Environmental Science and Pollution Research

, Volume 24, Issue 30, pp 23915–23925 | Cite as

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

  • Vibha Gupta
  • Pradeep Kumar Jatav
  • Raini Verma
  • Shanker Lal Kothari
  • Sumita Kachhwaha
Research Article


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.


Nickel accumulation Oxidative stress Millets Oats Seedling growth Phytoremediation 



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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 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 22:8148–8162CrossRefGoogle Scholar
  2. 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 22:11679–11689CrossRefGoogle Scholar
  3. Ahmad MSA, Ashraf M (2012) Essential roles and hazardous effects of nickel in plants. Rev Environ Contam Toxicol 214:pp125–pp167Google Scholar
  4. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress. J Exp Bot 53:1331–1341CrossRefGoogle Scholar
  5. Amadou I, Gounga ME, Le G-W (2013) Millets: nutritional composition, some health benefits and processing—a review. Emirates J Food Agric 25:501CrossRefGoogle Scholar
  6. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1CrossRefGoogle Scholar
  7. 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 62:533–546CrossRefGoogle Scholar
  8. Asada K (1992) Ascorbate peroxidase—a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241CrossRefGoogle Scholar
  9. 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, 00-00Google Scholar
  10. Assche FV, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206CrossRefGoogle Scholar
  11. Baccouch S, Chaoui A, El Ferjani E (2001) Nickel toxicity induces oxidative damage in Zea mays roots. J Plant Nutr 24:1085–1097CrossRefGoogle Scholar
  12. Bai C, Liu L, Wood BW (2013) Nickel affects xylem Sap RNase A and converts RNase A to a urease. BMC Plant Biol 13:1CrossRefGoogle Scholar
  13. Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  14. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287CrossRefGoogle Scholar
  15. 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 1864:52–61CrossRefGoogle Scholar
  16. 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 72:1213–1221CrossRefGoogle Scholar
  17. 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 64:915932Google Scholar
  18. Bhaduri AM, Fulekar M (2012) Antioxidant enzyme responses of plants to heavy metal stress. Rev Environ Sci Biotechnol 11:55–69CrossRefGoogle Scholar
  19. Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. New Phytol 156:205–215CrossRefGoogle Scholar
  20. Clarkson DT, Luttge U (1989) Mineral nutrition: divalent cations, transport and compartmentation. Prog Bot 51:93–112Google Scholar
  21. 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 25:643–651CrossRefGoogle Scholar
  22. Edreva AM, Georgieva ID, Cjholakova NI (1989) Pathogenic and non-pathogenic stress effects on peroxidases in leaves of tobacco. Environ Exp Bot 29:365–377CrossRefGoogle Scholar
  23. 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, Google Scholar
  24. Elstner EF (1982) Oxygen activation and oxygen toxicity. Ann Rev Plant Physiol 33:73–96CrossRefGoogle Scholar
  25. FAO (Food and Agriculture Organization) (2014) Accessed 10 November 2016
  26. 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 93:1568–1574CrossRefGoogle Scholar
  27. Flora S, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res 128:501Google Scholar
  28. Gabbrielli R, Pandolfini T, Vergnano O (1987) Peroxidase involvement in tolerance mechanisms. G Bot Ital 21:200–201Google Scholar
  29. Gajewska E, Skłodowska M (2005) Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 27:329–340CrossRefGoogle Scholar
  30. Gajewska E, Skłodowska M, Słaba M (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50:653–659CrossRefGoogle Scholar
  31. Gajewska E, Skłodowska M (2007a) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20:27–36CrossRefGoogle Scholar
  32. Gajewska E, Skłodowska M (2007b) Relations between tocopherol, chlorophyll and lipid peroxides contents in shoots of Ni-treated wheat. J Plant Physiol 164:364–366CrossRefGoogle Scholar
  33. 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, 8Google Scholar
  34. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  35. 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 92:19–25CrossRefGoogle Scholar
  36. Gupta N, Srivastava A, Pandey V (2012) Biodiversity and nutraceutical quality of some indian millets. Proceed Natl Acad Sci India Section B: Biological Sci 82:265–273CrossRefGoogle Scholar
  37. Halliwell B, Gutteridge JMC (1999) Free radicles in biology and medicine, 4th edn. Oxford University Press, New YorkGoogle Scholar
  38. 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 5:1713–1717CrossRefGoogle Scholar
  39. Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266CrossRefGoogle Scholar
  40. 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 125:189–198CrossRefGoogle Scholar
  41. 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 175:474–481CrossRefGoogle Scholar
  42. 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 84:223Google Scholar
  43. Izosimova A (2005) Modelling the interaction between calcium and nickel in the soil-plant system. Bundesforschungsanstalt für Landwirtschaft (FAL), GermanGoogle Scholar
  44. Kaul S, Sharma S, Mehta I (2008) Free radical scavenging potential of L-proline: evidence from in vitro assays. Amino Acids 34:315–320CrossRefGoogle Scholar
  45. 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 4:1036–1046Google Scholar
  46. Khellaf N, Zerdaoui M (2010) Growth response of the duckweed Lemna gibba L. to copper and nickel phytoaccumulation. Ecotoxicology 19:1363–1368CrossRefGoogle Scholar
  47. Küpper H, Kroneck PM (2007) Nickel in the environment and its role in the metabolism of plants and cyanobacteria. Met Ions Life Sci 2:31–62Google Scholar
  48. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592CrossRefGoogle Scholar
  49. Lin CC, Kao CH (2000) Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul 30:151–155CrossRefGoogle Scholar
  50. 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 45:618–623CrossRefGoogle Scholar
  51. Maheshwari R, Dubey R (2009) Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 59:37–49CrossRefGoogle Scholar
  52. McLaughlin MJ, Zarcinas BA, Stevens DP, Cook N (2000a) Soil testing for heavy metals. Commun Soil Sci Plant Anal 31:1661–1700CrossRefGoogle Scholar
  53. 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 38:1037–1086CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  56. Nagajyoti P, Lee K, Sreekanth T (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216CrossRefGoogle Scholar
  57. 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 31:237–247CrossRefGoogle Scholar
  58. Pandey N, Sharma CP (2002) Effect of heavy metals Co 2+, Ni 2+ and Cd 2+ on growth and metabolism of cabbage. Plant Sci 163:753–758CrossRefGoogle Scholar
  59. 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 22:482–494CrossRefGoogle Scholar
  60. Poonkothai M, Vijayavathi BS (2012) Nickel as an essential element and a toxicant. Int J Environ Sci 1:285–288Google Scholar
  61. Racusen D, Foote M (1965) Protein synthesis in dark-grown bean leaves. Can J Bot 43:817–824CrossRefGoogle Scholar
  62. 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 28:393–404CrossRefGoogle Scholar
  63. 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 157:113–128CrossRefGoogle Scholar
  64. Raskin I, Kumar PBAN, Dushenkov S, Salt DE (1994) Bioconcentration of heavy metals by plants. Curr Opin Biotechnol 5:285–290CrossRefGoogle Scholar
  65. 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 60:97–104CrossRefGoogle Scholar
  66. Saleh AS, Zhang Q, Chen J, Shen Q (2013) Millet grains: nutritional quality, processing, and potential health benefits. Compr Rev Food Sci Food Saf 12:281–295CrossRefGoogle Scholar
  67. 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 101:477–482CrossRefGoogle Scholar
  68. Schickler H, Caspi H (1999) Response of antioxidative enzymes to nickel and cadmium stress in hyperaccumulator plants of the genus Alyssum. Physiol Plant 105:39–44CrossRefGoogle Scholar
  69. Seregin I, Kozhevnikova A (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277CrossRefGoogle Scholar
  70. 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 57:711–726CrossRefGoogle Scholar
  71. Shen Z, Li X, Wang C, Chen H, Chua H (2002) Lead phytoextraction from contaminated soil with high biomass plant species. J Environ Qual 31:1893–1900CrossRefGoogle Scholar
  72. 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 7:1780Google Scholar
  73. Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847CrossRefGoogle Scholar
  74. Sreekanth T, Nagajyothi P, Lee K, Prasad T (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Technol 10:1129–1140CrossRefGoogle Scholar
  75. Teranishi Y, Tanaka A, Osumi M, Fukui S (1974) Catalase activities of hydrocarbon-utilizing Candida yeasts. Agric Biol Chem 38:1213–1220CrossRefGoogle Scholar
  76. 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 253:571–580CrossRefGoogle Scholar
  77. 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 52:103–115CrossRefGoogle Scholar
  78. Vigouroux Y, Barnaud A, Scarcelli N, Thuillet A-C (2011) Biodiversity, evolution and adaptation of cultivated crops. Comptes rendus biologies 334:450–457CrossRefGoogle Scholar
  79. 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 54:294–300Google Scholar
  80. Yusuf M, Fariduddin Q, Hayat S, Ahmad A (2011) Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86:1–17CrossRefGoogle Scholar
  81. Zurayk R, Sukkariyah B, Baalbaki R, Ghanem DA (2002) Ni phytoaccumulation in Mentha aquatica L. and Mentha sylvestris L. Water Air Soil Pollut 139:355–364CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Vibha Gupta
    • 1
  • Pradeep Kumar Jatav
    • 1
  • Raini Verma
    • 1
  • Shanker Lal Kothari
    • 2
  • Sumita Kachhwaha
    • 1
  1. 1.Department of BotanyUniversity of RajasthanJaipurIndia
  2. 2.Amity Institute of BiotechnologyAmity University RajasthanJaipurIndia

Personalised recommendations