Skip to main content
Log in

Nickel Toxicity, Altering ROS Scavenging Mechanism and Impairing Sugar Based Signaling in Vigna radiata (L.) Wilczek during Germination and Seedling Establishment

  • Published:
Tropical Plant Biology Aims and scope Submit manuscript

Abstract

Nickel is a heavy metal that has a minor requirement in plants and exerts strong toxic effects at low concentrations. Seed germination and pre-greening stages of seedling establishment represent a brief heterotrophic phase in the life of an otherwise autotrophic organism. Germination is also a stage when the seed relies on stored reserves, including minerals rather than carrying out their uptake and has not been studied. The present work is a study of alteration of germination-related biochemical parameters in the presence of Nickel. Manifestations of Nickel induced oxidative stress as well as antioxidant defenses together with sugar sensing and respiratory enzymatic factors were investigated in seeds of Vigna radiata. Ni treatment increased electron flow through complex IV in cotyledons. It is proposed that inactivation of α-amylase adversely affects sugar movement to the growing seedling, leading to poor sugar sensing by hexokinase. These factors, including possible mis-metallation of electron transport complexes, combine to produce the observed symptoms of Nickel toxicity. The altered antioxidants activity can be correlated with Reactive Oxygen Species production and subsequent changes in seed metabolism.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Ahmad MS, Ashraf M (2011) Essential roles and hazardous effects of nickel in plants. Rev Environ Contam Toxicol 214:125–167

    PubMed  CAS  Google Scholar 

  • Baccouch S, Chaoui A, Ferjani EE (2001) Nickel toxicity induces oxidative damage in Zea Mays roots. J Plant Nutr 24(7):1085–1097

    Article  CAS  Google Scholar 

  • Bernfeld P (1955) Amylase α and β. In: Colwick SP, Kaplan NO (eds) Methods in enzymology, vol 1. Academic Press, New York, p 149

    Google Scholar 

  • Blokhina O, Fagerstedt KV (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory system. Physiol Plant 138(4):447–462

    Article  PubMed  CAS  Google Scholar 

  • Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyperaccumulator Alyssum bertolonii. New Phytol 156(2):205–215

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Annu Rev Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Bunik VI, Sievers C (2002) Inactivation of the 2-oxo acid dehydrogenase complexes upon generation of intrinsic radical species. Eur J Biochem 269:5004–5015

    Article  PubMed  CAS  Google Scholar 

  • Bush DS, Sticher L, Van Huystee R, Wagner D, Jones RL (1989) The calcium requirement for stability and enzymatic activity of two isoforms of barley aleurone -amylase. J Biol Chem 264:19392–19398

    PubMed  CAS  Google Scholar 

  • Chen C, Huang D, Liu J (2009) Functions and toxicity of nickel in plants: recent advances and future prospects. Clean 37:304–313

    CAS  Google Scholar 

  • Cheruth AJ, Ksouri R, Ragupathi G, Paramasivam M, Jallali I, Hameed JA, Zhao CX, Shao HB, Rajaram P (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436

    Article  CAS  Google Scholar 

  • Cooper TG, Beevers HJ (1969) Mitochondria and glyoxysomes from castor bean endosperm. Enzyme constituents and catalytic capacity. J Biol Chem 244:3507–3513

    PubMed  CAS  Google Scholar 

  • Davies MJ (2005) The oxidative environment and protein damage. Biochim Biophys Acta 1703:93–109

    Article  PubMed  CAS  Google Scholar 

  • Day DA, Hanson JB (1977) Effect of phosphate and uncouplers on substrate transport and oxidation by isolated corn mitochondria. Plant Physiol 59(2):139–144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Tullio MC, De Gara L, Paciolla C, Arrigoni O (1998) Dehydroascorbate reducing proteins in maize are induced by the ascorbate biosynthesis inhibitor lycorine. Plant Physiol Biochem 36:433–440

    Article  Google Scholar 

  • Dizdaroglu M (1993) Chemistry of free radical damage to DNA and nucleoproteins. In- Halliwell B, Aruoma OI (ed) DNA and Free Radicals, Ellis Horwood Ltd, London, UK

  • Dubey D, Anjana P (2011) Effect of nickel (Ni) on chlorophyll, lipid peroxidation and antioxidative enzyme activities in black gram (Vigna mungo) leaves. Int J Sci Nat 2:395–340

    CAS  Google Scholar 

  • Duchen MR (2000) Mitochondria and calcium: from cell signalling to cell death. J Physiol 529(1):57–68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Folin O, Denis W (1915) The excretion of free and conjugated phenols and phenol derivatives. J Biol Chem 22:309–320

    CAS  Google Scholar 

  • Foster AW, Osman D, Robinson NJ (2014) Metal preferences and Metallation. J Biol Chem 289(41):28095–28103

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  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 shoot. Biol Plant 50(4):653–659

    Article  CAS  Google Scholar 

  • Granot D, David-Schwartz R, Kelly G (2013) Hexose kinases and their role in sugar-sensing and plant development. Front Plant Sci 4:44

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gutteridge JM, Halliwell B (1990) The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem Sci 15:129–135

    Article  PubMed  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139

    PubMed  CAS  Google Scholar 

  • Han C, Yin X, He D, Yang P (2013) Analysis of proteome profile in germinating soybean seed and its comparison with Rice showing the styles of reserves mobilization in different crops. PLoS One 8:e56947

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395

    CAS  Google Scholar 

  • Imlay JA (2014) The mismetallation of enzymes during oxidative stress. J Biol Chem 289:28121–28128

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Keilland J (1937) Individual activity coefficients of ions in aqueous solutions. J Am Chem Soc 59:1675–1678

    Article  Google Scholar 

  • Kramer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halacsy. Plant Physiol 115:1641–1650

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Levine RL, Willians JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–363

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247(10):3170–3173

    PubMed  CAS  Google Scholar 

  • Molas J, Baran S (2004) Relationship between the chemical form of nickel applied to the soil and its uptake and toxicity to barley plants (Hordeum vulgare L). Geoderma 122:247–255

    Article  CAS  Google Scholar 

  • Munzuroglu O, Geckil H (2002) Effects of metals on seed germination, root elongation, coleoptile and hypocotyl growth in Triticum aestivum and Cucumis sativus. Arch Environ Contam Toxicol 43:203–213

    Article  PubMed  CAS  Google Scholar 

  • Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13

    Article  PubMed  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplast. Plant Cell Physiol 22(5):867–880

    CAS  Google Scholar 

  • Neuburger M (1985) Preparation of plant mitochondria, criteria for Assessement of mitochondrial integrity and purity, survival in vitro. In: Douce R, Day DA (ed) Higher plant cell respiration, Enc. Plant Physiol, Vol. 18. Springer-Verlag, Berlin, pp7–24

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol 49:249–279

    Article  CAS  Google Scholar 

  • Omaye ST, Turnbull JD, Sauberlich HE (1979) Selected methods for the determination of ascorbic acid in animal cells, tissues and fluids. Methods Enzymol 62:3–11

    Article  PubMed  CAS  Google Scholar 

  • Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA and Brand MD (2012) Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J Biol Chem 287:27255–27264

  • Rolland F, Baena-Gonzalez B, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  PubMed  CAS  Google Scholar 

  • Romanowska E, Igamberdiev AU, Parys E, Gardeström P (2002) Stimulation of respiration by Pb2+ in detached leaves and mitochondria of C3 and C4 plants. Physiol Plant 116(2):148–154

    Article  PubMed  CAS  Google Scholar 

  • Rubin BA, Merzlyak MN, Juferova SG (1976) Oxidation of lipid components in isolated chloroplasts under lighting. The substrates and products of lipid peroxidation. Russ J Plant Physiol 23:254–261

    CAS  Google Scholar 

  • Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide Axis, hydrogen peroxide and hydroxyl Axis) and peroxidase in germinating radish seeds controlled by light, gibberellin and abscisic acid. Plant Physiol 125:1591–1602

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shah K, Nongkynrih JM (2007) Metal hyperaccumulation and bioremediation. Biol Plant 51(4):618–634

    Article  CAS  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma 248(3):503–511

    Article  PubMed  CAS  Google Scholar 

  • Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5, 5′-Dithio-bis(2-nitrobenzoic acid). Anal Biochem 175:408–413

    Article  PubMed  CAS  Google Scholar 

  • Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV (2013) Occurence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Tech10:1129–1140

  • Sturgeon RJ (1990) Monosaccharides. In: Dey PM (ed) Methods in plant biochemistry, vol 2. Academic Press, London, p 1

    Chapter  Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    Article  PubMed  CAS  Google Scholar 

  • Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552(2):335–344

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vitoria AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710

    Article  PubMed  CAS  Google Scholar 

  • Wiese A, Groner F, Sonnewald U, Deppner H, Lerchl J, Hebbeker U, Flugge, U, Weber A (1999) Spinach hexokinase is located in the outer envelope membrane of plastids. FEBS Lett 46:13–18

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN. Ecology 11:1–19

    Google Scholar 

  • Yilmaz DD, Parlak KU (2011) Nickel-induced changes in lipid peroxidation, Antioxidative enzymes and metal accumulation in Lemna gibba. Int J Phytoremediation 13:805–817

    Article  PubMed  CAS  Google Scholar 

  • Zeller S, Feller U (1999) Long-distance transport of cobalt and nickel in maturing wheat. Eur J Agron 10:91–98

    Article  CAS  Google Scholar 

  • Zhao H, Kalivendi S, Zhang H, Joseph J, Nithipatikom K, Vivar VJ, Kalyanaraman B (2003) Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic Biol Med 34:1359–1368

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

NY acknowledges the receipt of project assistantship from Department of Science and Technology, Government of India, under the PURSE scheme. KV acknowledges the receipt of fellowship from CSIR-JRF, Government of India. SS and SKA acknowledge the receipt of grants from the Department of Higher Education, Government of Uttar Pradesh for Center of Excellence in Biochemistry and also from Department of Science and Technology, Government of India, under the PURSE scheme.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Samir Sharma.

Additional information

Communicated by: Jorge M. Santamaria

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yadav, N., Vati, K., Agarwal, S.K. et al. Nickel Toxicity, Altering ROS Scavenging Mechanism and Impairing Sugar Based Signaling in Vigna radiata (L.) Wilczek during Germination and Seedling Establishment. Tropical Plant Biol. 11, 65–77 (2018). https://doi.org/10.1007/s12042-018-9201-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12042-018-9201-7

Keywords

Navigation