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Current Scenario of Pb Toxicity in Plants: Unraveling Plethora of Physiological Responses

  • Sukhmeen Kaur KohliEmail author
  • Neha Handa
  • Shagun Bali
  • Kanika Khanna
  • Saroj Arora
  • Anket Sharma
  • Renu BhardwajEmail author
Chapter
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 249)

Abstract

Lead (Pb) is an extremely toxic metal for all living forms including plants. It enters plants through roots from soil or soil solution. It is considered as one of the most eminent examples of anthropogenic environmental pollutant added in environment through mining and smelting of lead ores, coal burning, waste from battery industries, leaded paints, metal plating, and automobile exhaust. Uptake of Pb in plants is a nonselective process and is driven by H+/ATPases. Translocation of Pb metal ions occurs by apoplastic movement resulting in deposition of metal ions in the endodermis and is further transported by symplastic movement. Plants exposed to high concentration of Pb show toxic symptoms due to the overproduction of reactive oxygen species (ROS) through Fenton-Haber-Weiss reaction. ROS include superoxide anion, hydroxyl radical, and hydrogen peroxide, which reach to macro- and micro-cellular levels in the plant cells and cause oxidative damage. Plant growth and plethora of biochemical and physiological attributes including plant growth, water status, photosynthetic efficiency, antioxidative defense system, phenolic compounds, metal chelators, osmolytes, and redox status are adversely influenced by Pb toxicity. Plants respond to toxic levels of Pb in varied ways such as restricted uptake of metal, chelation of metal ions to the root endodermis, enhancement in activity of antioxidative defense, alteration in metal transporters expression, and involvement of plant growth regulators.

Keywords

Antioxidants Lead Metal chelators Osmolytes Phenolic compounds 

Abbreviations

AAS

Atomic absorption spectrophotometer

ABA

Abscisic acid

ABC

ATP-binding cassettes

Ag

Silver

APOX

Ascorbate peroxidase

As

Arsenic

ATSDR

Agency for Toxic Substances and Disease Registry

Au

Gold

Ca

Calcium

CAA

Clean Air Act

CAT

Catalase

Chl a

Chlorophyll a

Chl b

Chlorophyll b

CO2

Carbon dioxide

Cu

Copper

Cu/Zn-SOD

Copper/zinc superoxide dismutase

DHAR

Dehydroascorbate reductase

EDTA

Ethylene diamine tetraacetic acid

ETC

Electron transport chain

Fe

Iron

GB

Glycine betaine

GPOX

Glutathione peroxidase

GR

Glutathione reductase

GSH

Glutathione

GSSG

Glutathione disulfide

GST

Glutathione-S-transferase

H2O2

Hydrogen peroxide

Hg

Mercury

HO.

Hydroxyl radical

ICP-MS

Inductively coupled plasma-mass spectrometry

ICP-AES

Inductively coupled plasma atomic emission spectrometry

K

Potassium

MCs

Metallothionins

MDA

Malondialdehyde

MDHAR

Monodehydroascorbate reductase

Mg

Magnesium

Mn

Manganese

Mn/Zn-SOD

Manganese/zinc superoxide dismutase

Na

Sodium

Ni

Nickel

\( {\mathrm{NO}}_3^{-} \)

Nitrate

1O2

Singlet oxygen radical

O2−

Superoxide anion radical

P

Phosphorus

Pb

Lead

PCS

Phytochelatin synthetase

PCs

Phytochelatins

PGRs

Plant growth regulators

\( {\mathrm{PO}}_4^{-} \)

Phosphate

POD

Guaiacol peroxidase

ROS

Reactive oxygen species

SDWA

Safe Drinking Water Act

SOD

Superoxide dismutase

TBARs

Thiobarbituric acid

TF

Transfer factor

TSCA

Toxic Substances Control Act

WHO

World Health Organization

Zn

Zinc

Notes

Acknowledgment

Financial help for carrying out above work was given by the University Grant Commission, Government of India, GOI (Maulana Azad National Fellowship), and DST-FIST, of GOI, is also duly acknowledged.

Contribution of Authors

Sukhmeen Kaur Kohli, Renu Bhardwaj, and Saroj Arora designed the layout of the review article. Neha Handa, Shagun Bali, Kanika Khanna, and Anket Sharma helped in writing of the different sections of the manuscript. Renu Bhardwaj, Sukhmeen Kaur Kohli, and Kanika Khanna revised the manuscript to present form.

References

  1. Agency for Toxic Substances and Disease Registry (2007) CERCLA priority list of hazardous substances. ATSDR Home. Retrieved March 22, 2011. From http://www.atsdr.cdc.gov/cercla/07list.html
  2. Aggarwal A, Sharma I, Tripathi BN, Munjal AK, Baunthiyal M, Sharma V (2012) Metal toxicity and photosynthesis. In: Itoh S, Mohanty P, Guruprasad KN (eds.) Photosynthesis: Overviews on Recent Progress and Future Perspectives. IK International Publishing House (Pvt.) Limited, New Delhi, pp 229–236Google Scholar
  3. Allen SE, Grimshaw HM, Parkinson JA, Quarmby C, Roberts JD (1976) Chemical analysis. In: Chapman SB (ed) Methods in plant ecology. Blackwell, Oxford, pp 424–426Google Scholar
  4. Alves JD, Souza AP, Pôrto ML, Fontes RL, Arruda J, Marques LFH (2016) Potential of sunflower, castor bean, common buckwheat and vetiver as lead phytoaccumulators. Rev Bras Eng Agric Amb 20(3):243–249Google Scholar
  5. Ammann AA (2007) Inductively coupled plasma mass spectrometry (ICP MS): a versatile tool. J Mass Spectrom 42(4):419–427Google Scholar
  6. Andra SS, Datta R, Sarkar D, Makris KC, Mullens CP, Sahi SV, Bach SB (2010) Synthesis of phytochelatins in vetiver grass upon lead exposure in the presence of phosphorus. Plant Soil 326(1–2):171–185Google Scholar
  7. Anuradha S, Rao R, Eeta S (2011) Amelioration of lead toxicity in radish (Raphanus sativus L) plants by brassinolide. J Appl Biol Sci 5(3):43–48Google Scholar
  8. Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J 20(2):171–182Google Scholar
  9. Arias JA, Peralta-Videa JR, Ellzey JT, Ren M, Viveros MN, Gardea-Torresdey JL (2010) Effects of Glomus deserticola inoculation on Prosopis: enhancing chromium and lead uptake and translocation as confirmed by X-ray mapping, ICP-OES and TEM techniques. Environ Exp Bot 68(2):139–148Google Scholar
  10. Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid M, Guiresse M, Pradère P, Dumat C (2008) A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 71(11):2187–2192Google Scholar
  11. Arshad T, Maqbool N, Javed F, Arshad MU (2017) Enhancing the defensive mechanism of lead affected barley (Hordeum vulgare L.) genotypes by exogenously applied salicylic acid. J Agric Sci 9(2):139–146Google Scholar
  12. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27(1):84–93Google Scholar
  13. Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216Google Scholar
  14. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2):163–190Google Scholar
  15. Ashraf U, Kanu AS, Deng Q, Mo Z, Pan S, Tian H, Tang X (2017) Lead (Pb) toxicity; physio-biochemical mechanisms, grain yield, quality, and pb distribution proportions in scented rice. Front Plant Sci 8:259Google Scholar
  16. Atici Ö, Ağar G, Battal P (2005) Changes in phytohormone contents in chickpea seeds germinating under lead or zinc stress. Biol Plant 49(2):215–222Google Scholar
  17. Azhar NAZILA, Ashraf MY, Hussain M, Hussain F (2006) Phytoextraction of lead (Pb) by EDTA application through sunflower (Helianthus annuus L.) cultivation: seedling growth studies. Pak J Bot 38(5):1551–1560Google Scholar
  18. Barceló J, Poschenrieder C (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13(1):1–37Google Scholar
  19. Barrutia O, Garbisu C, Hernández-Allica J, García-Plazaola JI, Becerril JM (2010) Differences in EDTA-assisted metal phytoextraction between metallicolous and non-metallicolous accessions of Rumex acetosa L. Environ Pollut 158(5):1710–1715Google Scholar
  20. Bharwana SA, Ali S, Farooq MA, Iqbal N, Abbas F, Ahmad MSA (2013) Alleviation of lead toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake and oxidative stress in cotton. J Bioremed Biodegr 4(4):4153–4172Google Scholar
  21. Bharwana SA, Ali S, Farooq MA, Iqbal N, Hameed A, Abbas F, Ahmad MSA (2014) Glycine betaine-induced lead toxicity tolerance related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake and oxidative stress in cotton. Turk J Bot 38(2):281–292Google Scholar
  22. Bharwana SA, Shafaqat A, Farooq MA, Mujahid F, Nusrat B, Rehan A (2016) Physiological and biochemical changes induced by lead stress in cotton (Gossypium hirsutum L.) seedlings. Acad J Agric Res 4(4):160–167Google Scholar
  23. Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transducation in plants. Curr Sci 89:1113–1121Google Scholar
  24. Bhatti KH, Anwar S, Nawaz K, Hussain K (2013) Effect of heavy metal lead (Pb) stress of different concentration on wheat (Triticum aestivum L.). Middle-East J Sci Res 14(2):148–154Google Scholar
  25. Bhushan B, Gupta K (2008) Effect of lead on carbohydrate mobilization in oat seeds during germination. J Appl Sci Environ Manag 12(2):29–33Google Scholar
  26. Bi X, Ren L, Gong M, He Y, Wang L, Ma Z (2010) Transfer of cadmium and lead from soil to mangoes in an uncontaminated area, Hainan Island, China. Geoderma 155(1):115–120Google Scholar
  27. Blaylock MJ (2000) Field demonstrations of phytoremediation of lead-contaminated soils. In: Phytoremediation of contaminated soil and water. Lewis, Boca RatonGoogle Scholar
  28. Bressler JP, Olivi L, Cheong JH, Kim Y, Bannona D (2004) Divalent metal transporter 1 in lead and cadmium transport. Ann N Y Acad Sci 1012(1):142–152Google Scholar
  29. Brunet J, Varrault G, Zuily-Fodil Y, Repellin A (2009) Accumulation of lead in the roots of grass pea (Lathyrus sativus L.) plants triggers systemic variation in gene expression in the shoots. Chemosphere 77(8):1113–1120Google Scholar
  30. Carter KP, Young AM, Palmer AE (2014) Fluorescent sensors for measuring metal ions in living systems. Chem Rev 114(8):4564–4601Google Scholar
  31. Chatterjee C, Dube BK, Sinha P, Srivastava P (2004) Detrimental effects of lead phytotoxicity on growth, yield, and metabolism of rice. Commun Soil Sci Plant Anal 35(1–2):255–265Google Scholar
  32. 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(2):253–264Google Scholar
  33. Chereddy NR, Nagaraju P, Raju MN, Krishnaswamy VR, Korrapati PS, Bangal PR, Rao VJ (2015) A novel FRET ‘off–on’ fluorescent probe for the selective detection of Fe3+, Al3+ and Cr3+ ions: its ultrafast energy transfer kinetics and application in live cell imaging. Biosens Bioelectron 68:749–756Google Scholar
  34. Cho HJ, Myung SW (2011) Determination of cadmium, chromium and lead in polymers by icp-oes using a high pressure asher (hpa). Bull Kor Chem Soc 32(2):489–497Google Scholar
  35. Choudhary SP, Bhardwaj R, Gupta BD, Dutt P, Gupta RK, Kanwar M, Dutt P (2010) Changes induced by Cu2+ and Cr6+ metal stress in polyamines, auxins, abscisic acid titers and antioxidative enzymes activities of radish seedlings. Braz J Plant Physiol 22(4):263–270Google Scholar
  36. Choudhary SP, Kanwar M, Bhardwaj R, Gupta BD, Gupta RK (2011) Epibrassinolide ameliorates Cr (VI) stress via influencing the levels of indole-3-acetic acid, abscisic acid, polyamines and antioxidant system of radish seedlings. Chemosphere 84(5):592–600Google Scholar
  37. Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23(4):1219–1230Google Scholar
  38. Coco J, Bechlin MA, Barros AI, Ferreira EC, Veiga MA, Neto JA (2017) Development of analytical procedures for lead determination in incense by graphite furnace AAS. Atomic Spectrosc 1:208–212Google Scholar
  39. Cotter-Howells J, Thornton I (1991) Sources and pathways of environmental lead to children in a Derbyshire mining village. Environ Geochem Health 13(2):127–135Google Scholar
  40. Dai J, Mumper RJ (2010) Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15(10):7313–7352Google Scholar
  41. Decker A (1997) Phenolics: prooxidants or antioxidants? Nutr Rev 55(11):396–398Google Scholar
  42. Devi PB, Vijayabharathi R, Sathyabama S, Malleshi NG, Priyadarisini VB (2014) Health benefits of finger millet (Eleusine coracana L.) polyphenols and dietary fiber: a review. J Food Sci Technol 51(6):1021–1040Google Scholar
  43. Dey SK, Dey J, Patra S, Pothal D (2007) Changes in the antioxidative enzyme activities and lipid peroxidation in wheat seedlings exposed to cadmium and lead stress. Braz J Plant Physiol 19(1):53–60Google Scholar
  44. Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7(7):1085Google Scholar
  45. Dogan M, Karatas M, Aasim M (2018) Cadmium and lead bioaccumulation potentials of an aquatic macrophyte Ceratophyllum demersum L.: a laboratory study. Ecotoxicol Environ Saf 148:431–440Google Scholar
  46. Ducos S, Hamester M, Godula M (2010) ICP-MS for detecting heavy metals in foodstuffs: the technology can analyze 50 samples in an hour. Food Quality Safety Magazine, Hoboken, USAGoogle Scholar
  47. Dumat C, Quenea K, Bermond A, Toinen S, Benedetti MF (2006) Study of the trace metal ion influence on the turnover of soil organic matter in cultivated contaminated soils. Environ Pollut 142(3):521–529Google Scholar
  48. Đurđević B, Lisjak M, Stošić M, Engler M, Popović B (2008) Influence of Pb and Cu toxicity on lettuce photosynthetic pigments and dry matter accumulation. Cereal Res Commun 36:1951–1954Google Scholar
  49. Ederli L, Reale L, Ferranti F, Pasqualini S (2004) Responses induced by high concentration of cadmium in Phragmites australis roots. Physiol Plant 121(1):66–74Google Scholar
  50. EPA (2001) Lead safe yards: developing and implementing a monitoring, assessment, and outreach program for your community. U.S. EPA Office of Research and Development, EPA/625/R-00/012Google Scholar
  51. EPA (2017) United States Environmental Protection Agency: justification of appropriation estimates for the committee on appropriations. U.S. EPA Office of Research and Development, EPA/190/K-17/002Google Scholar
  52. Fargasova A (2004) Toxicity comparison of some possible toxic metals (Cd, Cu, Pb, Se, Zn) on young seedlings of Sinapis alba L. Plant Soil Environ 50(1):33–38Google Scholar
  53. Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z (2013) Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol Environ Saf 96:242–249Google Scholar
  54. Farooqi ZR, Iqbal MZ, Kabir M, Shafiq M (2009) Toxic effects of lead and cadmium on germination and seedling growth of Albizia lebbeck (L.) Benth. Pak J Bot 41(1):27–33Google Scholar
  55. Flora SJS, Flora GJS, Saxena G (2006) Environmental occurrence, health effects and management of lead poisoning. In: Cascas SB, Sordo J (eds) Lead: chemistry, analytical aspects, environmental impacts and health effects. Elsevier, Amsterdam, pp 158–228Google Scholar
  56. Gao W, Nan T, Tan G, Zhao H, Tan W, Meng F, Li Z, Li QX, Wang B (2015) Cellular and subcellular immunohistochemical localization and quantification of cadmium ions in wheat (Triticum aestivum). PLoS One 10(5):e0123779Google Scholar
  57. 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.) Mill sp. J Plant Growth Regul 30(3):286–300Google Scholar
  58. Ghani A (2010) Toxic effects of heavy metals on plant growth and metal accumulation in maize (Zea mays L.). Iran J Toxicol 4(3):325–334Google Scholar
  59. Ghani A, Khan I, Ahmed I, Mustafa I, Abd-Ur R, Muhammad N (2015) Amelioration of lead toxicity in Pisum sativum (L.) by foliar application of salicylic acid. J Environ Anal Toxicol 5:292Google Scholar
  60. Gichner T, Žnidar I, Száková J (2008) Evaluation of DNA damage and mutagenicity induced by lead in tobacco plants. Mutat Res 652(2):186–190Google Scholar
  61. Godbold DL, Kettner C (1991) Lead influences root growth and mineral nutrition of Picea abies seedlings. J Plant Physiol 139(1):95–99Google Scholar
  62. Godzik A (1996) The structural alignment between two proteins: is there a unique answer? Protein Sci 5(7):1325–1338Google Scholar
  63. Gopal R, Rizvi AH (2008) Excess lead alters growth, metabolism and translocation of certain nutrients in radish. Chemosphere 70(9):1539–1544Google Scholar
  64. Grill E, Löffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci 86(18):6838–6842Google Scholar
  65. Grover P, Rekhadevi PV, Danadevi K, Vuyyuri SB, Mahboob M, Rahman MF (2010) Genotoxicity evaluation in workers occupationally exposed to lead. Int J Hyg Environ Health 213(2):99–106Google Scholar
  66. Gupta DK, Srivastava A, Singh VP (2006) Phytoremediation of induced lead toxicity in Vigna mungo (L.) hepper by vetiver grass. Rohilkhand University, BareillyGoogle Scholar
  67. Gupta DK, Nicoloso FT, Schetinger MRC, Rossato LV, Pereira LB, Castro GY, Srivastava S, Tripathi RD (2009) Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater 172(1):479–484Google Scholar
  68. Gupta DK, Huang HG, Yang XE, Razafindrabe BHN, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater 177(1):437–444Google Scholar
  69. Gurer H, Ercal N (2000) Can antioxidants be beneficial in the treatment of lead poisoning? Free Radic Biol Med 29(10):927–945Google Scholar
  70. Harpaz-Saad S, Azoulay T, Arazi T, Ben-Yaakov E, Mett A, Shiboleth YM, Hörtensteiner S, Gidoni D, Gal-On A, Goldschmidt EE, Eyal Y (2007) Chlorophyllase is a rate-limiting enzyme in chlorophyll catabolism and is posttranslationally regulated. Plant Cell 19(3):1007–1022Google Scholar
  71. Hassan M, Mansoor S (2014) Oxidative stress and antioxidant defense mechanism in mung bean seedlings after lead and cadmium treatments. Turk J Agric For 38(1):55–61Google Scholar
  72. Hattab S, Hattab S, Flores-Casseres ML, Boussetta H, Doumas P, Hernandez LE, Banni M (2016) Characterisation of lead-induced stress molecular biomarkers in Medicago sativa plants. Environ Exp Bot 123:1–12Google Scholar
  73. He Q, Miller EW, Wong AP, Chang CJ (2006) A selective fluorescent sensor for detecting lead in living cells. J Am Chem Soc 128(29):9316–9317Google Scholar
  74. Hettiarachchi GM, Pierzynski GM (2004) Soil lead bioavailability and in situ remediation of lead-contaminated soils: a review. Environ Prog 23(1):78–93Google Scholar
  75. Hossain Z, Hajika M, Komatsu S (2012) Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acids 43(6):2393–2416Google Scholar
  76. Huang JW, Cunningham SD (1996) Lead phytoextraction: species variation in lead uptake and translocation. New Phytol 134(1):75–84Google Scholar
  77. Hussain A, Abbas N, Arshad F, Akram M, Khan ZI, Ahmad K, Mansha M, Mirzaei F (2013) Effects of diverse doses of Lead (Pb) on different growth attributes of Zea mays L. Agric Sci 4(5):262Google Scholar
  78. Islam E, Yang X, Li T, Liu D, Jin X, Meng F (2007) Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 147(3):806–816Google Scholar
  79. Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 154(1):914–926Google Scholar
  80. Jarvis MD, Leung DWM (2002) Chelated lead transport in Pinus radiata: an ultrastructural study. Environ Exp Bot 48(1):21–32Google Scholar
  81. Jayasri MA, Suthindhiran K (2017) Effect of zinc and lead on the physiological and biochemical properties of aquatic plant Lemna minor: its potential role in phytoremediation. Appl Water Sci 7(3):1247–1253Google Scholar
  82. Jiang W, Liu D (2010) Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biol 10(1):40Google Scholar
  83. Jiang N, Luo X, Zeng J, Yang Z, Zheng L, Wang S (2010) Lead toxicity induced growth and antioxidant responses in Luffa cylindrica seedlings. Int J Agric Biol 12(2):205–210Google Scholar
  84. Jiang Z, Qin R, Zhang H, Zou J, Shi Q, Wang J, Jiang W, Liu D (2014) Determination of Pb genotoxic effects in Allium cepa root cells by fluorescent probe, microtubular immunofluorescence and comet assay. Plant Soil 383(1–2):357–372Google Scholar
  85. Jing CHEN, Cheng ZHU, Li LP, Sun ZY, Pan XB (2007) Effects of exogenous salicylic acid on growth and H2O2-metabolizing enzymes in rice seedlings under lead stress. J Environ Sci 19(1):44–49Google Scholar
  86. John R, Ahmad P, Gadgil K, Sharma S (2012) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Prod 3(3):65–76Google Scholar
  87. Kabata-Pendias A (1993) Behavioural properties of trace metals in soils. Appl Geochem 8:3–9Google Scholar
  88. Kafel A, Nadgórska-Socha A, Gospodarek J, Babczyńska A, Skowronek M, Kandziora M, Rozpędek K (2010) The effects of Aphis fabae infestation on the antioxidant response and heavy metal content in field grown Philadelphus coronarius plants. Sci Total Environ 408(5):1111–1119Google Scholar
  89. Kanwar MK, Bhardwaj R (2015) Arsenic induced modulation of antioxidative defense system and brassinosteroids in Brassica juncea L. Ecotoxicol Environ Saf 115:119–125Google Scholar
  90. Karak D, Banerjee A, Lohar S, Sahana A, Mukhopadhyay SK, Adhikari SS, Das D (2013) Xanthone based Pb2+ selective turn on fluorescent probe for living cell staining. Anal Methods 5(1):169–172Google Scholar
  91. Kaur L, Gadgil K, Sharma S (2013) Comparative study of natural phyto-extraction and induced phyto-extraction of lead using mustard plant (Brassica juncea arawali). Int J Bioassays 2(1):352–357Google Scholar
  92. Khan AL, Waqas M, Hussain J, Al-Harrasi A, Hamayun M, Lee IJ (2015) Phytohormones enabled endophytic fungal symbiosis improve aluminum phytoextraction in tolerant Solanum lycopersicum: an examples of Penicillium janthinellum LK5 and comparison with exogenous GA 3. J Hazard Mater 295:70–78Google Scholar
  93. Khan M, Daud MK, Basharat A, Khan MJ, Azizullah A, Muhammad N, Muhammad N, ur Rehman Z, Zhu SJ (2016) Alleviation of lead-induced physiological, metabolic, and ultramorphological changes in leaves of upland cotton through glutathione. Environ Sci Pollut Res 23(9):8431–8440Google Scholar
  94. Kim DY, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140(3):922–932Google Scholar
  95. Kohli SK, Handa N, Sharma A, Kumar V, Kaur P, Bhardwaj R (2017) Synergistic effect of 24-epibrassinolide and salicylic acid on photosynthetic efficiency and gene expression in Brassica juncea L. under Pb stress. Turk J Biol 41(6):943–953Google Scholar
  96. Kohli SK, Handa N, Bali S, Arora S, Sharma A, Kaur R, Bhardwaj R (2018a) Modulation of antioxidative defense expression and osmolyte content by co-application of 24-epibrassinolide and salicylic acid in Pb exposed Indian mustard plants. Ecotoxicol Environ Saf 147:382–393Google Scholar
  97. Kohli SK, Handa N, Sharma A, Gautam V, Arora S, Bhardwaj R, Wijaya L, Alyemeni MN, Ahmad P (2018b) Interaction of 24-epibrassinolide and salicylic acid regulates pigment contents, antioxidative defense responses, and gene expression in Brassica juncea L. seedlings under Pb stress. Environ Sci Pollut Res 25(15):15159–15173Google Scholar
  98. Kopittke PM, Asher CJ, Kopittke RA, Menzies NW (2007) Toxic effects of Pb 2+ on growth of cowpea (Vigna unguiculata). Environ Pollut 150(2):280–287Google Scholar
  99. Kos B, Greman H, Lestan D (2003) Phytoextraction of lead, zinc and cadmium from soil by selected plants. Plant Soil Environ 49(12):548–553Google Scholar
  100. 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(1):35–51Google Scholar
  101. Krzesłowska M, Lenartowska M, Mellerowicz EJ, Samardakiewicz S, Woźny A (2009) Pectinous cell wall thickenings formation—a response of moss protonemata cells to lead. Environ Exp Bot 65(1):119–131Google Scholar
  102. Krzesłowska M, Lenartowska M, Samardakiewicz S, Bilski H, Woźny A (2010) Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable–a remobilization can occur. Environ Pollut 158(1):325–338Google Scholar
  103. Kumar M, Jayaraman P (2014) Toxic effect of lead nitrate [Pb(NO3)2] on the black gram seedlings (Vigna mungo L. Hepper). Int J Adv Res Biol Sci 1(9):209–213Google Scholar
  104. Kumar A, Pal L, Agrawal V (2017) Glutathione and citric acid modulates lead-and arsenic-induced phytotoxicity and genotoxicity responses in two cultivars of Solanum lycopersicum L. Acta Physiol Plant 39(7):151Google Scholar
  105. Lamhamdi M, Bakrim A, Aarab A, Lafont R, Sayah F (2010) A comparison of lead toxicity using physiological and enzymatic parameters on spinach (Spinacia oleracea) and wheat (Triticum aestivum) growth. Moroccan J Biol 6(7):64–73Google Scholar
  106. Lamhamdi M, El Galiou O, Bakrim A, Nóvoa-Muñoz JC, Arias-Estévez M, Aarab A, Lafont R (2013) Effect of lead stress on mineral content and growth of wheat (Triticum aestivum) and spinach (Spinacia oleracea) seedlings. Saudi J Biol Sci 20(1):29–36Google Scholar
  107. Lane SD, Martin ES (1977) A histochemical investigation of lead uptake in Raphanus sativus. New Phytol 79(2):281–286Google Scholar
  108. Lavid N, Schwartz A, Yarden O, Tel-Or E (2001) The involvement of polyphenols and peroxidase activities in heavy-metal accumulation by epidermal glands of the waterlily (Nymphaeaceae). Planta 212(3):323–331Google Scholar
  109. Lawal OS, Sanni AR, Ajayi IA, Rabiu OO (2010) Equilibrium, thermodynamic and kinetic studies for the biosorption of aqueous lead (II) ions onto the seed husk of Calophyllum inophyllum. J Hazard Mater 177(1):829–835Google Scholar
  110. Leal-Alvarado DA, Espadas-Gil F, Sáenz-Carbonell L, Talavera-May C, Santamaría JM (2016) Lead accumulation reduces photosynthesis in the lead hyper-accumulator Salvinia minima Baker by affecting the cell membrane and inducing stomatal closure. Aquat Toxicol 171:37–47Google Scholar
  111. Lewis A (2010) Determination of lead levels in soil and plant uptake studies. Rev J Undergrad Stud Res 12(1):48–56Google Scholar
  112. Li HY, Wei DQ, Shen M, Zhou ZP (2012) Endophytes and their role in phytoremediation. Fungal Divers 54(1):11–18Google Scholar
  113. Li Y, Zhou C, Huang M, Luo J, Hou X, Wu P, Ma X (2016) Lead tolerance mechanism in Conyza canadensis: subcellular distribution, ultrastructure, antioxidative defense system, and phytochelatins. J Plant Res 129(2):251–262Google Scholar
  114. Liao YC, Chien SC, Wang MC, Shen Y, Hung PL, Das B (2006) Effect of transpiration on Pb uptake by lettuce and on water soluble low molecular weight organic acids in rhizosphere. Chemosphere 65(2):343–351Google Scholar
  115. Lindsay WL (1979) Chemical equilibria in soils. Wiley, New YorkGoogle Scholar
  116. Liu D, Li TQ, Jin XF, Yang XE, Islam E, Mahmood Q (2008) Lead induced changes in the growth and antioxidant metabolism of the lead accumulating and non-accumulating ecotypes of Sedum alfredii. J Integr Plant Biol 50(2):129–140Google Scholar
  117. Liu X, Peng K, Wang A, Lian C, Shen Z (2010) Cadmium accumulation and distribution in populations of Phytolacca americana L. and the role of transpiration. Chemosphere 78(9):1136–1141Google Scholar
  118. Lokhande VH, Suprasanna P (2012) Prospects of halophytes in understanding and managing abiotic stress tolerance. In: Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 29–56Google Scholar
  119. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68(1):1–13Google Scholar
  120. Malar S, Vikram SS, Favas PJ, Perumal V (2014) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud 55(1):54Google Scholar
  121. Małecka A, Piechalak A, Morkunas I, Tomaszewska B (2008) Accumulation of lead in root cells of Pisum sativum. Acta Physiol Plant 30(5):629–637Google Scholar
  122. Malone C, Koeppe DE, Miller RJ (1974) Localization of lead accumulated by corn plants. Plant Physiol 53(3):388–394Google Scholar
  123. Manara A (2012) Plant responses to heavy metal toxicity. In: Plants and heavy metals. Springer, Dordrecht, pp 27–53Google Scholar
  124. Manginsay-Enot M, Sillero-Mahinay M (2017) A study of potential lead metal hyperaccumulator in tissue cultured plants of Tradescantia spathacea Sw. and Chlorophytum orchidastrum grown in hydroponics. Bull Environ Pharmacol Life Sci 6:45–50Google Scholar
  125. Maodzeka A, Hussain N, Wei L, Zvobgo G, Mapodzeke JM, Adil MF, Jabeen S, Wang F, Jiang L, Shamsi IH (2017) Elucidating the physiological and biochemical responses of different tobacco (Nicotiana tabacum) genotypes to lead toxicity. Environ Toxicol Chem 36(1):175–181Google Scholar
  126. McComb J, Hentz S, Miller GS, Begonia M (2012) Effects of lead on plant growth, lead accumulation and phytochelatin contents of hydroponically-grown Sesbania exaltata. World Environ 2(3):38–43Google Scholar
  127. Meyers DE, Auchterlonie GJ, Webb RI, Wood B (2008) Uptake and localisation of lead in the root system of Brassica juncea. Environ Pollut 153(2):323–332Google Scholar
  128. Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15(4):523–530Google Scholar
  129. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133(3):481–489Google Scholar
  130. 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(6):1027–1039Google Scholar
  131. Mishra S, Tripathi RD, Srivastava S, Dwivedi S, Trivedi PK, Dhankher OP, Khare A (2009) Thiol metabolism play significant role during cadmium detoxification by Ceratophyllum demersum L. Bioresour Technol 100(7):2155–2161Google Scholar
  132. Misra N, Saxena P (2009) Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci 177(3):181–189Google Scholar
  133. Mohan BS, Hosetti BB (1997) Potential phytotoxicity of lead and cadmium to Lemna minor grown in sewage stabilization ponds. Environ Pollut 98(2):233–238Google Scholar
  134. 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(1–2):267–276Google Scholar
  135. Moore KL, Lombi E, Zhao FJ, Grovenor CR (2012) Elemental imaging at the nanoscale: NanoSIMS and complementary techniques for element localisation in plants. Anal Bioanal Chem 402(10):3263–3273Google Scholar
  136. Mosavian SN, Chaab A (2012) Response of morphologic and physiologic two variety canola to stress concentration of lead. Adv Environ Biol 6:1503–1509Google Scholar
  137. Mudgal V, Madaan N, Mudgal A, Singh R, Mishra S (2010) Effect of toxic metals on human health. Open Nutraceuticals J 3:94–99Google Scholar
  138. Munzuroglu O, Geckil H (2002) Effects of metals on seed germination, root elongation, and coleoptile and hypocotyl growth in Triticum aestivum and Cucumis sativus. Arch Environ Contam Toxicol 43(2):203–213Google Scholar
  139. Muszyńska E, Kałużny K, Hanus-Fajerska E (2014) Phenolic compounds in Hippophaë rhamnoides leaves collected from heavy metals contaminated sites.[W:] Plants in urban areas and landscape. Slovak University of Agriculture in Nitra, Faculty of Horticulture and Landscape Engineering, Nitra, pp 11–14Google Scholar
  140. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216Google Scholar
  141. Nareshkumar A, Veeranagamallaiah G, Pandurangaiah M, Kiranmai K, Amaranathareddy V, Lokesh U, Venkatesh B, Sudhakar C (2015) Pb-stress induced oxidative stress caused alterations in antioxidant efficacy in two groundnut (Arachis hypogaea L.) cultivars. Agric Sci 6(10):1283Google Scholar
  142. Ojwang LO, Banerjee N, Noratto GD, Angel-Morales G, Hachibamba T, Awika JM, Mertens-Talcott SU (2015) Polyphenolic extracts from cowpea (Vigna unguiculata) protect colonic myofibroblasts (CCD18Co cells) from lipopolysaccharide (LPS)-induced inflammation–modulation of microRNA 126. Food Funct 6(1):145–153Google Scholar
  143. Olivares E (2003) The effect of lead on the phytochemistry of Tithonia diversifolia exposed to roadside automotive pollution or grown in pots of Pb-supplemented soil. Braz J Plant Physiol 15(3):149–158Google Scholar
  144. Padmavathiamma PK, Li LY (2010) Phytoavailability and fractionation of lead and manganese in a contaminated soil after application of three amendments. Bioresour Technol 101(14):5667–5676Google Scholar
  145. Pais I, Jones JB Jr (1997) The handbook of trace elements. CRC Press, Boca RatonGoogle Scholar
  146. Pan J, Lin S, Woodbury NW (2012) Bacteriochlorophyll excited-state quenching pathways in bacterial reaction centers with the primary donor oxidized. J Phys Chem B 116(6):2014–2022Google Scholar
  147. Parys E, Romanowska E, Siedlecka M, Poskuta JW (1998) The effect of lead on photosynthesis and respiration in detached leaves and in mesophyll protoplasts of Pisum sativum. Acta Physiol Plant 20(3):313–322Google Scholar
  148. Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52(3):199–223Google Scholar
  149. Piechalak A, Tomaszewska B, Baralkiewicz D, Malecka A (2002) Accumulation and detoxification of lead ions in legumes. Phytochemistry 60(2):153–162Google Scholar
  150. Pinho S, Ladeiro B (2012) Phytotoxicity by lead as heavy metal focus on oxidative stress. J Bot 20:1–10Google Scholar
  151. Piotrowska A, Bajguz A, Godlewska-Żyłkiewicz B, Czerpak R, Kamińska M (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot 66(3):507–513Google Scholar
  152. Pourrut B, Perchet G, Silvestre J, Cecchi M, Guiresse M, Pinelli E (2008) Potential role of NADPH-oxidase in early steps of lead-induced oxidative burst in Vicia faba roots. J Plant Physiol 165(6):571–579Google Scholar
  153. Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. In: Reviews of environmental contamination and toxicology. Springer, New York, pp 113–136Google Scholar
  154. Pratima M, Pratima H (2016) Copper toxicity causes oxidative stress in Brassica juncea L. seedlings. Indian J Plant Physiol 14(4):397–401Google Scholar
  155. Punamiya P, Datta R, Sarkar D, Barber S, Patel M, Das P (2010) Symbiotic role of Glomus mosseae in phytoextraction of lead in vetiver grass [Chrysopogon zizanioides (L.)]. J Hazard Mater 177(1):465–474Google Scholar
  156. Qian JIN, Shan XQ, Wang ZJ, Tu Q (2016) Distribution and plant availability of heavy metals in different particle-size fractions of soil. Sci Total Environ 187(2):131–141Google Scholar
  157. Qufei L, Fashui H (2009) Effects of Pb2+ on the structure and function of photosystem II of Spirodela polyrrhiza. Biol Trace Elem Res 129(1–3):251Google Scholar
  158. Quinn CF, Prins CN, Freeman JL, Gross AM, Hantzis LJ, Reynolds RJ, Covey PA, Bañuelos GS, Pickering IJ, Fakra SC, Marcus MA (2011) Selenium accumulation in flowers and its effects on pollination. New Phytol 192(3):727–737Google Scholar
  159. Qureshi MI, Abdin MZ, Qadir S, Iqbal M (2007) Lead-induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. Biol Plant 51(1):121–128Google Scholar
  160. Rao SSR, Raghu K (2016) Amelioration of lead toxicity by 24-epibrassinolide in rose-scented geranium [Pelargonium graveolens (L.) Herit], a potential agent for phytoremediation. J Med Plants 4(6):06–08Google Scholar
  161. Reddy KE, Park KR, Lee SD, Yoo JH, Son AR, Lee HJ (2017) Effects of graded concentrations of supplemental lead on lead concentrations in tissues of pigs and prediction equations for estimating dietary lead intake. PeerJ 5:e3936Google Scholar
  162. Rêgo JF, Virgilio A, Nobrega JA, Neto JA (2012) Determination of lead in medicinal plants by high-resolution continuum source graphite furnace atomic absorption spectrometry using direct solid sampling. Talanta 100:21–26Google Scholar
  163. Rice-Evans C, Miller N, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2(4):152–159Google Scholar
  164. Romanowska E, Wróblewska B, Drozak A, Siedlecka M (2006) High light intensity protects photosynthetic apparatus of pea plants against exposure to lead. Plant Physiol Biochem 44(5):387–394Google Scholar
  165. Rossato LV, Nicoloso FT, Farias JG, Cargnelluti D, Tabaldi LA, Antes FG, Dressler VL, Morsch VM, Schetinger MRC (2012) Effects of lead on the growth, lead accumulation and physiological responses of Pluchea sagittalis. Ecotoxicology 21(1):111–123Google Scholar
  166. Sakihama Y, Yamasaki H (2002) Lipid peroxidation induced by phenolics in conjunction with aluminum ions. Biol Plant 45(2):249–254Google Scholar
  167. Saleem M, Asghar HN, Zahir ZA, Shahid M (2018) Impact of lead tolerant plant growth promoting rhizobacteria on growth, physiology, antioxidant activities, yield and lead content in sunflower in lead contaminated soil. Chemosphere 195:606–614Google Scholar
  168. Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52(364):2115–2126Google Scholar
  169. Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38(7):995–1014Google Scholar
  170. Šebestík J, Marques SM, Falé PL, Santos S, Arduíno DM, Cardoso SM, Oliveira CR, Serralheiro MLM, Santos MA (2011) Bifunctional phenolic-choline conjugates as anti-oxidants and acetylcholinesterase inhibitors. J Enzyme Inhib Med Chem 26(4):485–497Google Scholar
  171. Sengar AS, Thind KS, Kumar B, Pallavi M, Gosal SS (2009) In vitro selection at cellular level for red rot resistance in sugarcane (Saccharum sp.). Plant Growth Regul 58(2):201–209Google Scholar
  172. Seregin IV, Ivanov VB (2001) Physiological aspects of cadmium and lead toxic effects on higher plants. Russ J Plant Physiol 48(4):523–544Google Scholar
  173. Seregin IV, Shpigun LK, Ivanov VB (2004) Distribution and toxic effects of cadmium and lead on maize roots. Russ J Plant Physiol 51(4):525–533Google Scholar
  174. Serraj R, Sinclair TR (2002) Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant Cell Environ 25(2):333–341Google Scholar
  175. Shahid MA, Pervez MA, Balal RM, Mattson NS, Rashid A, Ahmad R, Ayyub CM, Abbas T (2011) Brassinosteroid (24-epibrassinolide) enhances growth and alleviates the deleterious effects induced by salt stress in pea (’Pisum sativum’ L.). Aust J Crop Sci 5(5):500Google Scholar
  176. 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(4):448–454Google Scholar
  177. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57(4):711–726Google Scholar
  178. Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17(1):35–52Google Scholar
  179. Sharma I, Pati PK, Bhardwaj R (2011) Effect of 28-homobrassinolide on antioxidant defence system in Raphanus sativus L. under chromium toxicity. Ecotoxicology 20(4):862–874Google Scholar
  180. Shu X, Yin L, Zhang Q, Wang W (2012) Effect of Pb toxicity on leaf growth, antioxidant enzyme activities, and photosynthesis in cuttings and seedlings of Jatropha curcas L. Environ Sci Pollut Res 19(3):893–902Google Scholar
  181. Sidhu GPS, Singh HP, Batish DR, Kohli RK (2016) Effect of lead on oxidative status, antioxidative response and metal accumulation in Coronopus didymus. Plant Physiol Biochem 105:290–296Google Scholar
  182. Sidhu GPS, Bali AS, Bhardwaj R, Singh HP, Batish DR, Kohli RK (2018) Bioaccumulation and physiological responses to lead (Pb) in Chenopodium murale L. Ecotoxicol Environ Saf 151:83–90Google Scholar
  183. Silva S, Pinto G, Santos C (2017) Low doses of Pb affected Lactuca sativa photosynthetic performance. Photosynthetica 55(1):50–57Google Scholar
  184. Singh R, Tripathi RD, Dwivedi S, Kumar A, Trivedi PK, Chakrabarty D (2010) Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol 101(9):3025–3032Google Scholar
  185. Sinha P, Dube BK, Srivastava P, Chatterjee C (2006) Alteration in uptake and translocation of essential nutrients in cabbage by excess lead. Chemosphere 65(4):651–656Google Scholar
  186. Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115(3):433–447Google Scholar
  187. Song WY, Yamaki T, Yamaji N, Ko D, Jung KH, Fujii-Kashino M, An G, Martinoia E, Lee Y, Ma JF (2014) A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc Natl Acad Sci 111(44):15699–15704Google Scholar
  188. Srivastava D, Singh A, Baunthiyal M (2015) Lead toxicity and tolerance in plants. J Plant Sci Res 2(2):123Google Scholar
  189. Stefanov K, Seizova K, Yanishlieva N, Marinova E, Popov S (1995) Accumulation of lead, zinc and cadmium in plant seeds growing in metalliferous habitats in Bulgaria. Food Chem 54(3):311–313Google Scholar
  190. Tabelin CB, Igarashi TO (2009) Mechanisms of arsenic and lead release from hydrothermally altered rock. J Hazard Mater 169(1):980–990Google Scholar
  191. Taiz L, Zeiger E (2010) Photosynthesis: the light reactions. Plant Physiol 5:163–198Google Scholar
  192. Tang C, Song J, Hu X, Hu X, Zhao Y, Li B, Ou D, Peng L (2017) Exogenous spermidine enhanced Pb tolerance in Salix matsudana by promoting Pb accumulation in roots and spermidine, nitric oxide, and antioxidant system levels in leaves. Ecol Eng 107:41–48Google Scholar
  193. Tangahu BV, Sheikh Abdullah SR, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 2011:31Google Scholar
  194. Teklić T, Hancock JT, Engler M, Paradicović N, Cesar V, Lepeduš H, Štolfa I, Bešlo D (2008) Antioxidative responses in radish (Raphanus sativus L.) plants stressed by copper and lead in nutrient solution and soil. Acta Biol Cracov 50(2):79–86Google Scholar
  195. Terryn C, Paës G, Spriet C (2018) FRET-SLiM on native autofluorescence: a fast and reliable method to study interactions between fluorescent probes and lignin in plant cell wall. Plant Methods 14(1):74Google Scholar
  196. Tripathi DK, Singh VP, Prasad SM, Dubey NK, Chauhan DK, Rai AK (2016) LIB spectroscopic and biochemical analysis to characterize lead toxicity alleviative nature of silicon in wheat (Triticum aestivum L.) seedlings. J Photochem Photobiol B Biol 154:89–98Google Scholar
  197. Uzu G, Sobanska S, Aliouane Y, Pradere P, Dumat C (2009) Study of lead phytoavailability for atmospheric industrial micronic and sub-micronic particles in relation with lead speciation. Environ Pollut 157(4):1178–1185Google Scholar
  198. Vatamaniuk OK, Bucher EA, Ward JT, Rea PA (2001) A new pathway for heavy metal detoxification in animals phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans. J Biol Chem 276(24):20817–20820Google Scholar
  199. Vega FA, Andrade ML, Covelo EF (2010) Influence of soil properties on the sorption and retention of cadmium, copper and lead, separately and together, by 20 soil horizons: comparison of linear regression and tree regression analyses. J Hazard Mater 174(1):522–533Google Scholar
  200. Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181(4):759–776Google Scholar
  201. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164(4):645–655Google Scholar
  202. Wang HH, Shan XQ, Wen B, Owens G, Fang J, Zhang SZ (2007) Effect of indole-3-acetic acid on lead accumulation in maize (Zea mays L.) seedlings and the relevant antioxidant response. Environ Exp Bot 61(3):246–253Google Scholar
  203. WHO (2001) Regional Office for Europe, air quality guidelines, chapter 6.7, Lead, Copenhagen, Denmark, 2nd edn. http://www.euro.who.int/document/aiq/67lead.pdf
  204. Wierzbicka M (1999) Comparison of lead tolerance in Allium cepa with other plant species. Environ Pollut 104(1):41–52Google Scholar
  205. Wierzbicka MH, Przedpełska E, Ruzik R, Ouerdane L, Połeć-Pawlak K, Jarosz M, Szpunar J, Szakiel A (2007) Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma 231(1):99–111Google Scholar
  206. Williams JC (1976) The segregation of particulate materials. A review. Powder Technol 15(2):245–251Google Scholar
  207. Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5(3):218–223Google Scholar
  208. Wiszniewska A, Muszyńska E, Hanus-Fajerska E, Smoleń S, Dziurka M, Dziurka K (2017) Organic amendments enhance Pb tolerance and accumulation during micropropagation of Daphne jasminea. Environ Sci Pollut Res 24(3):2421–2432Google Scholar
  209. Wojas S, Ruszczyńska A, Bulska E, Wojciechowski M, Antosiewicz DM (2007) Ca2+-dependent plant response to Pb 2+ is regulated by LCT1. Environ Pollut 147(3):584–592Google Scholar
  210. Wu SC, Luo YM, Cheung KC, Wong MH (2006) Influence of bacteria on Pb and Zn speciation, mobility and bioavailability in soil: a laboratory study. Environ Pollut 144(3):765–773Google Scholar
  211. Xiong ZT (1997) Bioaccumulation and physiological effects of excess lead in a roadside pioneer species Sonchus oleraceus L. Environ Pollut 97(3):275–279Google Scholar
  212. Xiong ZT, Wang H (2005) Copper toxicity and bioaccumulation in Chinese cabbage (Brassica pekinensis Rupr.). Environ Toxicol 20(2):188–194Google Scholar
  213. Xu B, Wang Y, Zhang S, Guo Q, Jin Y, Chen J, Gao Y, Ma H (2017) Transcriptomic and physiological analyses of Medicago sativa L. roots in response to lead stress. PLoS One 12(4):e0175307Google Scholar
  214. Yadav DV, Jain R, Rai RK (2010) Impact of heavy metals on sugar cane. In: Sherameti I, Varma A (eds) Soil heavy metals, Soil biology series. Springer, Berlin, pp 339–367Google Scholar
  215. Yan ZZ, Ke L, Tam NFY (2010) Lead stress in seedlings of Avicennia marina, a common mangrove species in South China, with and without cotyledons. Aquat Bot 92(2):112–118Google Scholar
  216. Yang YY, Jung JY, Song WY, Suh HS, Lee Y (2000) Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiol 124(3):1019–1026Google Scholar
  217. Zafari S, Sharifi M, Chashmi NA, Mur LA (2016) Modulation of Pb-induced stress in Prosopis shoots through an interconnected network of signaling molecules, phenolic compounds and amino acids. Plant Physiol Biochem 99:11–20Google Scholar
  218. Zaier H, Ghnaya T, Ghabriche R, Chmingui W, Lakhdar A, Lutts S, Abdelly C (2014) EDTA-enhanced phytoremediation of lead-contaminated soil by the halophyte Sesuvium portulacastrum. Environ Sci Pollut Res 21(12):7607–7615Google Scholar
  219. Zhao HJ, Ge ML, Yan Y, Zhang TJ, Zeng J, Zhou WY, Wang YF, Meng QH, Zhang CB (2018) Inductively coupled plasma mass spectrometry as a reference method to evaluate serum calcium measurement bias and the commutability of processed materials during routine measurements. Chin Med J 131(13):1584Google Scholar
  220. Zhong WS, Ren T, Zhao LJ (2016) Determination of Pb (Lead), Cd (Cadmium), Cr (Chromium), Cu (Copper), and Ni (Nickel) in Chinese tea with high-resolution continuum source graphite furnace atomic absorption spectrometry. J Food Drug Anal 24(1):46–55Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Sukhmeen Kaur Kohli
    • 1
    Email author
  • Neha Handa
    • 2
  • Shagun Bali
    • 1
  • Kanika Khanna
    • 1
  • Saroj Arora
    • 1
  • Anket Sharma
    • 3
  • Renu Bhardwaj
    • 1
    Email author
  1. 1.Department of Botanical and Environmental SciencesGuru Nanak Dev UniversityAmritsarIndia
  2. 2.Department of Botany, School of Bioengineering and BiosciencesLovely Professional UniversityPhagwaraIndia
  3. 3.State Key Laboratory of Subtropical SilvicultureZhejiang A&F UniversityHangzhouChina

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