Skip to main content
SpringerLink
Log in

Heavy Metal Toxicity: Physiological Implications of Metal Toxicity in Plants

  • Chapter
  • First Online:
Plant Metallomics and Functional Omics

Abstract

When content of HMs, such as Cd, Cr, Ni, Pb or Zn, in soils is high, then they are taken up in excess and affect different physiological processes in plants. HMs affect growth of roots and shoots, changing their morphology and anatomy. However, at low doses HMs may stimulate plant growth, which is termed hormesis. At cellular level HMs cause changes in the configuration of the endoplasmic reticulum, higher vacuolization of cells, increase in the size of the cell nucleus, changes in the shape of the Golgi apparatus, as well as disruption of chloroplasts and mitochondria ultrastructure. HMs usually cause a decrease of chlorophyll content and significant inhibition of photosynthetic rate. The use of chlorophyll a fluorescence measurements to examine photosynthetic performance revealed that HMs affect negatively photosystems II and I, diminishing considerably such parameters as φP0. Excess of HM disturb also plant water relations. As a result strong reduction in transpiration rate (E), stomatal conductance (gs) and water use efficiency (WUE) is observed. Excess of reactive oxygen species (ROS) is produced in plants as a response to heavy metal stress. High amount of ROS cause lipid peroxidation, inactivation and/or direct damage to nucleic acids, modification of proteins and carbohydrates. In consequence, content of malondialdehyde (MDA) increases as well as activity of ROS-scavenging enzymes, such as catalase (CAT), superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxidase (APX) and glutathione reductase (GR). Synthesis of phytochelatins is one of the plant responses to the presence of heavy metals (HM) in the environment. Phytochelatins (PCs) are synthesized from glutathione (GSH) by PC synthase (PCS) that is activated by HM ions. The role of PCs in HM stress relies on chelating metals, which are subsequently transported to the vacuole.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agrawal J, Sherameti I, Varma A (2011) Detoxification of heavy metals: state of art. In: Sherameti I, Varma A (eds) Detoxification of heavy metals. Soil biology, vol 30. Springer, Heidelberg, pp 1–34

    Chapter  Google Scholar 

  • Ahmad MSA, Ashraf M, Tabassam Q, Hussain M, Firdous H (2011) Lead (Pb)-induced regulation of growth, photosynthesis, and mineral nutrition in maize (Zea mays L.) plants at early growth stages. Biol Trace Elem Res 144:1229–1239

    Article  CAS  PubMed  Google Scholar 

  • Ait Ali N, Dewez D, Didur O, Popovic R (2006) Inhibition of photosystem II photochemistry by Cr is caused by the alteration of both D1 protein and oxygen evolving complex. Photosynth Res 89:81–87

    Article  CAS  Google Scholar 

  • Akhtar T, Zia-ur-Rehman M, Naeem A, Nawaz R, Ali S, Murtaza G, Maqsood MA, Azhar M, Khalid H, Rizwan M (2017) Photosynthesis and growth response of maize (Zea mays L.) hybrids exposed to cadmium stress. Environ Sci Pollut Res 24:5521–5529

    Article  CAS  Google Scholar 

  • Akhter MF, Omelon CR, Gordon RA, Moser D, Macfie SM (2014) Localization and chemical speciation of cadmium in the roots of barley and lettuce. Environ Exp Bot 100:10–19

    Article  CAS  Google Scholar 

  • Alloway BJ (1990) The origins of heavy metals in soils. In: Alloway BJ (ed) Heavy metals in soils. Blackie and Son/Wiley, Glasgow/New York, pp 29–39

    Google Scholar 

  • Alloway BJ (2013a) Introduction. In: Alloway BJ (ed) Heavy metals in soils. Trace metals and metalloids in soils and their bioavailability. Environmental pollution, vol 22, 3rd edn. Springer, Dordrecht, pp 3–9

    Google Scholar 

  • Alloway BJ (2013b) Sources of heavy metals and metalloids in soils. In: Alloway BJ (ed) Heavy metals in soils. Trace metals and metalloids in soils and their bioavailability. Environmental pollution, vol 22, 3rd edn. Springer, Dordrecht, pp 11–50

    Google Scholar 

  • Alvesa LR, Monteiroa CC, Carvalhoa RF, Ribeiroa PC, Tezottob T, Azevedoc RA, Gratãoa PL (2017) Cadmium stress related to root-to-shoot communication depends on ethylene and auxin in tomato plants. Environ Exp Bot 134:102–115

    Article  CAS  Google Scholar 

  • Amaria T, Ghnaya T, Debez A, Taamali M, Youssef NB, Lucchini G, Sacchi GA, Abdelly C (2014) Comparative Ni tolerance and accumulation potentials between Mesembryanthemum crystallinum (halophyte) and Brassica juncea: metal accumulation, nutrient status and photosynthetic activity. J Plant Physiol 171:1634–1644

    Article  CAS  Google Scholar 

  • An YJ (2004) Soil ecotoxicity assessment using cadmium sensitive plants. Environ Pollut 127:21–26

    Article  CAS  PubMed  Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Anjum SA, Ashraf U, Khan I, Tanveer M, Saleem MF, Wang L (2016) Aluminum and chromium toxicity in maize: implications for agronomic attributes, net photosynthesis, physio-biochemical oscillations, and metal accumulation in different plant Parts. Water Air Soil Pollut 227:326

    Article  CAS  Google Scholar 

  • Antosiewicz DM (1993) Mineral status of dicotyledonous crop plants in relation to their constitutional tolerance to lead. Environ Exp Bot 33:575–589

    Article  CAS  Google Scholar 

  • Antosiewicz DM (1995) The relationships between constitutional and inducible Pb-tolerance and tolerance to mineral deficits in Biscutella laevigata and Silene inflate. Environ Exp Bot 35:55–69

    Article  CAS  Google Scholar 

  • Antosiewicz DM (2005) Study of calcium-dependent lead-tolerance on plants differing in their level of Ca-deficiency tolerance. Environ Pollut 134:23–34

    Article  CAS  PubMed  Google Scholar 

  • Appenroth KJ (2010) Definition of “heavy metals” and their role in biological systems. In: Sherameti I, Varma A (eds) Soil heavy metals. Soil biology, vol 19. Springer, Heidelberg, pp 19–29

    Chapter  Google Scholar 

  • Ashraf U, Kanu AS, Mo Z, Hussain S, Anjum SA, Khan I, Abbas RN, Tang X (2015) Lead toxicity in rice: effects, mechanisms, and mitigation strategies—a mini review. Environ Sci Pollut Res 22:18318–18332

    Article  CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. Lewis Publishers, Boca Raton, pp 85–107

    Google Scholar 

  • Ban Y, Xu Z, Yang Y, Zhang H, Chen H, Tang M (2017) Effect of dark septate endophytic fungus Gaeumannomyces cylindrosporus on plant growth, photosynthesis and Pb tolerance of maize (Zea mays L.). Pedosphere 27:283–292

    Article  Google Scholar 

  • Barabasz A, Klimecka M, Kendziorek M, Weremczuk A, Ruszczyńska A, Bulska E, Antosiewicz DM (2016) The ratio of Zn to Cd supply as a determinant of metal-homeostasis gene expression in tobacco and its modulation by overexpressing the metal exporter AtHMA4. J Exp Bot 67:6201–6214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrameda-Medina Y, Montesinos-Pereira D, Romero L, Ruiz JM, Blasco B (2014) Comparative study of the toxic effect of Zn in Lactuca sativa and Brassica oleracea plants: I. Growth, distribution, and accumulation of Zn, and metabolism of carboxylates. Environ Exp Bot 107:98–104

    Article  CAS  Google Scholar 

  • Basta NT, McGowen SL (2004) Evaluation of chemical immobilization treatments for reducing heavy metal transport in a smelter-contaminated soil. Environ Pollut 127:73–82

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Bazzaz FA, Rolfe GL, Windle P (1974) Differing sensitivity of corn and Soybean photosynthesis and transpiration to lead contamination. J Environ Qual 3:156–158

    Article  CAS  Google Scholar 

  • Becerril JM, González-Murua C, Muñoz-Rueda A, De Felipe MR (1989) Changes induced by cadmium and lead in gas exchange and water relations of clover and lucerne. Plant Physiol Biochem 27:913–918

    CAS  Google Scholar 

  • Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268

    Article  CAS  PubMed  Google Scholar 

  • Benáková M, Ahmadi H, Dučaiová Z, Tylová E, Clemens S, Tůma J (2017) Effects of Cd and Zn on physiological and anatomical properties of hydroponically grown Brassica napus plants. Environ Sci Pollut Res 24:20705–20716

    Article  CAS  Google Scholar 

  • Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34

    Article  CAS  Google Scholar 

  • Benyó D, Horváth E, Németh E, Leviczky T, Takács K, Lehotai N, Feigl G, Kolbert Z, Ördög A, Gallé R, Csiszár J, Szabados L, Erdei L, Gallé A (2016) Physiological and molecular responses to heavy metal stresses suggest different detoxification mechanism of Populus deltoides and P.x canadensis. J. Plant Physiol 201:62–70

    Article  PubMed  CAS  Google Scholar 

  • Bernabé-Antonio A, Álvarez L, Buendía-González L, Maldonado-Magaña A (2015) Accumulation and tolerance of Cr and Pb using a cell suspension culture system of Jatropha curcas. Plant Cell Tiss Organ Cult 120:221–228

    Article  CAS  Google Scholar 

  • Bernardini A, Salvatori E, Di Re S, Fusaro L, Nervo G, Manes F (2016a) Natural and commercial Salix clones differ in their ecophysiological response to Zn stress. Photosynthetica 54:56–64

    Article  CAS  Google Scholar 

  • Bernardini A, Salvatori E, Guerrini V, Fusaro L, Canepari S, Manes F (2016b) Effects of high Zn and Pb concentrations on Phragmites australis (Cav.) Trin. Ex. Steudel: photosynthetic performance and metal accumulation capacity under controlled conditions. Int J Phytoremediat 18:16–24

    Article  CAS  Google Scholar 

  • Berry RA (1924) The manurial properties of lead nitrate. J. Agric Sci 14:58–65

    Article  CAS  Google Scholar 

  • Bert V, Meerts P, Saumitou-Laprade P, Salis P, Gruber W, Verbruggen N (2003) Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil 249:9–18

    Article  CAS  Google Scholar 

  • Bothe H (2011) Plants in heavy metal soils. In: Sherameti I, Varma A (eds) Detoxification of heavy metals. Soil biology, vol 30. Springer, Heidelberg, pp 35–57

    Chapter  Google Scholar 

  • Broadley MR, White PH, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  PubMed  Google Scholar 

  • Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Function of nutrients: micronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Elsevier, London, pp 191–248

    Chapter  Google Scholar 

  • Brooks RR (ed) (1998) Plants that hyperaccumulate heavy metals: their role in phytoremediation, microbiology, archeology, mineral exploration and phytomining. Cab International, Wallingford

    Google Scholar 

  • Broyer TC, Johnson CM, Paull RE (1972) Some aspects of lead in plant nutrition. Plant Soil 36:301–313

    Article  CAS  Google Scholar 

  • Brunet J, Varrault G, Zuily-Fodil Y, Repelline A (2009) Accumulation of lead in the roost of grass pea (Lathyrus sativus L.) plants triggers systemic variation in gene expression in the shoots. Chemosphere 77:1113–1120

    Article  CAS  PubMed  Google Scholar 

  • Calabrese EJ (2004) Hormesis: from marginalization to mainstream A case for hormesis as the default dose-response model in risk assessment. Toxicol Appl Pharm 197:125–136

    Article  CAS  Google Scholar 

  • Calabrese EJ (2008) Hormesis: why it is important to toxicology and toxicologists. Environ Toxicol Chem 27:1451–1474

    Article  CAS  PubMed  Google Scholar 

  • Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157:42–48

    Article  CAS  PubMed  Google Scholar 

  • Calabrese EJ, Mattson MP (2011) Hormesis provides a generalized quantitative estimate of biological plasticity. J Cell Commun Signal 5:25–38

    Article  PubMed  PubMed Central  Google Scholar 

  • Caldelas C, Araus JL, Febrero A, Bort J (2012) Accumulation and toxic effects of chromium and zinc in Iris pseudacorus L. Acta Physiol Plant 34:1217–1228

    Article  CAS  Google Scholar 

  • Cazalé AC, Clemens S (2001) Arabidopsis thaliana expresses a second functional phytochelatin synthase. FEBS Lett 507:215–219

    Article  PubMed  Google Scholar 

  • Cenkci S, Ciğerci IH, Yıldız M, Özay C, Bozdağ A, Terzi H (2010) Lead contamination reduces chlorophyll biosynthesis and genomic template stability in Brassica rapa L. Environ Exp Bot 67:467–473

    Article  CAS  Google Scholar 

  • Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Zhang X, Liu Y, Wei J, Shen W, Shen Z, Cui J (2017) Hemin-mediated alleviation of zinc, lead and chromium toxicity is associated with elevated photosynthesis, antioxidative capacity; suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regul 81:253–264

    Article  CAS  Google Scholar 

  • Cho M, Chardonnens AN, Dietz K-J (2003) Differential heavy metal tolerance of Arabidopsis halleri and Arabidopsis thaliana: a leaf slice test. New Phytol 158:287–293

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315

    Article  CAS  PubMed  Google Scholar 

  • Clijsters H, van Assche F (1985) Inhibition of photosynthesis by heavy metals. Photosynth Res 7:31–40

    Article  CAS  PubMed  Google Scholar 

  • Conn S, Gilliham M (2010) Comparative physiology of elemental distributions in plants. Ann Bot 105:1081–1102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cseh E, Fodor F, Varga A, Zaray G (2000) Effect of lead treatment on the distribution of essential elements in cucumber. J Plant Nutr 23:1095–1105

    Article  CAS  Google Scholar 

  • DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integrat Plant Biol 50:1268–1280

    Article  CAS  Google Scholar 

  • DalCorso G, Fasani E, Furini A (2013) Recent advances in the analysis of metal hyperaccumulation and hypertolerance in plants using proteomics. Front Plant Sci 4:280

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dalla Vecchia F, La Rocca N, Moro I, De Faveri S, Andreoli C, Rascio N (2005) Morphogenetic, ultrastructural and physiological damages suffered by submerged leaves of Elodea canadensis exposed to cadmium. Plant Sci 168:329–338

    Article  CAS  Google Scholar 

  • Das N, Bhattacharya S, Bhattacharyya S, Maiti MK (2017) Identification of alternatively spliced transcripts of rice phytochelatin synthase 2 gene OsPCS2 involved in mitigation of cadmium and arsenic stresses. Plant Mol Biol 94:167–183

    Article  CAS  PubMed  Google Scholar 

  • Davies FT Jr, Puryear JD, Newton RJ, Egilla JN, Saraiva Grossi JA (2001) Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). J. Plant Physiol 158:777–786

    Article  CAS  Google Scholar 

  • Davies FT Jr, Puryear JD, Newton RJ, Egilla JN, Saraiva Grossi JA (2002) Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth and gas exchange. J. Plant Nutr 25:2389–2407

    Article  CAS  Google Scholar 

  • Dazy M, Masfaraud J-F, Férard J-F (2009) Induction of oxidative stress biomarkers associated with heavy metal stress in Fontinalis antipyretica Hedw. Chemosphere 75:297–302

    Article  CAS  PubMed  Google Scholar 

  • Dehno AH, Mohtadi A (2018) The effect of different iron concentrations on lead accumulation in hydroponically grown Matthiola flavida Boiss. Ecol Res 33:757–765

    Article  CAS  Google Scholar 

  • Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228

    Article  CAS  Google Scholar 

  • Deng THB, van der Ent A, Tang YT, Sterckeman T, Echevarria G, Morel JL, Qiu RL (2018) Nickel hyperaccumulation mechanisms: a review on the current state of knowledge. Plant Soil 423:1–11

    Article  CAS  Google Scholar 

  • Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plant 35:1281–1289

    Article  CAS  Google Scholar 

  • Diwan H, Khan I, Ahmad A, Iqbal M (2010) Induction of phytochelatins and antioxidant defence system in Brassica juncea and Vigna radiata in response to chromium treatments. Plant Growth Regul 61:97–107

    Article  CAS  Google Scholar 

  • Dong Y, Ogawa T, Lin D, Koh HJ, Kamiunten H, Matsuo M, Cheng S (2006) Molecular mapping of quantitative trait loci for zinc toxicity tolerance in rice seedling (Oryza sativa L.). Field Crop Res 95:420–425

    Article  Google Scholar 

  • Đorđević B, Prášková M, Hampel D, Havel L (2017) Effects of cadmium and lead stress on somatic embryogenesis of coniferous species. Part II: changes of thiol substances. Acta Physiol Plant 39:141

    Article  CAS  Google Scholar 

  • Duffus JH (2002) “Heavy metal”—a meaningless term? Pure Appl Chem 74:793–807

    Article  CAS  Google Scholar 

  • Dunlap CE, Bouse R, Flegal AR (2000) Past leader gasoline emissions as a nonpoint source tracer in riparian systems: a study of river inputs to San Francisco bay. Environ Sci Technol 34:1211–1215

    Article  CAS  Google Scholar 

  • Ekmekçi Y ¸ Tanyolaç D¸ Ayhan B (2009) A crop tolerating oxidative stress induced by excess lead: maize. Acta Physiol Plant 31: 319–330

    Article  CAS  Google Scholar 

  • Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:756120. https://doi.org/10.1155/2015/756120

    Article  CAS  Google Scholar 

  • Fahra M, Laplaze L, El Mzibri M, Doumas P, Bendaou N, Hocher V, Bogusz D, Smouni A (2015) Assessment of lead tolerance and accumulation in metallicolous and non-metallicolous populations of Hirschfeldia incana. Environ Exp Bot 109:186–192

    Article  CAS  Google Scholar 

  • Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol 64:429–450

    Article  CAS  PubMed  Google Scholar 

  • Fergusson J (1991) The heavy elements: chemistry, environmental impact and health effects. Pergamon Press plc, Oxford

    Google Scholar 

  • Fernàndez-Martínez J, Zacchini M, Fernández-Marínc B, García-Plazaolac JI, Fleck I (2014) Gas-exchange, photo- and antioxidant protection, and metal accumulation in I-214 and Eridano Populus sp. clones subjected to elevated zinc concentrations. Environ Exp Bot 107:144–153

    Article  CAS  Google Scholar 

  • Fischer S, Kühnlenz T, Thieme M, Schmidt H, Clemens S (2014) Analysis of plant tolerance at realistic submicromolar concentrations demonstrates the role of phytochelatin synthesis for Pb detoxification. Environ Sci Technol 48:7552–7559

    Article  CAS  PubMed  Google Scholar 

  • Fodor F (2002) Physiological responses of vascular plants to heavy metals. In: Prasad M, Strzałka K (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer Academic Publishers, Dordrecht, pp 149–177

    Chapter  Google Scholar 

  • Fontes RLS, Cox FR (1998) Zinc toxicity in soybean grown at high iron concentration in nutrient solution. J Plant Nutr 21:1723–1730

    Article  CAS  Google Scholar 

  • Friedland AJ (1990) The movement of metals through soils and ecosystems. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Inc., Boca Raton, pp 7–19

    Google Scholar 

  • Fry SC, Miller JG, Dumville JC (2002) A proposed role for copper ions in cell wall loosening. Plant Soil 247:57–67

    Article  CAS  Google Scholar 

  • Furini A (ed) (2012) Plants and heavy metals. Springer, Dordrecht

    Google Scholar 

  • Gabbrielli R, Pandolfini T, Espen L, Palandri MR (1999) Growth, peroxidase activity and cytological modifications in Pisum sativum seedlings exposed to Ni2+ toxicity. J Plant Physiol 155:639–645

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M (2010) Differential effect of equal copper, cadmium and nickel concentration on biochemical reactions in wheat seedlings. Ecotoxicol Environ Saf 73:996–1003

    Article  CAS  PubMed  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 50:653–659

    Article  CAS  Google Scholar 

  • Gardea-Torresdey JL, Peralta-Videa JR, Montes M, de la Rosa G, Corral-Diaz B (2004) Bioaccumulation of cadmium, chromium and copper by Convolvulus arvensis L.: impact on plant growth and uptake of nutritional elements. Bioresour Technol 92:229–235

    Article  CAS  PubMed  Google Scholar 

  • Garg N, Aggarwal N (2011) Effects of interactions between cadmium and lead on growth, nitrogen fixation, phytochelatin, and glutathione production in mycorrhizal Cajanus cajan (L.) Millsp. J Plant Growth Regul 30:286–300

    Article  CAS  Google Scholar 

  • Gielen H, Vangronsveld J, Cuypers A (2017) Cd-induced Cu deficiency responses in Arabidopsis thaliana: are phytochelatins involved? Plant Cell Environ 40:390–400

    Article  CAS  PubMed  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Gill RA, Ali B, Islam F, Farooq MA, Gill MB, Mwamba TM, Zhou W (2015) Physiological and molecular analyses of black and yellow seeded Brassica napus regulated by 5-aminolivulinic acid under chromium stress. Plant Physiol Biochem 94:130–143

    Article  CAS  PubMed  Google Scholar 

  • Glińska S, Bartczak M, Oleksiak S, Wolska A, Gabara B, Posmyk M, Janas K (2007) Effects of anthocyanins-rich extract from red cabbage leaves on meristematic cells of Allium cepa L. roots treated with heavy metals. Ecotoxicol Environ Saf 68:343–350

    Article  PubMed  CAS  Google Scholar 

  • González Á, del Mar Gil-Diaz M, del Carmen Lobo M (2015) Response of two barley cultivars to increasing concentrations of cadmium or chromium in soil during the growing period. Biol Trace Elem Res 163:235–243

    Article  PubMed  CAS  Google Scholar 

  • González Á, del Mar Gil-Diaz M, del Carmen Lobo M (2017) Metal tolerance in barley and wheat cultivars: physiological screening methods and application in phytoremediation. J Soil Sedim 17:1403–1412

    Article  CAS  Google Scholar 

  • Gonzalez-Mendoza D, Quiroz Moreno A, Zapata-Perez O (2007) Coordinated responses of phytochelatin synthase and metallothionein genes in black mangrove, Avicennia germinans, exposed to cadmium and copper. Aquat Toxicol 83:306–314

    Article  CAS  PubMed  Google Scholar 

  • Govarthanan M, Kamala-Kannan S, Kim SA, Seo Y-S, Park J-H, Oh B-T (2016) Synergistic effect of chelators and Herbaspirillum sp. GW103 on lead phytoextraction and its induced oxidative stress in Zea mays. Arch Microbiol 198:737–742

    Article  CAS  PubMed  Google Scholar 

  • Gupta DK, Sandalio LM (eds) (2012) Metal toxicity in plants: perception, signaling and remediation. Springer, Heidelberg

    Google Scholar 

  • Gupta DK, Huang HG, Nicoloso FT, Schetinger MR, Farias JG, Li TQ, Razafindrabe BHN, Aryal N, Inouhe M (2013) Effect of Hg, As and Pb on biomass production, photosynthetic rate, nutrients uptake and phytochelatin induction in Pfaffia glomerata. Ecotoxicology 22:1403–1412

    Article  CAS  PubMed  Google Scholar 

  • Gupta V, Jatav PK, Verma R, Kothari SL, Kachhwaha S (2017) Nickel accumulation and its effect on growth, physiological and biochemical parameters in millets and oats. Environ Sci Pollut Res 24:23915–23925

    Article  CAS  Google Scholar 

  • Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connell MJ, Goldsbrough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast, Schizosaccharomyces pombe. Plant Cell 11:1153–1164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Habiba U, Ali S, Farid M, Shakoor MB, Rizwan M, Ibrahim M, Abbasi GH, Hakat T, Ali B (2015) EDTA enhanced plant growth, antioxidant defense system, and phytoextraction of copper by Brassica napus L. Environ Sci Pollut Res 22:1534–1544

    Article  CAS  Google Scholar 

  • Hammett FS (1928a) Studies in the biology of metals. I. The localization of lead by growing roots. Protoplasma 4:183–186

    Article  Google Scholar 

  • Hammett FS (1928b) Studies in the biology of metals. II. The reatardative influence of lead on root growth. Protoplasma 4:187–191

    Article  Google Scholar 

  • Hanikenne M, Nouet C (2011) Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Curr Opin Plant Biol 14:252–259

    Article  CAS  PubMed  Google Scholar 

  • He J-Y, Ren Y-F, Zhu C, Yan Y-P, Jiang D-A (2008) Effect of Cd on growth, photosynthetic gas exchange, and chlorophyll fluorescence of wild and Cd-sensitive mutant rice. Photosynthetica 46:466–470

    Article  CAS  Google Scholar 

  • Hettiarachchi GM, Pierzynski GM, Ransom MD (2000) In situ stabilization of soil lead using phosphorus and manganese oxide. Environ Sci Technol 34:4614–4619

    Article  CAS  Google Scholar 

  • Hojati M, Modarres-Sanavy SAM, Enferadi ST, Majdi M, Ghanati F, Farzadfar S, Pazoki A (2017) Cadmium and copper induced changes in growth, oxidative metabolism and terpenoids of Tanacetum parthenium. Environ Sci Pollut Res 24:12261–12272

    Article  CAS  Google Scholar 

  • Hooda PS (ed) (2010) Trace elements in soils. Wiley, Chichester

    Google Scholar 

  • Hu Y, Wang NS, Hu XJ, Lin XY, Feng Y, Jin CW (2013) Nitrate nutrition enhances nickel accumulation and toxicity in Arabidopsis plants. Plant Soil 371:105–115

    Article  CAS  Google Scholar 

  • Huang CY, Bazzaz FA, Vanderhoef LN (1974) The inhibition of soybean metabolism by cadmium and lead. Plant Physiol 54:122–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Izmaiłow R, Biskup A (2003) Reproduction of Echium vulgare L (Boraginaceae) at contaminated sites. Acta Biol Cracov 45:69–75

    Google Scholar 

  • Izmaiłow R, Kościńska-Pająk M, Kwiatkowska M, Musiał K (2015) Effect of heavy metals on reproduction in plants. In: Wierzbicka M (ed) Ecotoxicology: plants, soils, metals: monograph. Wydawnictwa Uniwersytetu Warszawskiego, Warszawa, pp 96–116. (in Polish)

    Google Scholar 

  • Jain R, Srivastava S, Solomon S, Shrivastava AK, Chandra A (2010) Impact of excess zinc on growth parameters, cell division, nutrient accumulation, photosynthetic pigments and oxidative stress of sugarcane (Saccharum spp.). Acta Physiol Plant 32:979–986

    Article  CAS  Google Scholar 

  • Javed MT, Akram MS, Tanwir K, Chaudhary HJ, Ali Q, Stoltz E, Lindberg S (2017) Cadmium spiked soil modulates root organic acids exudation and ionic contents of two differentially Cd tolerant maize (Zea mays L.) cultivars. Ecotoxicol Environ Saf 141:216–225

    Article  CAS  PubMed  Google Scholar 

  • Jean L, Bordas F, Gautier-Moussard C, Vernay P, Hitmi A, Bollinger J-C (2008) Effect of citric acid and EDTA on chromium and nickel uptake and translocation by Datura innoxia. Environ Pollut 153:555–563

    Article  CAS  PubMed  Google Scholar 

  • Jensen GH (1907) Toxic limits and stimulation effects of some salts and poisons on wheat. Bot Gazette 43:11–44

    Article  CAS  Google Scholar 

  • Jia L, He X, Chen W, Liu Z, Huang Y, Yu S (2013) Hormesis phenomena under Cd stress in a hyperaccumulator—Lonicera japonica Thunb. Ecotoxicology 22:476–485

    Article  CAS  PubMed  Google Scholar 

  • Jia L, Liu Z, Chen W, Ye Y, Yu S, He X (2015) Hormesis effects induced by cadmium on growth and photosynthetic performance in a hyperaccumulator, Lonicera japonica Thunb. J Plant Growth Regul 34:13–21

    Article  CAS  Google Scholar 

  • Jiang HM, Yang JC, Zhang JF (2007) Effects of external phosphorus on the cell ultrastructure and chlorophyll content of maize under cadmium and zinc stress. Environ Pollut 147:750–756

    Article  CAS  PubMed  Google Scholar 

  • Jinadasa N, Collins D, Holford P, Milham PJ, Conroy JP (2016) Reactions to cadmium stress in a cadmium-tolerant variety of cabbage (Brassica oleracea L.): is cadmium tolerance necessarily desirable in food crops? Environ Sci Pollut Res 23:5296–5306

    Article  CAS  Google Scholar 

  • Ju XH, Tang S, Jia Y, Guo J, Ding Y, Song Y, Zhao Y (2011) Determination and characterization of cysteine, glutathione and phytochelatins (PC2–6) in Lolium perenne L. exposed to Cd stress under ambient and elevated carbon dioxide using HPLC with fluorescence detection. J Chromatogr B 879:1717–1724

    Article  CAS  Google Scholar 

  • Juknys R, Vitkauskaitė G, Račaitė M, Venclovienė J (2012) The impacts of heavy metals on oxidative stress and growth of spring barley. Cent Eur J Biol 7:299–306

    CAS  Google Scholar 

  • Kabata-Pendias A (2011) Trace elements in soils and plants. CRC Press/Taylor and Francis Group, Boca Raton

    Google Scholar 

  • Kabata-Pendias A, Mukherjee AB (2007) Trace elements from soils to human. Springer, Heidelberg

    Book  Google Scholar 

  • Kabata-Pendias A, Pendias H (1999) Biogeochemistry of trace elements. Wydawnictwo Naukowe PWN, Warszawa. (in Polish)

    Google Scholar 

  • Kabir AH (2016) Biochemical and molecular changes in rice seedlings (Oryza sativa L.) to cope with chromium stress. Plant Biol 18:710–719

    Article  CAS  PubMed  Google Scholar 

  • Kalaji HM, Loboda T (2007) Photosystem II of barley seedlings under cadmium and lead stress. Plant Soil Environ 53:511–516

    Article  CAS  Google Scholar 

  • Kalaji HM, Rastogi A, Zivcak M, Brestic M, Daszkowska-Golec A, Sitko K, Alsharafa KY, Lotfi R, Samborska IA, Cetner MD (2018) Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. Photosynthetica 56(3):953–961

    Article  CAS  Google Scholar 

  • Kapoor S, Kobayashi A, Takatsuji H (2002) Silencing of the tapetum-specific zinc finger gene TAZ1 causes premature degeneration of tapetum and pollen abortion in petunia. Plant Cell 14:2353–2367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapusta P, Szarek-Łukaszewska G, Stefanowicz AM (2011) Direct and indirect effects of metal contamination on soil biota in a Zn-Pb post-mining and smelting area (S Poland). Environ Pollut 159:1516–1522

    Article  CAS  PubMed  Google Scholar 

  • Kelly EF, Chadwick OA, Hilinski TE (1998) The effect of plants on mineral weathering. In: van Breemen N (ed) Plant-induced soil changes: processes and feedbacks. Springer, Dordrecht, pp 21–53

    Chapter  Google Scholar 

  • Kennedy CD (1983) Transient potential shifts with pH glass electrodes due to divalent cations. Analyst 108:1003–1006

    Article  CAS  Google Scholar 

  • Kennedy CD, Gonsalves FAN (1987) The action of divalent zinc, cadmium, mercury, copper and lead on the trans-root potential and H+ efflux of excised roots. J Exp Bot 38:800–817

    Article  CAS  Google Scholar 

  • Khudsar T, Mahmooduzzafar I, Iqbal M, Sairam RK (2004) Zinc-induced changes in morpho-physiological and biochemical parameters in Artemisia annua. Biol Plant 48:255–260

    Article  CAS  Google Scholar 

  • Kopittke PM, Asher CJ, Kopittke RA, Menzies NW (2007a) Toxic effects of Pb2+ on growth of cowpea (Vigna unguiculata). Environ Pollut 150:280–287

    Article  CAS  PubMed  Google Scholar 

  • Kopittke PM, Asher CJ, Blamey FPC, Menzies NW (2007b) Toxic effects of Pb2+ on growth and mineral nutrition of signal grass (Brachiaria decumbens) and Rhodes grass (Chloris gayana). Plant Soil 300:127–136

    Article  CAS  Google Scholar 

  • Kopittke PM, Asher CJ, Menzies NW (2008) Prediction of Pb speciation in concentrated and diluted nutrient solutions. Environ Pollut 153:548–554

    Article  CAS  PubMed  Google Scholar 

  • Kopittke PM, Blamey FPC, Asher CJ, Menzies NW (2010) Trace metal phytotoxicity in solution culture: a review. J Exp Bot 61:945–954

    Article  CAS  PubMed  Google Scholar 

  • Korzeniowska J, Stanislawska-Glubiak E (2015) Phytoremediation potential of Miscanthus × giganteus and Spartina pectinata in soil contaminated with heavy metals. Environ Sci Pollut Res 22:11648–11657

    Article  CAS  Google Scholar 

  • Kováčik J, Klejdusb B, Hedbavny J, Zoń J (2011) Significance of phenols in cadmium and nickel uptake. J Plant Physiol 168:576–584

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Krämer U (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Curr Opin Biotech 16:133–141

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Krämer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272

    Article  PubMed  CAS  Google Scholar 

  • Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51

    Article  CAS  Google Scholar 

  • Krzesłowska M, Rabęda I, Basińska A, Lewandowski M, Mellerowicz EJ, Napieralska A, Samardakiewicz S, Woźny A (2016) Pectinous cell wall thickenings formation – A common defense strategy of plants to cope with Pb. Environ Pollut 214:354–361

    Article  PubMed  CAS  Google Scholar 

  • Kühnlenz T, Schmidt H, Uraguchi S, Clemens S (2014) Arabidopsis thaliana phytochelatin synthase 2 is constitutively active in vivo and can rescue the growth defect of the AtPCS1-defcient cad1-3 mutant on Cd-contaminated soil. J Exp Bot 65:4241–4253

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar A, Prasad MNV (2015) Lead-induced toxicity and interference in chlorophyll fluorescence in Talinum triangulare grown hydroponically. Photosynthetica 53:66–71

    Article  CAS  Google Scholar 

  • Kumar A, Prasad MNV, Sytar O (2012) Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere 89:1056–1065

    Article  CAS  PubMed  Google Scholar 

  • Kummerová M, Zezulka Š, Kráľová K, Masarovičová E (2010) Effect of zinc and cadmium on physiological and production characteristics in Matricaria recutita. Biol Plant 54:308–314

    Article  CAS  Google Scholar 

  • Küpper H, Parameswaran A, Leitenmaier B, Trtílek M, Šetlík I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674

    Article  PubMed  Google Scholar 

  • Kutrowska A (2013) Trace metals membrane transporters in plants. Kosmos 298:105–113. (in Polish)

    Google Scholar 

  • Kwiatkowska M, Izmaiłow R (2014) Ovules, female gametophytes and embryos are more sensitive to heavy metal pollution than anthers and pollen of Cardaminopsis arenosa (L.) Hayek (Brassicaceae), a member of calamine flora. Acta Biol Cracov Ser Bot 56(1):128–137

    Google Scholar 

  • Lamhamdi M, Bakrim A, Aarab A, Lafont R, Sayah F (2011) Lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedlings growth. C R Biol 334:118–126

    Article  CAS  PubMed  Google Scholar 

  • Lane SD, Martin ES, Garrod JF (1978) Lead toxicity effects on indole-3-ylacetic acid-induced cell elongation. Planta 144:79–84

    Article  CAS  PubMed  Google Scholar 

  • Laportea M-A, Sterckeman T, Dauguet S, Denaix L, Nguyen C (2015) Variability in cadmium and zinc shoot concentration in 14 cultivars of sunflower (Helianthus annuus L.) as related to metal uptake and partitioning. Environ Exp Bot 109:45–53

    Article  CAS  Google Scholar 

  • Lebeau T, Jézéquel K, Braud A (2011) Bioaugmentation-assisted phytoextraction applied to metal-contaminated soils: state of the art and future prospects. In: Ahamd I, Ahmad F, Pichtel J (eds) Microbes and microbial technology. Springer, New York, pp 229–266

    Chapter  Google Scholar 

  • Lee S, Moon JS, Ko T-S, Petros D, Goldsbrough PB, Korban SS (2003) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Khan MA, Yanaguchi S, Kamiya Y (2005) Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Regul 46:45–50

    Article  CAS  Google Scholar 

  • Li X, Zhang L, Li Y, Ma L, Bu N, Ma C (2012) Changes in photosynthesis, antioxidant enzymes and lipid peroxidation in soybean seedlings exposed to UV-B radiation and/or Cd. Plant Soil 352:377–387

    Article  CAS  Google Scholar 

  • Li L, Scheckel KG, Zheng L, Liu G, Xing W, Xiang G (2014) Immobilization of lead in soil influenced by soluble phosphate and calcium: lead speciation evidence. J Environ Qual 43:468–474

    Article  PubMed  CAS  Google Scholar 

  • Li B, Liu J-F, Yang J-X, Ma Y-B, Chen S-B (2015a) Comparison of phytotoxicity of copper and nickel in soils with different Chinese plant species. J Integr Agric 14:1192–1201

    Article  CAS  Google Scholar 

  • Li S, Yang W, Yang T, Chen Y, Ni W (2015b) Effects of cadmium stress on leaf chlorophyll fluorescence and photosynthesis of Elsholtzia argyi—a cadmium accumulating plant. Int J Phytoremediat 17:85–92

    Article  CAS  Google Scholar 

  • Lin Y-F, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206

    Article  CAS  PubMed  Google Scholar 

  • Lin T, Wan X, Zhang F (2016) The short-term responses of glutathione and phytochelation synthetic pathways genes to additional nitrogen under cadmium stress in poplar leaves. Russ J Plant Physiol 63:754–762

    Article  CAS  Google Scholar 

  • Liu D, Kottke I (2004) Subcellular localization of cadmium in the roots cells of Allium cepa by electron energy loss spectroscopy and cytochemistry. J Biosci 29:329–335

    Article  PubMed  Google Scholar 

  • Liu J, Li K, Xu J, Zhang Z, Ma T, Lu X, Yang J, Zhu Q (2003) Lead toxicity, uptake, and translocation in different rice cultivars. Plant Sci 165:793–802

    Article  CAS  Google Scholar 

  • Liu C-H, Huang W-D, Kao CH (2012) The decline in potassium concentration is associated with cadmium toxicity of rice seedlings. Acta Physiol Plant 34:495–502

    Article  CAS  Google Scholar 

  • Liu H, Wang H, Ma Y, Wang H, Shi Y (2016) Role of transpiration and metabolism in translocation and accumulation of cadmium in tobacco plants (Nicotiana tabacum L.). Chemosphere 144:1960–1965

    Article  CAS  PubMed  Google Scholar 

  • Lv S, Sun Z, Qian J, Ma X, Yu B, Chen X, Cao S (2012) Isolation and characterization of a novel cadmium-sensitive mutant in Arabidopsis. Acta Physiol Plant 34:1107–1118

    Article  CAS  Google Scholar 

  • Lysenko EA, Klaus AA, Pshybytko NL, Kusnetsov VV (2015) Cadmium accumulation in chloroplasts and its impact on chloroplastic processes in barley and maize. Photosynth Res 125:291–303

    Article  CAS  PubMed  Google Scholar 

  • Ma QY, Logan TJ, Traina SJ, Ryan JA (1994) Effects of NO3−, Cl−, F−, SO42−, and CO32− on Pb2+ immobilization by hydroxyapatite. Environ Sci Technol 28:408–418

    Article  CAS  PubMed  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 

  • Mahdavian K, Ghaderian SM, Schat H (2016) Pb accumulation, Pb tolerance, antioxidants, thiols, and organic acids in metallicolous and non-metallicolous Peganum harmala L. under Pb exposure. Environ Exp Bot 126:21–31

    Article  CAS  Google Scholar 

  • Maksimović I, Kastori R, Krstić L, Luković 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

    Article  Google Scholar 

  • Maksymiec W, Wójcik M, Krupa Z (2007) Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere 66:421–427

    Article  CAS  PubMed  Google Scholar 

  • Małecka A, Piechalak A, Morkunas I, Tomaszewska B (2008) Accumulation of lead in root cells of Pisum sativum. Acta Physiol Plant 30:629–637

    Article  CAS  Google Scholar 

  • Małecka A, Derba-Maceluch M, Kaczorowska K, Piechalak A, Tomaszewska B (2009) Reactive oxygen species production and antioxidative defense system in pea root tissue treated with lead ions: mitochondrial and peroxisomal level. Acta Physiol Plant 31:1065–1075

    Article  CAS  Google Scholar 

  • Małkowski E, Kita A, Galas W, Karcz W, Kuperberg JM (2002) Lead distribution in corn seedlings (Zea mays L.) and its effect on growth and the concentrations of potassium and calcium. Plant Growth Regul 37:66–76

    Article  Google Scholar 

  • Mallick S, Sinam G, Mishra RK, Sinha S (2010) Interactive effects of Cr and Fe treatments on plants growth, nutrition and oxidative status in Zea mays L. Ecotoxicol Environ Saf 73:987–995

    Article  CAS  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press Ltd., London

    Google Scholar 

  • Mathur S, Kalaji HM, Jajoo A (2016) Investigation of deleterious effects of chromium phytotoxicity and photosynthesis in wheat plant. Photosynthetica 54:185–192

    Article  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J et al (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mengel K, Kirkby EA, Kosegarten H, Appel T (2001) Principles of plant nutrition, 5th edn. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Meyer C-L, Kostecka AA, Saumitou-Laprade P, Créach A, Castric V, Pauwels M, Frérot H (2010) Variability of zinc tolerance among and within populations of the pseudometallophyte species Arabidopsis halleri and possible role of directional selection. New Phytol 185:130–142

    Article  CAS  PubMed  Google Scholar 

  • Meyer C-L, Juraniec M, Huguet S, Chaves-Rodriguez E, Salis P, Isaure MP, Goormaghtigh E, Verbruggen N (2015) Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri. J Exp Bot 66:3215–3227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michalak E, Wierzbicka M (1998) Differences in lead tolerance between Allium cepa plants developing from seeds and bulbs. Plant Soil 199:251–260

    Article  CAS  Google Scholar 

  • Milner MJ, Seamon J, Craft E, Kochian LV (2013) Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot 64:369–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039

    Article  CAS  PubMed  Google Scholar 

  • Mohtadi A, Ghaderian SM, Schat H (2012) A comparison of lead accumulation and tolerance among heavy metal hyperaccumulating and non-hyperaccumulating metallophytes. Plant Soil 352:267–276

    Article  CAS  Google Scholar 

  • Monnet F, Vaillant N, Vernay P, Coudret A, Sallanon H, Hitmi A (2001) Relationship between PSII activity, CO2 fixation, and Zn, Mn and Mg contents of Lolium perenne under zinc stress. J Plant Physiol 158:1137–1144

    Article  CAS  Google Scholar 

  • Moradi L, Ehsanzadeh P (2015) Effects of Cd on photosynthesis and growth of safflower (Carthamus tinctorius L.) genotypes. Photosynthetica 53:506–518

    Article  CAS  Google Scholar 

  • Moya JL, Ros R, Picazo I (1993) Influence of cadmium and nickel on growth, net photosynthesis and carbohydrate distribution in rice plants. Photosynth Res 36:75–80

    Article  CAS  PubMed  Google Scholar 

  • Mroczek-Zdyrska M, Wójcik M (2012) The influence of selenium on root growth and oxidative stress induced by lead in Vicia faba L. minor plants. Biol Trace Elem Res 147:320–328

    Article  CAS  PubMed  Google Scholar 

  • Murshed R, Lopez-Lauri F, Sallanon H (2008) Microplate quantification of enzymes of the plant ascorbate–glutathione cycle. Anal Biochem 383:320–322

    Article  CAS  PubMed  Google Scholar 

  • Mvamba TM, Ali S, Ali B, Lwalaba JL, Liu H, Farooq MA, Shou J, Zhou W (2016) Interactive effects of cadmium and copper on metal accumulation, oxidative stress, and mineral composition in Brassica napus. Int J Environ Sci Technol 13:2163–2174

    Article  CAS  Google Scholar 

  • Nada E, Ferjani BA, Ali R, Bechir BR, Imed M, Makki B (2007) Cadmium-induced growth inhibition and alteration of biochemical parameters in almond seedlings grown in solution culture. Acta Physiol Plant 29:57–62

    Article  CAS  Google Scholar 

  • Nadgórska-Socha A, Ptasiński B, Kita A (2013) Heavy metal bioaccumulation and antioxidative responses in Cardaminopsis arenosa and Plantago lanceolata leaves from metalliferous and non-metalliferous sites: a field study. Ecotoxicology 22:1422–1434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nakazawa R, Ozawa T, Naito T, Kameda Y, Takenaga H (2001) Interactions between cadmium and nickel in phytochelatin biosynthesis and the detoxification of the two metals in suspension-cultured tobacco cells. Biol Plant 44:627–630

    Article  CAS  Google Scholar 

  • Nakos G (1983) Total concentrations of Mn, Zn and Cu in certain forest soils in Greece. Plant Soil 74:137–140

    Article  CAS  Google Scholar 

  • Nanda R, Agrawal V (2016) Elucidation of zinc and copper induced oxidative stress, DNA damage and activation of defence system during seed germination in Cassia angustifolia Vahl. Environ Exp Bot 125:31–41

    Article  CAS  Google Scholar 

  • Nsanganwimana F, Pourrut B, Mench M, Douay F (2014) Suitability of Miscanthus species for managing inorganic and organic contaminated land and restoring ecosystem services. A review. J Environ Manag 143:123–134

    Article  CAS  Google Scholar 

  • Olko A (2009) Physiological aspects of plant heavy metal tolerance. Kosmos 58:221–228. (in Polish)

    CAS  Google Scholar 

  • Osma E, Elveren M, Karakoyun G (2017) Heavy metal accumulation affects growth of Scots pine by causing oxidative damage. Air Qual Atmos Health 10:85–92

    Article  CAS  Google Scholar 

  • Oustriere N, Marchand L, Rosette G, Friesl-Hanl W, Mench M (2017) Wood-derived-biochar combined with compost or iron grit for in situ stabilization of Cd, Pb and Zn in a contaminated soil. Environ Sci Pollut Res 24:7468–7481

    Article  CAS  Google Scholar 

  • Panda SK, Choudhury S (2005) Chromium stress in plant. Braz J Plant Physiol 17:95–102

    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 

  • Parkinson BM, Pacini E (1995) A comparison of tapetal structure and function in pteridophytes and angiosperms. Plant Syst Evol 198:55–88

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Patniak AR, Achary VMM, Panda B (2013) Chromium (VI)-induced hormesis and genotoxicity are mediated through oxidative stress in root cells of Allium cepa L. Plant Growth Regul 71:157–170

    Article  CAS  Google Scholar 

  • Per TS, Khan S, Asgher M, Bano B, Khan NA (2016) Photosynthetic and growth responses of two mustard cultivars differing in phytocystatin activity under cadmium stress. Photosynthetica 54:491–501

    Article  CAS  Google Scholar 

  • Peralta JR, Gardea Torresdey JL, Tiemann KJ, Gomez E, Arteaga S, Rascon E (2001) Uptake and effects of five heavy metals on seed germination and plant growth in alfalfa (Medicago sativa) L. Bull Environ Contam Toxicol 66:727–734

    CAS  PubMed  Google Scholar 

  • Phang IC, Leung DWM, Taylor HH, Burritt DJ (2011) The protective effect of sodium nitroprusside (SNP) treatment on Arabidopsis thaliana seedlings exposed to toxic level of Pb is not linked to avoidance of Pb uptake. Ecotoxicol Environ Saf 74:1310–1315

    Article  CAS  PubMed  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 

  • Pogrzeba M, Rusinowski S, Sitko K, Krzyżak J, Skalska A, Małkowski E, Ciszek D, Werle S, McCalmont JP, Mos M, Kalaji HM (2017) Relationships between soil parameters and physiological status of Miscanthus x giganteus cultivated on soil contaminated with trace elements under NPK fertilisation vs. microbial inoculation. Environ Pollut 225:163–174

    Article  CAS  PubMed  Google Scholar 

  • Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217-218:8–17

    Article  CAS  PubMed  Google Scholar 

  • Poschenrieder C, Cabot C, Martos S, Gallego B, Barceló J (2013) Do toxic ions induce hormesis in plants? Plant Sci 212:15–25

    Article  CAS  PubMed  Google Scholar 

  • Postrigan’ BN, Knyazev AV, Kuluev BR, Chemeris AV (2013) Effect of cadmium on promoter activity of rice phytochelatin synthase gene in transgenic tobacco plants. Russ J Plant Physiol 60:701–705

    Article  CAS  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, amd detoxification in plants. Rev Environ Contam Toxicol 213:113–136

    CAS  PubMed  Google Scholar 

  • Przedpełska-Wąsowicz EM, Wierzbicka M (2011) Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells. Protoplasma 248:663–671

    Article  PubMed  CAS  Google Scholar 

  • Przymusiński R, Woźny A (1985) The reactions of lupin roots to the presence of lead in the medium. Biochem Physiol Pflanzen 180:309–318

    Article  Google Scholar 

  • Qiao X, Shi G, Chen L, Tian X, Xu X (2013) Lead-induced oxidative damage in steriled seedlings of Nymphoides peltatum. Environ Sci Polut Res 20:5047–5055

    Article  CAS  Google Scholar 

  • Rabęda I, Bilski H, Mellerowicz EJ, Napieralska A, Suski S, Woźny A, Krzesłowska M (2015) Colocalization of low-methylesterified pectins and Pb deposits in the apoplastu of aspen roots exposed to lead. Environ Pollut 205:315–326

    Article  PubMed  CAS  Google Scholar 

  • Rascio N, Navari-Izzo F (2010) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181

    Article  PubMed  CAS  Google Scholar 

  • Rauser WE (1995) Phytochelatins and related peptides. Structure, biosynthesis, and function. Plant Physiol 109:1141–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–229

    Google Scholar 

  • Rengel Z, Graham RD (1996) Uptake of zinc from chelate-buffered nutrient solutions by wheat genotypes differing in zinc efficiency. J Exp Bot 47:217–226

    Article  CAS  Google Scholar 

  • Rivelli AR, Maria SD, Puschenreiter M, Gherbin P (2012) Accumulation of cadmium, zinc, and copper by Helianthus annuus L.: impact on plant growth and uptake of nutritional elements. Int J Phytoremediat 14:320–334

    Article  CAS  Google Scholar 

  • Rizvi A, Khan M-S (2017) Biotoxic impact of heavy metals on growth, oxidative stress and morphological changes in root structure of wheat (Triticum aestivum L.) and stress alleviation by Pseudomonas aeruginosa strain CPSB1. Chemosphere 185:942–952

    Article  CAS  PubMed  Google Scholar 

  • Rizwan M, Ali S, Rehman MZ, Javed MR, Bashir A (2018) Lead toxicity in cereals and its management strategies: a critical review. Water Air Soil Pollut 229:211

    Article  CAS  Google Scholar 

  • Robinson MWH, Bañelos G, Conesa HM, Evangelou MWH, Schulin R (2009) The phytomanagement of trace elements in soil. Crit Rev Plant Sci 28:240–266

    Article  CAS  Google Scholar 

  • Rodrigues dos Reis A, Barcelos J, Wruck de Souza Osório CR, Santos EF, Lisboa LAM, Santini JMK, Dornelas dos Santos JM, Junior FE, Campos M, Monteiro de Figueiredo PA, Lavres J, Gratão PP (2017) A glimpse into the physiological, biochemical and nutritional status of soybean plants under Ni-stress conditions. Environ Exp Bot 144:76–87

    Article  CAS  Google Scholar 

  • Rodriguez N, Amils R, Jiménez-Ballesta R, Rufo L, de la Fuente V (2007) Heavy metal content in Erica andevalensis: an endemic plant from the extreme acidic environment of Tinto River and its soils. Arid Land Res Manag 21:51–65

    Article  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 116:148–154

    Article  CAS  PubMed  Google Scholar 

  • Ross SM (1994a) Sources and forms of potentially toxic metals in soil—plant systems. In: Ross SM (ed) Toxic metals in soil-plant systems. Wiley, Chichester, pp 3–25

    Google Scholar 

  • Ross SM (1994b) Retention, transformation and mobility of toxic metals in soils. In: Ross SM (ed) Toxic metals in soil-plant systems. Wiley, Chichester, pp 63–152

    Google Scholar 

  • Rout GR, Sanghamitra S, Das P (2000) Effects of chromium and nickel on germination and growth in tolerant and non-tolerant populations of Echinochloa colona (L). Chemosphere 40:855–859

    Article  CAS  PubMed  Google Scholar 

  • Saha J, Majumder B, Mumtaz B, Biswas A (2017) Arsenic-induced oxidative stress and thiol metabolism in two cultivars of rice and its possible reversal by phosphate. Acta Physiol Plant 39:263

    Google Scholar 

  • Sanitá di Toppi L, Fossati F, Musetti R, Mikerezi I, Favali MA (2002) Effects of hexavalent chromium on maize, tomato, and cauliflower plants. J Plant Nutr 25:701–717

    Article  Google Scholar 

  • Sauvé S, McBride M, Hendershot W (1998) Lead phosphate solubility in water and soil suspension. Environ Sci Technol 32:388–393

    Article  Google Scholar 

  • Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 53:2381–2392

    Article  CAS  PubMed  Google Scholar 

  • Sengar RS, Gautam M, Sengar RS, Garg SK, Sengar K, Chaudhary R (2008) Lead stress effects on physiobiochemical activities of higher plants. Rev Environ Contam Toxicol 196:73–93

    CAS  PubMed  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

    Article  CAS  Google Scholar 

  • Serrano N, Díaz-Cruz JM, Ariño C, Esteban M (2015) Recent contributions to the study of phytochelatins with an analytical approach. Trends Anal Chem 73:129–145

    Article  CAS  Google Scholar 

  • Seth CS, Chaturvedi PK, Misra V (2008) The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotox Environ Safe 71:76–85

    Article  CAS  Google Scholar 

  • Shahid M, Dumat C, Pourrut B, Abbas G, Shahid N, Pinelli E (2015) Role of metal speciation in lead-induced oxidative stress to Vicia faba roots. Russ J Plant Physiol 62:448–454

    Article  CAS  Google Scholar 

  • Shanker AK, Djanaguiraman M, Sudhagar R, Chandrashekar CN, Pathmanabhan G (2004) Differential antioxidative response of ascorbate glutathione pathway enzymes and metabolites to chromium speciation stress in green gram (Vigna radiata (L.) R.Wilczek. cv CO 4) roots. Plant Sci 166:1035–1043

    Article  CAS  Google Scholar 

  • Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52

    Article  CAS  Google Scholar 

  • Shaw AJ (ed) (1990) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Inc., Boca Raton

    Google Scholar 

  • Sherameti I, Varma A (eds) (2010) Soil heavy metals. Soil biology, vol 19. Springer, Heidelberg

    Google Scholar 

  • Sherameti I, Varma A (eds) (2015) Heavy metal contamination of soils. Monitoring and remediation. Soil biology, vol 44. Springer, Cham

    Google Scholar 

  • Shi GR, Cai QS (2009) Photosynthetic and anatomic responses of peanut leaves to zinc stress. Biol Plant 53:391–394

    Article  CAS  Google Scholar 

  • Shi GR, Cai QS, Liu QQ, Wu L (2009) Salicylic acid-mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake, photosynthesis, and antioxidant enzymes. Acta Physiol Plant 31:969–977

    Article  CAS  Google Scholar 

  • Silva S, Pinto G, Santos C (2017) Low doses of Pb affected Lactuca sativa photosynthetic performance. Photosynthetica 55:50–57

    Article  CAS  Google Scholar 

  • Simek J, Tuma J, Dohnal V, Musil K, Ducaiová Z (2016) Salicylic acid and phenolic compounds under cadmium stress in cucumber plants (Cucumis sativus L.). Acta Physiol Plant 38:172

    Article  CAS  Google Scholar 

  • Simmons RW, Chaney RL, Angle JS, Kruatrachue M, Klinphoklap S, Reeves RD, Bellamy P (2014) Towards practical cadmium Phytoextraction with Noccaea caerulescens. Int J Phytoremediat 17:191–199

    Article  CAS  Google Scholar 

  • Singh S, Prasad SM (2015) IAA alleviates Cd toxicity on growth, photosynthesis and oxidative damages in eggplant seedlings. Plant Growth Regul 77:87–98

    Article  CAS  Google Scholar 

  • Singh V, Tripathi B-N, Sharma V (2016) Interaction of Mg with heavy metals (Cu, Cd) in T. aestivum with special reference to oxidative and proline metabolism. J Plant Res 129:487–497

    Article  CAS  PubMed  Google Scholar 

  • Sitko K, Rusinowski S, Kalaji HM, Szopiński M, Małkowski E (2017) Photosynthetic efficiency as bioindicator of environmental pressure in A. halleri. Plant Physiol 175:290–302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Słomka A, Kawalec P, Kellner K, Jędrzejczyk-Korycińska M, Rostański A, Kuta E (2010) Was reduced pollen viability in Viola tricolor L. the result of heavy metal pollution or rather the test applied? Acta Biol Cracov Ser Bot 52(1):123–127

    Google Scholar 

  • Słomka A, Jędrzejczyk-Korycińska M, Rostański A, Karcz J, Kawalec P, Kuta E (2012) Heavy metals in soil affect reproductive processes more than morphological characters in Viola tricolor. Environ Exp Bot 75:204–211

    Article  CAS  Google Scholar 

  • Smýkalová I, Zámečníková B (2003) The relationship between salinity and cadmium stress in barley. Biol Plant 46:269–273

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sresty TVS, Madhava Rao KV (1999) Ultrastructural alterations in response to zinc and nickel stress in the root cells of pigeonpea. Environ Exp Bot 41:3–13

    Article  CAS  Google Scholar 

  • Stiborová M, Ditrichová M, Březinová A (1987) Effect of heavy metal ions on growth and biochemical characteristics of photosynthesis of barley and maize seedlings. Biol Plant 29:453–467

    Article  Google Scholar 

  • Stroiński A, Chadzinikolau T, Giżewska K, Zielezińska M (2010) ABA or cadmium induced phytochelatin synthesis in potato tubers. Biol Plant 54:117–120

    Article  CAS  Google Scholar 

  • Subrahmanyam D (2008) Effects of chromium toxicity on leaf photosynthetic characteristics and oxidative changes in wheat (Triticum aestivum L.). Photosynthetica 46:339–345

    Article  CAS  Google Scholar 

  • Sun Q, Wang XR, Ding SM, Yuan XF (2005) Effects of Interactions between cadmium and zinc on phytochelatin and glutathione production in wheat (Triticum aestivum L.). Environ Toxicol 20:195–201

    Article  CAS  PubMed  Google Scholar 

  • Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999

    Article  CAS  Google Scholar 

  • Tack FMG (2010) Trace elements: general soil chemistry, principles and processes. In: Hooda PS (ed) Trace elements in soils. Blackwell Publishing, Ltd, London, pp 9–37

    Chapter  Google Scholar 

  • Talke IN, Hanikenne M, Krämer U (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang YT, Qiua RL, Zeng XW, Ying RR, Yu FM, Zhou XY (2009) Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ Exp Bot 66:126–134

    Article  CAS  Google Scholar 

  • Tennstedt P, Peisker D, Böttcher C, Trampczynska A, Clemens S (2009) Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol 149:938–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thangavel P, Long S, Minocha R (2007) Changes in phytochelatins and their biosynthetic intermediates in red spruce (Picea rubens Sarg.) cel suspension cultures under cadmium and zinc stress. Plant Cell Tiss Organ Cult 88:201–216

    Article  CAS  Google Scholar 

  • Thomine S, Lelievre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695

    Article  CAS  PubMed  Google Scholar 

  • Titov AF, Talanova VV, Boeva NP (1996) Growth responses of barley and wheat seedlings to lead and cadmium. Biol Plant 38:431–436

    Article  CAS  Google Scholar 

  • Tripathi DK, Singh VP, Prasad SM, Chauhan DK, Dubey NK (2015) Silicon nanoparticles (SiNp) alleviate chromium (VI) phytotoxicity in Pisum sativum (L.) seedlings. Plant Physiol Biochem 96:189–198

    Article  CAS  PubMed  Google Scholar 

  • Trivedi S, Erdei L (1992) Effects of cadmium and lead on the accumulation of Ca2+ and K+ and on the influx and translocation of K+ in wheat pf low and high K+ status. Physiol Plant 84:94–100

    Article  CAS  Google Scholar 

  • Tu C, He T, Liu C, Lu X, Lang Y (2011) Accumulation of trace elements in agricultural topsoil under different geological background. Plant Soil 349:241–251

    Article  CAS  Google Scholar 

  • Turpeinen R, Salminene J, Kairesalo T (2000) Mobility and bioavailability lead in contaminated boreal forest soil. Environ Sci Technol 34:5152–5156

    Article  CAS  Google Scholar 

  • Uraguchi S, Tanaka N, Hofmann C, Abiko K, Ohkama-Ohtsu N, Weber M, Kamiya T, Sone Y, Nakamura R, Takanezawa Y, Kiyono M, Fujiwara T, Clemens S (2017) Phytochelatin synthase has contrasting effects on cadmium and arsenic accumulation in rice grains. Plant Cell Physiol 58:1730–1742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van de Mortel JE, Almar Villanueva L, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Ver Loren van Themaat E, Koornneef M, Aarts MGM (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van de Mortel JE, Schat H, Moerland PD, Ver Loren van Themaat E, van der Ent S, Blankestijn H, Ghandilyan A, Tsiatsiani S, Aarts MGM (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324

    Article  PubMed  CAS  Google Scholar 

  • Van der Ent A, Baker JM, Reeves D, Pollard J, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334

    Article  CAS  Google Scholar 

  • Vangronsveld J, Colpaert JV, van Tichelen KK (1996) Reclamation of a bare industrial area contaminated by non-ferrous metals: physicochemical and biological evaluation of the durability of soil treatment and revegetation. Environ Pollut 94:131–140

    Article  CAS  PubMed  Google Scholar 

  • Vassilev A, Lidon FC, Ramalho JC, do Céu Matos M, Bareiro MG (2004) Shoot cadmium accumulation and photosynthetic performance of barley plants exposed to high cadmium treatments. J Plant Nutr 27:775–795

    Article  CAS  Google Scholar 

  • Vassilev A, Nikolova A, Koleva L, Lidon F (2011) Effects of excess Zn on growth and photosynthetic performance of young bean plants. J Phytol 3:58–62

    CAS  Google Scholar 

  • Velikova V, Tsonev T, Loreto F, Centritto M (2011) Changes in photosynthesis, mesophyll conductance to CO2, and isoprenoid emissions in Populus nigra plants exposed to excess nickel. Environ Pollut 159:1058–1066

    Article  CAS  PubMed  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776

    Article  CAS  PubMed  Google Scholar 

  • Verbruggen N, Juraniec M, Baliardini C, Meyer CL (2013) Tolerance to cadmium in plants: the special case of hyperaccumulators. Biometals 26:633–638

    Article  CAS  PubMed  Google Scholar 

  • Verkleij JAC, Golan-Goldhirsh A, Antosiewicz DM, Schwitzguébel J-P, Schröder P (2009) Dualites in plant tolerance to pollutants and their uptake and translocation to the upper plant parts. Environ Exp Bot 67:10–22

    Article  CAS  Google Scholar 

  • Vesely T, Neuberg M, Trakal L, Szakova J, Tlustoš P (2012) Water lettuce Pistia stratiotes L. response to lead toxicity. Water Air Soil Pollut 223:1847–1859

    Article  CAS  Google Scholar 

  • Vogel AI (1951) A text-book of quantitative inorganic analysis. Theory and practice, 2nd edn. Longmans, Green and Company, Ltd., Suffolk

    Google Scholar 

  • Vondráčková S, Hejcman M, Száková J, Müllerová V, Tlustš P (2014) Soil chemical properties affect the concentration of elements (N, P, K, Ca, Mg, As, Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn) and their distribution between organs of Rumex obtusifolius. Plant Soil 379:231–245

    Article  CAS  Google Scholar 

  • Wang EX, Benoit G (1996) Mechanisms controlling the mobility of lead in the spodosols of a northern hardwood forest ecosystem. Environ Sci Technol 30:2211–2219

    Article  CAS  Google Scholar 

  • Wang Y, Wang S, Nan Z, Ma J, Zang F, Chen Y, Li Y, 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

    Article  CAS  Google Scholar 

  • Warne MS, Heemsbergen D, Stevens D, McLaughlin M, Cozens G, Whatmuff M, Broos K, Barry G, Bell M, Nash D, Pritchard D, Penney N (2008) Modeling the toxicity of copper and zinc salts to wheat in 14 soils. Environ Toxicol Chem 27:786–792

    Article  PubMed  Google Scholar 

  • Weber M, Harada E, Vess C, Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281

    Article  CAS  PubMed  Google Scholar 

  • Wierzbicka M (1987) Lead accumulation and its translocation barriers in roots of Allium cepa L.—autoradiographic and ultrastructural studies. Plant Cell Environ 10:17–26

    Article  CAS  PubMed  Google Scholar 

  • Wierzbicka M (1989) Disturbances in cytokinesis caused by inorganic lead. Environ Exp Bot 29:123–133

    Article  CAS  Google Scholar 

  • Wierzbicka M (2015) Defense of plants against heavy metals. In: Wierzbicka M (ed) Ecotoxicology: plants, soils, metals: monograph. Wydawnictwa Uniwersytetu Warszawskiego, Warszawa, pp 96–116. (in Polish)

    Google Scholar 

  • Wierzbicka M, Obidzińska J (1998) The effect of lead on seed imbibition and germination in different plant species. Plant Sci 137:155–171

    Article  CAS  Google Scholar 

  • Wójcik M, Tukendorf A (1999) Cd-tolerance of maize, rye and wheat seedlings. Acta Phys Plant 21:99–107

    Article  Google Scholar 

  • Wójcik M, Sugier P, Siebielec G (2014) Metal accumulation strategies in plants spontaneously inhabiting Zn-Pb waste deposits. Sci Total Environ 487:313–322

    Article  PubMed  CAS  Google Scholar 

  • Woźny A, Jerczynska E (1991) The effect of lead on early stages of Phaseolus vulgaris L. growth in vitro conditions. Biol Plant 33:32–39

    Article  Google Scholar 

  • Wu X, He J, Ding H, Zhu Z, Chen J, Xu S, Zh D (2015) Modulation of zinc-induced oxidative damage in Solanum melongena by 6-benzylaminopurine involves ascorbate–glutathione cycle metabolism. Environ Exp Bot 116:1–11

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

    Article  CAS  Google Scholar 

  • Ying R-R, Qiu R-L, Tang Y-T, Hua P-J, Qiu H, Chen H-R, Shi T-H, Morel J-L (2010) Cadmium tolerance of carbon assimilation enzymes and chloroplast in Zn/Cd hyperaccumulator Picris divaricata. J Plant Physiol 167:81–87

    Article  CAS  PubMed  Google Scholar 

  • Zeid IM (2001) Responses of Phaseolus vulgaris to chromium and cobalt treatments. Biol Plant 44:111–115

    Article  CAS  Google Scholar 

  • Zeng F, Chen S, Miao Y, Wu F, Zhang G (2008) Changes of organic acid exudation and rhizosphere pH in rice plants under chromium stress. Environ Pollut 155:284–289

    Article  CAS  PubMed  Google Scholar 

  • Zeng L, Zhu T, Gao Y, Wang Y, Ning C, Björn LO, Chen D, Li S (2017) Effects of Ca addition on the uptake, translocation, and distribution of Cd in Arabidopsis thaliana. Ecotoxicol Environ Saf 139:228–237

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Fukami M, Sekimoto H (2000) Genotypic differences in effects of cadmium on growth and nutrient compositions in wheat. J Plant Nutr 23:1337–1350

    Article  CAS  Google Scholar 

  • Zhang X, Gao B, Xia H (2014) Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of bana grass and vetiver grass. Ecotox Environ Safe 106:102–108

    Article  CAS  Google Scholar 

  • Zornoza P, Roblesand S, Martin N (1999) Alleviation of nickel toxicity by ammonium supply to sunflower plants. Plant Soil 208:221–226

    Article  CAS  Google Scholar 

  • Zorrig W, Shahzad Z, Abdelly C, Berthomieu P (2012) Calcium enhances cadmium tolerance and decreases cadmium accumulation in lettuce (Lactuca sativa). Afr J Biotechnol 11:8441–8448

    CAS  Google Scholar 

Download references

Acknowledgements

We apologize to authors whose relevant works on physiological implications of metal toxicity in plants have not been cited, either inadvertently or because of length constraints. We also wish to thank Mr. Szymon Rusinowski for providing of several important references. Finally, we thank Ms Elżbieta Małkowski for drawing Figure 1.

Author information

Authors and Affiliations

  1. Department of Plant Physiology, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Katowice, Poland

    Eugeniusz Małkowski, Krzysztof Sitko, Paulina Zieleźnik-Rusinowska, Żaneta Gieroń & Michał Szopiński

Authors
  1. Eugeniusz Małkowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Krzysztof Sitko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paulina Zieleźnik-Rusinowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Żaneta Gieroń
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michał Szopiński
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eugeniusz Małkowski .

Editor information

Editors and Affiliations

  1. University of Technology, Sydney, NSW, Australia

    Gaurav Sablok

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Małkowski, E., Sitko, K., Zieleźnik-Rusinowska, P., Gieroń, Ż., Szopiński, M. (2019). Heavy Metal Toxicity: Physiological Implications of Metal Toxicity in Plants. In: Sablok, G. (eds) Plant Metallomics and Functional Omics. Springer, Cham. https://doi.org/10.1007/978-3-030-19103-0_10

Download citation

Publish with us

Policies and ethics

Search

Navigation