Environmental Science and Pollution Research

, Volume 20, Issue 4, pp 2150–2161 | Cite as

Lead tolerance in plants: strategies for phytoremediation

Review Article

Abstract

Lead (Pb) is naturally occurring element whose distribution in the environment occurs because of its extensive use in paints, petrol, explosives, sludge, and industrial wastes. In plants, Pb uptake and translocation occurs, causing toxic effects resulting in decrease of biomass production. Commonly plants may prevent the toxic effect of heavy metals by induction of various celular mechanisms such as adsorption to the cell wall, compartmentation in vacuoles, enhancement of the active efflux, or induction of higher levels of metal chelates like a protein complex (metallothioneins and phytochelatins), organic (citrates), and inorganic (sulphides) complexes. Phyotochelains (PC) are synthesized from glutathione (GSH) and such synthesis is due to transpeptidation of γ-glutamyl cysteinyl dipeptides from GSH by the action of a constitutively present enzyme, PC synthase. Phytochelatin binds to Pb ions leading to sequestration of Pb ions in plants and thus serves as an important component of the detoxification mechanism in plants. At cellular level, Pb induces accumulation of reactive oxygen species (ROS), as a result of imbalanced ROS production and ROS scavenging processes by imposing oxidative stress. ROS include superoxide radical (O2.−), hydrogen peroxide (H2O2) and hydroxyl radical (·OH), which are necessary for the correct functioning of plants; however, in excess they caused damage to biomolecules, such as membrane lipids, proteins, and nucleic acids among others. To limit the detrimental impact of Pb, efficient strategies like phytoremediation are required. In this review, it will discuss recent advancement and potential application of plants for lead removal from the environment.

Keywords

Lead Detoxification Transport Phytoremediation 

References

  1. Abioye OP, Agamuthu P, Abdul AA (2012) Phytotreatment of soil contaminated with used lubricating oil using Hibiscus cannabinus. Biodegradation 23:277–286CrossRefGoogle Scholar
  2. Airaki M, Sánchez-Moreno L, Leterrier M, Barroso JB, Palma JM, Corpas FJ (2011) Detection and quantification of S-nitrosoglutathione (GSNO) in pepper (Capsicum annuum L.) plant organs by LC-ES/MS. Plant Cell Physiol 52:2006–2015CrossRefGoogle Scholar
  3. Andra SS, Datta R, Sarkar D, Makris KC, Mullens CP, Sahi SV, Bach SBH (2010) Synthesis of phytochelatins in vetiver grass upon lead exposure in the presence of phosphorus. Plant Soil 326:171–185CrossRefGoogle Scholar
  4. Antosiewicz DM (2005) Study of calcium-dependent lead-tolerance on plants differing in their level of Ca-deficiency tolerance. Environ Pollut 134:23–34CrossRefGoogle Scholar
  5. 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 20:171–182CrossRefGoogle Scholar
  6. Arias JA, Peralta-Videa JR, Ellzey JT, Ren MH, 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 68:139–148CrossRefGoogle Scholar
  7. Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid A, Guiresse M, Pradere P, Dumat C (2008) A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 71:2187–2192CrossRefGoogle Scholar
  8. Baranowska-Morek A, Wierzbicka M (2004) Localization of lead in root tip of Dianthus carthusianorum. Acta Biol Cracov Series Bot 46:45–56Google Scholar
  9. Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315CrossRefGoogle Scholar
  10. Bhuiyan MSU, Min SR, Jeong WJ, Sultana S, Choi KS, Lee Y, Liu JR (2011a) Overexpression of AtATM3 in Brassica juncea confers enhanced heavy metal tolerance and accumulation. Plant Cell Tiss Org 107:69–77CrossRefGoogle Scholar
  11. Bhuiyan MSU, Min SR, Jeong WJ, Sultana S, Choi KS, Song WY, Lee Y, Lim YP, Liu JR (2011b) Overexpression of a yeast cadmium factor 1 (YCF1) enhances heavy metal tolerance and accumulation in Brassica juncea. Plant Cell Tiss Org 105:85–91CrossRefGoogle Scholar
  12. 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 77:1113–1120CrossRefGoogle Scholar
  13. Cao SQ, Chen ZY, Liu GQ, Jiang L, Yuan HB, Ren G, Bian XH, Jian HY, Ma XL (2009) The Arabidopsis Ethylene-Insensitive 2 gene is required for lead resistance. Plant Physiol Biochem 47:308–312CrossRefGoogle Scholar
  14. Chen G, Sun GR, Liub AP, Zhou WD (2008) Lead enrichment in different genotypes of rice grains. Food Chem Toxicol 46:1152–1156CrossRefGoogle Scholar
  15. Chevns K, Peeters S, Delcourt D, Smolders E (2012) Lead phytotoxicity in soil and nutrient solutions is related to lead induced phosphorus deficiency. Environ Pollut 164:242–247CrossRefGoogle Scholar
  16. Clemens S (2006) Evolution and function of phytochelatin synthases. J Plant Physiology 163:319–332CrossRefGoogle Scholar
  17. Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604–611CrossRefGoogle Scholar
  18. Cotter-Howells JD, Champness PE, Charnock JM (1999) Mineralogy of Pb-P grains in the roots of Agrostis capillaris L-by ATEM and EXAFS. Mineral Mag 63:777–789CrossRefGoogle Scholar
  19. Couselo JL, Navarro-Avino J, Ballester A (2010) Expression of the phytochelatin synthase TaPCS1 in transgenic aspen, insight into the problems and qualities in phytoremediation of Pb. Int J Phytorem 12:358–370CrossRefGoogle Scholar
  20. de la Rosa G, Peralta-Videa JR, Cruz-Jimenez G, Duarte-Gardea M, Martinez-Martinez A, Cano-Aguilera I, Sharma NC, Sahi SV, Gardea-Torresdey JL (2007) Role of ethylenediaminetetraacetic acid on lead uptake and translocation by tumbleweed (Salsola kali L.). Environ Toxicol Chem 26:1033–1039CrossRefGoogle Scholar
  21. Deng Z, Cao L, Huang H, Jiang X, Wang W, Shi Y, Zhang R (2011) Characterization of Cd- and Pb-resistant fungal endophyte Mucor sp. CBRF59 isolated from rapes (Brassica chinensis) in a metal-contaminated soil. J Hazard Mater 185:717–724CrossRefGoogle Scholar
  22. Estrella-Gomez N, Mendoza-Cozatl D, Moreno-Sanchez R, Gonzalez-Mendoza D, Zapata-Perez O, Martinez-Hernandez A, Santamaria JM (2009) The Pb-hyperaccumulator aquatic fern Salvinia minima Baker, responds to Pb2+ by increasing phytochelatins via changes in SmPCS expression and in phytochelatin synthase activity. Aquatic Toxicol 91:320–328CrossRefGoogle Scholar
  23. Freitas EVD, do Nascimento CWA (2009) The use of NTA for lead phytoextraction from soil from a battery recycling site. J Hazard Mater 171:833–837CrossRefGoogle Scholar
  24. Ginn BR, Szymanowski JS, Fein JB (2008) Metal and proton binding onto the roots of Fescue rubra. Chem Geol 253:130–135CrossRefGoogle Scholar
  25. Gisbert C, Ros R, De Haro A, Walker DJ, Bernal MP, Serrano R, Navarro-Avino J (2003) A plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochem Biophy Res Comm 303:440–445CrossRefGoogle Scholar
  26. Guo H, Luo S, Chen L, Xiao X, Xi Q, Wei W, Zeng G, Liu C, Wan Y, Chen J, He Y (2010) Bioremediation of heavy metals by growing hyperaccumulaor endophytic bacterium Bacillus sp. L14. Biores Technol 101:8599–8605CrossRefGoogle Scholar
  27. Gupta DK, Nicoloso FT, Schetinger MRC, Rossato LV, Pereira LB, Castro GY, Srivastava S, Tripathi RD (2009) Antioxidant defence mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater 172:479–484CrossRefGoogle Scholar
  28. 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 177:437–444CrossRefGoogle Scholar
  29. Gupta DK, Nicoloso FT, Schetinger MRC, Rossato LV, Huang HG, Srivastava S, Yang XE (2011) Lead induced responses of Pfaffia glomerata, an economically important Brazilian medicinal plant, under in vitro culture conditions. Bull Environ Cont Toxicol 86:272–277CrossRefGoogle Scholar
  30. Gupta DK, Inouhe M, Rodríguez-Serrano M, Romero-Puerta MC, Sandalio LM (2013) Oxidative stress and arsenic toxicity: Role of NADPH oxidases. Chemosphere http://dx.doi.org/10.1016/j.chemosphere.2012.10.066 (In Press).
  31. Han YL, Huang SZ, Gu JG, Qiu S, Chen JM (2008) Tolerance and accumulation of lead by species of Iris L. Ecotoxicology 17:853–859CrossRefGoogle Scholar
  32. Hassan M, Sighicelli M, Lai A, Colao F, Ahmed AHH, Fantoni R, Harith MA (2008) Studying the enhanced phytoremediation of lead contaminated soils via laser induced breakdown spectroscopy. Spectroch Acta Part B 63:1225–1229CrossRefGoogle Scholar
  33. He B, Yang XE, Ni WZ, Wei YZ, Long XX, Ye ZQ (2002) Sedum alfredii: a new lead-accumulating ecotype. Acta Bot Sin 44:1365–1370Google Scholar
  34. He LY, Chen ZJ, Ren GD, Zhang YF, Qian M, Sheng XF (2009) Increased cadmium and lead uptake of a cadmium hyperaccumulator tomato by cadmium-resistant bacteria. Ecotoxicol Environ Saf 72:1343–1348CrossRefGoogle Scholar
  35. Huang HG, Li TX, Tian SK, Gupta DK, Zhang XZ, Yang XE (2008) Role of EDTA in alleviating lead toxicity in accumulator species of Sedum alfredii H. Biores Technol 99:6088–6096CrossRefGoogle Scholar
  36. Huang HG, Gupta DK, Tian SK, Yang XE, Li TX (2012) Lead tolerance and physiological adaptation mechanism in roots of accumulating and non-accumulating ecotypes of Sedum alfredii. Environ Sci Poll Res 19:1640–1651CrossRefGoogle Scholar
  37. Israr M, Sahi SV (2008) Promising role of plant hormones in translocation of lead in Sesbania drummondii shoots. Environ Pollut 153:29–36CrossRefGoogle Scholar
  38. Jabeen R, Ahmad A, Iqbal M (2009) Phytoremediation of heavy metals: Physiological and molecular mechanisms. Bot Rev 75:339–364CrossRefGoogle Scholar
  39. Jarup L (2003) Hazards of heavy metal contamination. Brit Med Bull 68:167–182CrossRefGoogle Scholar
  40. Jiang W, Liu D (2010) Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biol 10:40–40CrossRefGoogle Scholar
  41. Jiang CY, Sheng XF, Qian M, Wang QY (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164CrossRefGoogle Scholar
  42. Juwarkar AA, Singh SK, Mudhoo A (2010) A comprehensive overview of elements in bioremediation. Rev Environ Sci Biotech 9:215–288CrossRefGoogle Scholar
  43. Kim YY, Yang YY, Lee Y (2002) Pb and Cd uptake in rice roots. Physiol Planta 116:368–372CrossRefGoogle Scholar
  44. Kim DY, Bovet L, Kushnir S, Noh EU, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932CrossRefGoogle Scholar
  45. Kodera H, Nishioka H, Muramatsu Y, Terada Y (2008) Distribution of lead in lead-accumulating pteridophyte Blechnum niponicum, measured by synchrotron radiation micro X-ray fluorescence. Analyt Sci 24:1545–1549CrossRefGoogle Scholar
  46. Kohler C, Merkle T, Neuhaus G (1999) Characterization of a novel gene family of putative cyclic nucleotide and calmodulin-regulated ion channels in Arabidopsis thaliana. Plant J 18:97–104CrossRefGoogle Scholar
  47. Kopittke PM, Asher CJ, Blamey FP, Auchterlonie GJ, Guo YN, Menzies NW (2008) Localization and chemical speciation of Pb in roots of signal grass (Brachiaria decumbens) and Rhodes grass (Chloris gayana). Environ Sci Technol 42:4595–4599CrossRefGoogle Scholar
  48. Kopittke PM, Kinraide TB, Wang P, Blarney FPC, Reichman SM, Menzies NW (2011) Alleviation of Cu and Pb rhizotoxicities in Cowpea (Vigna unguiculata) as related to ion activities at root-cell plasma membrane surface. Environ Sci Technol 45:4966–4973CrossRefGoogle Scholar
  49. Kopyra M, Gwozdz EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017CrossRefGoogle Scholar
  50. Kotrba P, Najmanova J, Macek T, Ruml T, Mackova M (2009) Genetically modified plants in phytoremediation of heavy metal and metalloid soil and sediment pollution. Biotechnol Adv 27:799–810CrossRefGoogle Scholar
  51. Krzeslowska M, Lenartowska M, Mellerowicz EJ, Samardakiewicz S, Wozny A (2009) Pectinous cell wall thickenings formation–A response of moss protonemata cells to lead. Environ Exp Bot 65:119–131CrossRefGoogle Scholar
  52. Krzeslowska M, Lenartowska M, Samardakiewicz S, Bilski H, Wozny A (2010) Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable-A remobilization can occur. Environ Pollut 158:325–338CrossRefGoogle Scholar
  53. Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330CrossRefGoogle Scholar
  54. Lee M, Lee K, Lee J, Noh EW, Lee Y (2005) AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol 138:827–836CrossRefGoogle Scholar
  55. Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143CrossRefGoogle Scholar
  56. Lin CC, Liu J, Liu L, Zhu TC, Sheng LX, Wang DL (2009) Soil amendment application frequency contributes to phytoextraction of lead by sunflower at different nutrient levels. Environ Exp Bot 65:410–416CrossRefGoogle Scholar
  57. Liu D, Islam E, Li TQ, Yang X, Jin XF, Mahmood Q (2008) Comparison of synthetic chelators and low molecular weight organic acids in enhancing phytoextraction of heavy metals by two ecotypes of Sedum alfredii Hance. J Hazard Mater 153:114–122CrossRefGoogle Scholar
  58. Liu T, Liu S, Guan H, Ma L, Chen Z, Gu H (2009) Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead (Pb). Environ Exp Bot 67:377–386CrossRefGoogle Scholar
  59. Lombi E, Susini J (2009) Synchrotron-based techniques for plant and soil science: Opportunities, challenges and future perspectives. Plant Soil 320:1–35CrossRefGoogle Scholar
  60. Lopez ML, Peralta-Videa JR, Parsons JG, Benitez T, Gardea-Torresdey JL (2007) Gibberellic acid, kinetin, and the mixture indole-3-acetic acid-kinetin assisted with EDTA-induced lead hyperaccumulation in alfalfa plants. Environ Sci Technol 41:8165–8170CrossRefGoogle Scholar
  61. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Ann Rev Microbio 63:541–556CrossRefGoogle Scholar
  62. Lum HK, Butt YK, Lo SS (2002) Hydrogen peroxide induces a rapid production of nitric oxide in mung vean (Phaseolus aureus). Nitric Oxide 6:205–213CrossRefGoogle Scholar
  63. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13CrossRefGoogle Scholar
  64. Małecka A, Piechalak A, Morkunas I, Tomaszewska B (2008) Accumulation of lead in root cells of Pisum sativum. Acta Physiol Planta 30:629–637CrossRefGoogle Scholar
  65. McGrath SP, Zhao FJ, Lombi E (2002) Phytoremediation of metals, metalloids, and radionuclides. Adv Agron 75:1–56CrossRefGoogle Scholar
  66. Meers E, Tack FMG, Van Slycken S, Ruttens A, Laing GD, Vangronsveld J, Verloo MG (2008) Chemically assisted phytoextraction: a review of potential soil amendments for increasing plant uptake of heavy metals. Int J Phytorem 10:390–414CrossRefGoogle Scholar
  67. Meyers DER, Auchterlonie GJ, Webb RI, Wood B (2008) Uptake and localisation of lead in the root system of Brassica juncea. Environ Pollut 153:323–332CrossRefGoogle Scholar
  68. Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotech Adv 29:645–653CrossRefGoogle Scholar
  69. 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 65:1027–1039CrossRefGoogle Scholar
  70. Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P(1B)-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904CrossRefGoogle Scholar
  71. Newman LA, Reynolds CM (2005) Bacteria and phytoremediation: new uses for endophytic bacteria in plants. Trends Biotech 23:6–8, discussion 8–9CrossRefGoogle Scholar
  72. Phang IC, Leung DWM, Taylor HH, Burritt DJ (2010) Correlation of growth inhibition with accumulation of Pb in cell wall and changes in response to oxidative stress in Arabidopsis thaliana seedlings. Plant Growth Reg 64:17–25CrossRefGoogle Scholar
  73. Phang IC, Leung DW, 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. Ecotox Environ Saf 74:1310–1315CrossRefGoogle Scholar
  74. Pilon-Smits E (2005) Phytoremediation. Ann Rev Plant Biol 56:15–39CrossRefGoogle Scholar
  75. Polec-Pawlak K, Ruzik R, Lipiec E, Ciurzynska M, Gawronska H (2007) Investigation of Pb(II) binding to pectin in Arabidopsis thaliana. J Anal Atomic Spectrom 22:968–972CrossRefGoogle Scholar
  76. 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 165:571–579CrossRefGoogle Scholar
  77. Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxificaion in plants. Rev Environ Cont Toxicol 213:113–136CrossRefGoogle Scholar
  78. 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 177:465–474CrossRefGoogle Scholar
  79. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181CrossRefGoogle Scholar
  80. Rotkittikhun P, Kruatrachue M, Chaiyarat R, Ngernsansaruay C, Pokethitiyook P, Paijitprapaporn A, Baker AJM (2006) Uptake and accumulation of lead by plants from the Bo Ngam lead mine area in Thailand. Environ Pollut 144:681–688CrossRefGoogle Scholar
  81. Sahi SV, Bryant NL, Sharma NC, Singh SR (2002) Characterization of a lead hyperaccumulator shrub, Sesbania drummondii. Environ Sci Tech 36:4676–4680CrossRefGoogle Scholar
  82. Saifullah ME, Qadir M, de Caritat P, Tack FMG, Du Laing G, Zia MH (2009) EDTA-assisted Pb phytoextraction. Chemosphere 74:1279–1291CrossRefGoogle Scholar
  83. Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Ann Rev Plant Physiol Plant Mol Biol 49:643–668CrossRefGoogle Scholar
  84. Sarkar D, Andra SS, Saminathan SKM, Datta R (2008) Chelant-aided enhancement of lead mobilization in residential soils. Environ Pollut 156:1139–1148CrossRefGoogle Scholar
  85. Seregin IV, Shpigun LK, Ivanov VB (2004) Distribution and toxic effects of cadmium and lead on maize roots. Russ J Plant Physiol 51:525–533CrossRefGoogle Scholar
  86. Sheng XF, Jiang CY, He LY (2008a) Characterization of plant growth-promoting Bacillus edaphicus NBT and its effect on lead uptake by Indian mustard in a lead-amended soil. Canad J Microb 54:417–422CrossRefGoogle Scholar
  87. Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008b) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170CrossRefGoogle Scholar
  88. Shu WS, Xia HP, Zhang ZQ, Lan CY, Wong MH (2002) Use of vetiver and three other grasses for revegetation of Pb/Zn mine tailings: Field experiment. Int J Phytorem 4:47–57CrossRefGoogle Scholar
  89. Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455CrossRefGoogle Scholar
  90. Song WY, Sohn EJ, Martinoia E, Lee YJ, Yang YY, Jasinski M, Forestier C, Hwang I, Lee Y (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotech 21:914–919CrossRefGoogle Scholar
  91. Tamura H, Honda M, Sato T, Kamachi H (2005) Pb hyperaccumulation and tolerance in common buckwheat (Fagopyrum esculentum Moench). J Plant Res 118:355–359CrossRefGoogle Scholar
  92. Tang YT, Qiu RL, Zeng XW, Ying RR, Yu FM, Zhou XY (2009) Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ Exp Bot 66:126–134CrossRefGoogle Scholar
  93. Tanhan P, Pokethitiyook P, Kruatrachue M, Chaiyarat R, Upatham S (2011) Effects of soil amendments and EDTA on lead uptake by Chromolaena odorata: Greenhouse and field trial experiments. Int J Phytorem 13:897–911CrossRefGoogle Scholar
  94. Tian SK, Lu LL, Yang XE, Webb SM, Du YH, Brown PH (2010) Spatial imaging and speciation of lead in the accumulator plant Sedum alfredii by microscopically focused synchrotron X-ray investigation. Environ Sci Technol 44:5920–5926Google Scholar
  95. Tian SK, Lu LL, Yang XE, Huang HG, Brown P, Labavitch J, Liao HB, He ZL (2011) The impact of EDTA on lead distribution and speciation in the accumulator Sedum alfredii by synchrotron X-ray investigation. Environ Pollut 159:782–788CrossRefGoogle Scholar
  96. Tung G, Temple PJ (1996) Uptake and localization of lead in corn (Zea mays L.) seedlings: a study by histochemical and electron microscopy. Sci Total Environ 188:71–85CrossRefGoogle Scholar
  97. 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 157:1178–1185CrossRefGoogle Scholar
  98. Vogel-Mikus K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242CrossRefGoogle Scholar
  99. Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923CrossRefGoogle Scholar
  100. Wang H, Shan X, Wen B, Owens G, Fang J, Zhang S (2007) Effect of indole-3-acetic acid on lead accumulation in maize (Zea mays L.) seedlings and the relevant antioxidant response. Environ Exp Bot 61:246–253CrossRefGoogle Scholar
  101. Wang X, Wang Y, Mahmood Q, Islam E, Jin XF, Li TQ, Yang XE, Liu D (2009) The effect of EDDS addition on the phytoextraction efficiency from Pb contaminated soil by Sedum alfredii Hance. J Hazard Mater 168:530–535CrossRefGoogle Scholar
  102. Wang C, Tian Y, Wang X, Geng J, Jiang J, Yu H, Wang C (2010) Lead-contaminated soil induced oxidative stress, defense response and its indicative biomarkers in roots of Vicia faba seedlings. Ecotoxicology 19:1130–1139CrossRefGoogle Scholar
  103. Waranusantigul P, Kruatrachue M, Pokethitiyook P, Auesukaree C (2008) Evaluation of Pb phytoremediation potential in Buddleja asiatica and B-paniculata. Water Air Soil Poll 193:79–90CrossRefGoogle Scholar
  104. Waranusantigul P, Lee H, Kruatrachue M, Pokethitiyook P, Auesukaree C (2011) Isolation and characterization of lead-tolerant Ochrobactrum intermedium and its role in enhancing lead accumulation by Eucalyptus camaldulensis. Chemosphere 85:584–590CrossRefGoogle Scholar
  105. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opi Biotech 20:248–254CrossRefGoogle Scholar
  106. Wojas S, Ruszczynska A, Bulska E, Wojciechowski M, Antosiewicz DM (2007) Ca2+-dependent plant response to Pb2+ is regulated by LCT1. Environ Pollut 147:584–592CrossRefGoogle Scholar
  107. Xu Y, Yamaji N, Shen RF, Ma JF (2007) Sorghum roots are inefficient in uptake of EDTA-chelated lead. Ann Bot London 99:869–875CrossRefGoogle Scholar
  108. Xu MJ, Dong JF, Zhang XB (2008) Signal interaction between nitric oxide and hydrogen peroxide in heat shock induced hypericin production of Hypericum perforatum suspension cells. Sci China Ser C: Life Sci 51:676–686CrossRefGoogle Scholar
  109. Yang X, Long XX, Ni WZ, Fu CX (2002) Sedum alfredii H: a new Zn hyperaccumulating plant first found in China. Chi Sci Bull 47:1634–1637Google Scholar
  110. Yu Q, Sun L, Jin H, Chen Q, Chen Z, Xu M (2012) Lead-induced nitric oxide generation plays a critical role in lead uptake by Pogonatherum crinitum root cells. Plant Cell Physiol 53:1728–1736CrossRefGoogle Scholar
  111. Zaier H, Ghnaya T, Ben Rejeb K, Lakhdar A, Rejeb S, Jemal F (2010a) Effects of EDTA on phytoextraction of heavy metals (Zn, Mn and Pb) from sludge-amended soil with Brassica napus. Biores Technol 101:3978–3983CrossRefGoogle Scholar
  112. Zaier H, Ghnaya T, Lakhdar A, Baioui R, Ghabriche R, Mnasri M, Sghair S, Lutts S, Abdelly C (2010b) Comparative study of Pb-phytoextraction potential in Sesuvium portulacastrum and Brassica juncea: Tolerance and accumulation. J Hazard Mater 183:609–615CrossRefGoogle Scholar
  113. Zhang YF, He LY, Chen ZJ, Zhang WH, Wang QY, Qian M, Sheng XF (2011) Characterization of lead-resistant and ACC deaminase-producing endophytic bacteria and their potential in promoting lead accumulation of rape. J Hazard Mater 186:1720–1725CrossRefGoogle Scholar
  114. Zheng LJ, Liu XM, Lutz-Meindl U, Peer T (2011) Effects of lead and EDTA-assisted lead on biomass, lead uptake and mineral nutrients in Lespedeza chinensis and Lespedeza davidii. Water Air Soil Poll 220:57–68CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Departamento de Bioquímica, Biología Cellular y Molecular de PlantasEstación Experimental del Zaidín, CSICGranadaSpain
  2. 2.Ministry of Education key laboratory of Environmental Remediation and Ecosystem HealthZhejiang UniversityHangzhouChina

Personalised recommendations