Skip to main content

Advertisement

Log in

Evaluation of nickel tolerance in Amaranthus paniculatus L. plants by measuring photosynthesis, oxidative status, antioxidative response and metal-binding molecule content

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Among metals, Ni has been indicated as one of the most dangerous for the environment, and plants exposed to this metal are frequently reported to undergo a severe stress condition. In this work, the tolerance responses to different Ni concentrations at physiological and biochemical levels were evaluated in Amaranthus paniculatus L., a plant species previously characterised for their ability to phytoremove Ni from metal-spiked water. Results indicated a good metal tolerance of this plant species at environmentally relevant Ni concentrations, while clear symptoms of oxidative damages were detected at higher Ni concentrations, both in roots and leaves, by measuring lipid peroxide content. At the photosynthetic level, pigment content determination, chlorophyll fluorescence image analysis and gas-exchange parameter measurements revealed a progressive impairment of the photosynthetic machinery at increasing Ni concentrations in the solution. Regarding biochemical mechanisms involved in antioxidative defence and metal binding, antioxidative enzyme (ascorbate peroxidase, APX; catalase, CAT; guaiacol peroxidase, GPX; superoxide dismutase, SOD) activity, polyamine (PA) content, polyamine oxidase (PAO) activity and organic acid (OA) content were differently affected by Ni concentration in the growth solution. A role for GPX, SOD, PAs, and oxalic and citric acid in Ni detoxification is suggested. These results can contribute to elucidate the tolerance mechanisms carried out by plants when facing environmentally relevant Ni concentrations and to identify some traits characterising the physiological and biochemical responses of Amaranthus plants to the presence and bioaccumulation of Ni.

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

  • Assunção AGL, Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419

    Article  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 

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

    Article  CAS  Google Scholar 

  • Cabanillas J, Ginebreda A, Guillén D, Martínez E, Barceló D, Moragas L, Robusté J, Darbra RM (2012) Fuzzy logic based risk assessment of effluents from waste-water treatment plants. Sci Tot Environ 439:202–210

    Article  CAS  Google Scholar 

  • Callahan DL, Baker AJM, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11:2–12

    Article  CAS  Google Scholar 

  • Cerovic ZG, Masdoumier G, Ghozlen NB, Latouche G (2012) A new optical leaf-clip meter for simultaneous non-destructive assessment of leaf chlorophyll and epidermal flavonoids. Physiol Plant 146:251–260

    Article  CAS  Google Scholar 

  • Chance B, Maehly C (1955) Assay of catalase and peroxidases. Meth Enzymol 11:764–775

    Article  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719

    Article  CAS  Google Scholar 

  • Cona A, Cenci F, Cervelli M, Federico R, Mariottini P, Moreno S, Angelini R (2003) Polyamine oxidase, a hydrogen peroxide-producing enzyme, is up-regulated by light and down-regulated by auxin in the outer tissues of the maize mesocotyl. Plant Physiol 131:803–813

    Article  CAS  Google Scholar 

  • de Agazio M, Zacchini M (2001) Dimethylthiourea, a hydrogen peroxide trap, partially prevents stress effects and ascorbate peroxidase increase in spermidine-treated maize roots. Plant Cell Environ 24:237–244

    Article  Google Scholar 

  • Dietz KJ, Baier M, Krämer U (1999) Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants: from molecules to ecosystems. Springer Verlag, Berlin, pp 73–97

    Chapter  Google Scholar 

  • Draźkiewicz M, Baszyński T (2005) Growth parameters and photosynthetic pigments in leaf segments of Zea mays exposed to cadmium, as related to protection mechanisms. J Plant Physiol 162:1013–1021

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Galardi F, Corrales I, Mengoni A, Pucci S, Barletti L, Barzanti R, Arnetoli M, Gabbrielli R, Gonnelli C (2007) Intra-specific differences in nickel tolerance and accumulation in the Ni-hyperaccumulator Alyssum bertolonii. Environ Exp Bot 60:377–384

    Article  CAS  Google Scholar 

  • Gonnelli C, Galardi F, Gabbrielli R (2001) Nickel and copper tolerance and toxicity in three Tuscan populations of Silene paradoxa. Physiol Plant 113:507–514

    Article  CAS  Google Scholar 

  • Groppa MD, Tomaro ML, Benavides MP (2007) Polyamines and heavy metal stress: the antioxidant behaviour of spermine in cadmium- and copper-treated wheat leaves. Biometals 20:185–195

    Article  CAS  Google Scholar 

  • Handa AK, Matoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Biochem 48:540–546

    Article  CAS  Google Scholar 

  • Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Iori V, Pietrini F, Cheremisina A, Shevyakova NI, Radyukina N, Kuznetsov VLV, Zacchini M (2013) Growth responses, metal accumulation and phytoremoval capability in Amaranthus plants exposed to nickel under hydroponics. Water Air Soil Poll 224:1450–1459

    Article  Google Scholar 

  • Kováčik J, Klejdus B, Hedbavny J, Bačkor M (2009) Nickel uptake and its effect on some nutrient levels, amino acid contents and oxidative status in Matricaria chamomilla plants. Water Air Soil Poll 202:199–209

    Article  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Ann Rev Plant Biol 61:517–534

    Article  Google Scholar 

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

    Google Scholar 

  • Küpper 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, vol 2. Wiley Ltd, pp31–62

  • Kuznetsov VV, Radyukina NL, Shevyakova NI (2006) Polyamines and stress: biological role, metabolism, and regulation. Russ J Plant Physiol 53:658–683

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lomozik L, Gasowska A, Bregier-Jarzebowska R, Jastrzab R (2005) Coordination chemistry of polyamines and their interactions in ternary systems including metal ions, nucleosides and nucleotides. Coord Chem Rev 249:2335–2350

    Article  CAS  Google Scholar 

  • Long SP (1999) Environmental responses. In: Sage RF, Monson RK (eds) C4 Plant biology. Academic, San Diego, pp 215–249

    Chapter  Google Scholar 

  • López-Bucio J, Martínez de la Vega O, Guevara-García A, Herrera-Estrella L (2000) Enhanced phosphorus uptake in tobacco transgenic plants that overproduce citrate. Nat Biotech 18:450–453

    Article  Google Scholar 

  • Madzhugina YG, Kuznetsov VV, Shevyakova NI (2008) Plants inhabiting polygons for megapolis waste as promising species for phytoremediation. Russ J Plant Physiol 55:410–419

    Article  CAS  Google Scholar 

  • Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: cost and trade-offs between traits and environment. Environ Exp Bot 68:1–13

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Mellem JJ, Baijnath H, Odhav B (2009) Translocation and accumulation of Cr, Hg, As, Pb, Cu and Ni by Amaranthus dubius (Amaranthaceae) from contaminated sites. J Environ Sci Health 44:568–575

    Article  CAS  Google Scholar 

  • Memon AR, Schröder P (2009) Implications of metal accumulation mechanisms to phytoremediation. Environ Sci Pollut Res 16:162–175

    Article  CAS  Google Scholar 

  • Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Palacios G, Gómez I, Carbonell-Barrachina A, Navarro Pedreño J, Mataix J (1998) Effect of nickel concentration on tomato plant nutrition and dry matter yield. J Plant Nutr 21:2179–2191

    Article  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

    Article  CAS  Google Scholar 

  • Pietrini F, Iannelli MA, Montanari R, Bianconi D, Massacci A (2005) Cadmium interaction with thiols and photosynthesis in higher plants. In: Hemantaranjan A (ed) Advances in plant physiology. Scientific Publishers (India), Jodhpur, pp 313–326

    Google Scholar 

  • Pietrini F, Zacchini M, Iori V, Pietrosanti L, Ferretti M, Massacci A (2010) Spatial distribution of cadmium in leaves and its impact on photosynthesis: examples of different strategies in willow and poplar clones. Plant Biol 12:355–363

    Article  CAS  Google Scholar 

  • Robinson BH, Chiarucci A, Brooks RR, Petit D, Kirkman JH, Gregg PEH, De Dominicis V (1997) The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel. J Geochem Explor 59:75–86

    Article  CAS  Google Scholar 

  • Sagardoy R, Morales F, Rellán-Álvarez R, Abadía A, Abadía J, López-Millán AF (2011) Carboxylate metabolism in sugar beet plants grown with excess Zn. J Plant Physiol 168:730–733

    Article  CAS  Google Scholar 

  • Saito A, Higuchi K, Hirai M, Nakane R, Yoshiba M, Tadano T (2005) Selection and characterization of a nickel-tolerant cell line from tobacco (Nicotiana tabacum cv. bright yellow-2) suspension culture. Physiol Plant 125:441–453

    CAS  Google Scholar 

  • Salt DE, Prince RC, Pickering IJ (2002) Chemical speciation of accumulated metals in plants: evidence from X-ray absorption spectroscopy. Microchem J 71:255–259

    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 IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:285–308

    Article  Google Scholar 

  • Shevyakova NI, Cheremisina A, Kuznetsov VV (2011) Phytoremediation potential of Amaranthus hybrids: antagonism between nickel and iron and chelating role of polyamines. Russ J Plant Physiol 58:634–642

    Article  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

    Article  CAS  Google Scholar 

  • Subhan D, Murthy SDS (2001) Senescence retarding effect of metal ions: pigment and protein content and photochemical activities of detached primary leaves of wheat. Photosynthetica 39:53–58

    Article  CAS  Google Scholar 

  • Takao K, Rickhag M, Hegardt C, Oredsson S, Persson L (2006) Induction of apoptotic cell death by putrescine. Int J Biochem Cell Biol 38:621–628

    Article  CAS  Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  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 grown with different nickel levels. Plant Soil 196:271–276

    Article  CAS  Google Scholar 

  • Yusuf M, Fariduddin Q, Varshney P, Ahmad A (2012) Salicylic acid minimizes nickel and/or salinity-induced toxicity in Indian mustard (Brassica juncea) through an improved antioxidant system. Environ Sci Pollut Res 19:8–18

    Article  CAS  Google Scholar 

  • Zacchini M, de Agazio M (2004) Spread of oxidative damage and antioxidative response through tobacco callus cell layers after UV-C pulse treatment. Plant Physiol Biochem 42:445–450

    Article  CAS  Google Scholar 

  • Zacchini M, Iori V, Scarascia Mugnozza G, Pietrini F, Massacci A (2011) Cadmium accumulation and tolerance in Populus nigra and Salix alba. Biol Plant 55:383–386

    Article  CAS  Google Scholar 

  • Zhang X, Zhang S, Xu X, Li T, Gong G, Jia Y, Li Y, Deng L (2010) Tolerance and accumulation characteristics of cadmium in Amaranthus hybridus L. J Haz Mat 180:303–308

    Article  CAS  Google Scholar 

  • Zhao J, Shi G, Yuan Q (2008) Polyamines content and physiological and biochemical responses to ladder concentration of nickel stress in Hydrocharis dubia (Bl.) Backer leaves. Biometals 21:665–674

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was performed within the Joint Project between National Research Council of Italy (CNR) and Russian Academy of Sciences (RAS) ‘Mechanisms of plant adaptation to stress action of heavy metals: possible implications for the phytoremediation technology’. Authors wish to thank Mr. Ermenegildo Magnani and Mr. Pierangelo Bertolotto for their valuable technical assistance in heavy metal determination and HPLC analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Massimo Zacchini.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pietrini, F., Iori, V., Cheremisina, A. et al. 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 (2015). https://doi.org/10.1007/s11356-014-3349-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3349-y

Keywords

Navigation