake and translocation of Ni and other mineral nutrition elements in mature wheat grown in sierozems from northwest of China. Environ Sci Pollut Res 22:19756–19763

    CAS  Google Scholar 

  • Welch RM (1981) The biological significance of nickel. J Plant Nutr 3:345–356

    CAS  Google Scholar 

  • Weyens N, Vander DL, Taghavi S, Newman L, Vangronsveld N (2009) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27(10):591–598

    CAS  Google Scholar 

  • Wheeler CT, Hughes LT, Oldroyd J, Pulford ID (2001) Effects of nickel on Frankia and its symbiosis with Alnus glutinosa (L.). Gaertn Plant Soil 231:81–90

    CAS  Google Scholar 

  • Wood BW, Reilly CC (2007) Interaction of nickel and plant disease. In: Datnoff LE, Elmer WH, Huber DM (eds) Mineral nutrition and plant disease. American Phytopathological Society Press, Minneapolis, MN, pp 217–247

    Google Scholar 

  • Wood BW, Reilly CC, Nyczepir AP (2006) Field deficiency of nickel in trees: symptoms and causes. Acta Hortic 721:83–98

    CAS  Google Scholar 

  • Yang X, Baligar VC, Martens DC, Clark RB (1996) Plant tolerance to Ni toxicity. I. Influx, transport and accumulation of Ni in four species. J Plant Nutr 19:73–85

    CAS  Google Scholar 

  • Yang XE, Baligar VC, Foster JC, Martens DC (1997) Accumulation and transport of nickel in relation to organic acids in ryegrass and maize with different nickel levels. Plant Soil 196:271–276

    CAS  Google Scholar 

  • Yusuf M, Fariduddin Q, Hayat S, Hasan SA, Ahmad A (2010) Protective responses of 28 homobrssinolide in cultivars of Triticum aestivum with different levels of nickel. Arch Environ Contam Toxicol 60(1):68–76

    Google Scholar 

  • Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64(6):991–997

    CAS  Google Scholar 

  • Zarcinas BA, Ishak CF, McLaughlin MJ, Cozens G (2004) Heavy metals in soils and crops in Southeast Asia. 1. Peninsular Malaysia. Environ Geochem Health 26:343–357

    CAS  Google Scholar 

  • Zhang L, Angle JS, Chaney RL (2007) Do high-nickel leaves shed by the nickel hyperaccumulator Alyssum murale inhibit seed germination of competing plants. New Phytol 173:509–516

    CAS  Google Scholar 

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Acknowledgements

We are thankful to Dr. Lorenzo Barbanti, Department of Agricultural and Food Sciences, University of Bologna, Italy for his valuable suggestions to improve the quality of the manuscript.

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  1. Department of Agronomy, University of Agriculture, Faisalabad, Pakistan

    Muhammad Umair Hassan, Muhammad Umer Chattha, Imran Khan, Muhammad Aman Ullah Khan & Tahir Abbas Khan

  2. Department of Agricultural and Food Sceinces, University of Bologna, Bologna, Italy

    Muhammad Umair Hassan & Abid Ali

  3. Institute of Agricultural Sciences, University of the Punjab, Lahore, Pakistan

    Muhammad Bilal Chattha

  4. Research Center on Ecological Sciences, Jiangxi Agricultural University, Nanchang, China

    Muhammad Aamer

  5. College of Agriculture, Bahadur Campus Layyah, Bahauddin Zakariya University, Multan, Pakistan

    Muhammad Nawaz

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Hassan, M.U., Chattha, M.U., Khan, I. et al. Nickel toxicity in plants: reasons, toxic effects, tolerance mechanisms, and remediation possibilities—a review. Environ Sci Pollut Res 26, 12673–12688 (2019). https://doi.org/10.1007/s11356-019-04892-x

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