Skip to main content
SpringerLink
Log in

Genetic Engineering of Plants for Heavy Metal Removal from Soil

  • Chapter
Book cover Heavy Metal Contamination of Soils

Part of the book series: Soil Biology ((SOILBIOL,volume 44))

Abstract

A large amount of hazardous materials including heavy metals were released into the environment from natural and extensive anthropogenic activities, which cause soil, air, and water pollution and deterioration. At higher concentration, these metals exert toxic effects on plant and animal health including human. Among various traditional soil remediation technologies, use of phytoremediation to clean up metal(loid)-contaminated sites has gained increasing attention as an inexpensive, eco-friendly, and publicly acceptable remediation technology but has experienced varied successes in practice. Recent scientific discoveries that resulted from the application of molecular biology, bioinformatics, omics, and next-generation DNA sequencing technologies have assisted the remarkable impact of these immensely parallel platforms on genetics. In this context, genetic engineering has contributed rapid and significant changes in the crop improvement by offering a wide array of novel genes and traits which can be effectively inserted into candidate plants to raise its phytoremediation potential for metal removal. This review summarizes recent advances in the field of transgenic plant research with particular emphasis on genetic engineering of plants for heavy metal removal from contaminated soils, potential target genes, plant transformation methods, model systems for transgenic studies, optimization of transgene expressions in transgenic plants, along with risk assessment and mitigation strategies. Besides, the role of transgenic hairy roots and genetic engineering of plant symbionts in heavy metal phytoremediation is also discussed. However, translation of this knowledge into usable technologies is the need of the hour to accelerate phytoremediation as an eco-friendly and cost-effective technology.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
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

  • Aken BV (2008) Transgenic plants for phytoremediation helping nature to clean up environmental pollution. Trends Biotechnol 26:225–227

    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, vol 19, Soil biology. Springer, Berlin, pp 19–29

    Google Scholar 

  • 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 20:171–182

    CAS  PubMed  Google Scholar 

  • Arthur EL, Rice PJ, Rice PJ, Anderson TA, Baladi SM, Henderson KLD, Coats JR (2005) Phytoremediation - an overview. Crit Rev Plant Sci 24:109–122

    CAS  Google Scholar 

  • Bañuelos G, LeDuc DL, Pilon-Smits EAH, Tagmount A, Terry N (2007) Transgenic Indian mustard overexpressing selenocysteine lyase or selenocysteine methyltransferase exhibit enhanced potential for selenium phytoremediation under field conditions. Environ Sci Technol 41:599–605

    PubMed  Google Scholar 

  • Bañuelos G, Terry N, LeDuc DL, Pilon-Smits EAH, Mackey B (2005) Field trial of transgenic Indian mustard plants shows enhanced phytoremediation of selenium- contaminated sediment. Environ Sci Technol 39:1771–1777

    PubMed  Google Scholar 

  • Bell TH, Joly S, Pitre FE, Yergeau E (2014) Increasing phytoremediation efficiency and reliability using novel omics approaches. Trends Biotechnol 32:271–280

    CAS  PubMed  Google Scholar 

  • Bennett LE, Burkhead JL, Hale KL, Terry N, Pilon M, Pilon-Smits EAH (2003) Analysis of transgenic Indian mustard plants for phytoremediation of metal-contaminated mine tailings. J Environ Qual 32:432–440

    CAS  PubMed  Google Scholar 

  • Bizily SP, Kim T, Kandasamy MK, Meagher RB (2003) Subcellular targeting of methylmercury lyase enhances its specific activity for organic mercury detoxification in plants. Plant Physiol 131:463–471

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bizily SP, Rugh CL, Meagher RB (2000) Phytodetoxification of hazardous organomercurials by genetically engineered plants. Nat Biotechnol 18:213–217

    CAS  PubMed  Google Scholar 

  • Bizily SP, Rugh CL, Summers AO, Meagher RB (1999) Phytoremediation of methylmercury pollution: merB expression in Arabidopsis thaliana confers resistance to organomercurials. Proc Natl Acad Sci U S A 96:6808–6813

    PubMed Central  CAS  PubMed  Google Scholar 

  • Block M (1993) The cell biology of plant transformation: current state, problems, prospects and the implications for the plant breeding. Euphytica 71:1–14

    Google Scholar 

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

    CAS  Google Scholar 

  • Boominathan R, Doran PM (2003a) Organic acid complexation, heavy metal distribution and the effect of ATPase inhibition in hairy roots of hyperaccumulator plant species. J Biotechnol 101:131–146

    CAS  PubMed  Google Scholar 

  • Boominathan R, Doran PM (2003b) Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator Thlaspi caerulescens. Biotechnol Bioeng 83:158–167

    CAS  PubMed  Google Scholar 

  • Chaney RL, Li YM, Brown SL, Homer FA, Malik M, Angle JS, Baker AJM, Reeves RD, Chin M (2000) Improving metal hyperaccumulator wild plants to develop commercial phytoextraction systems: approaches and progress. In: Terry N, Bañuelos G (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, FL, pp 129–158

    Google Scholar 

  • Chatterjee S, Mitra A, Datta S, Veer V (2013) Phytoremediation protocols: an overview. In: Gupta DK (ed) Plant-based remediation processes. Springer, Berlin, pp 1–18

    Google Scholar 

  • Cherian S, Oliveira M (2005) Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Technol 39:9377–9390

    CAS  PubMed  Google Scholar 

  • Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832

    PubMed Central  CAS  PubMed  Google Scholar 

  • Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of Nramp1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755

    PubMed Central  CAS  PubMed  Google Scholar 

  • Czakó M, Feng X, He Y, Liang D, Márton L (2006) Transgenic Spartina alterniflora for phytoremediation. Environ Geochem Health 28:103–110

    PubMed  Google Scholar 

  • Daghan H, Arslan M, Uygur V, Koleli N (2013) Transformation of tobacco with ScMTII gene-enhanced cadmium and zinc accumulation. Clean Soil Air Water 41:503–509

    CAS  Google Scholar 

  • Daniell H (2002) Molecular strategies for gene containment in transgenic crops. Nat Biotechnol 20:581–586

    PubMed Central  CAS  PubMed  Google Scholar 

  • de la Fuente JM, Ramírez-Rodríguez V, Cabrera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276:1566–1568

    PubMed  Google Scholar 

  • Denkhaus E, Salnikow K (2002) Nickel essentiality, toxicity and carcinogenicity. Crit Rev Oncol Hemat 42:35–56

    CAS  Google Scholar 

  • Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Sashti NA, Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and γ- glutamylcysteine synthetase expression. Nat Biotechnol 20:1140–1145

    CAS  PubMed  Google Scholar 

  • Dickinson NM, Baker AJM, Doronila A, Laidlaw S, Reeves RD (2009) Phytoremediation of inorganics: realism and synergies. Int J Phytorem 11:97–114

    CAS  Google Scholar 

  • Domínguez-Solís JR, López-Martín MC, Ager FJ, Ynsa MD, Romero LC, Gotor C (2004) Increased cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis thaliana. Plant Biotechnol J 2:469–476

    PubMed  Google Scholar 

  • Doran PM (2009) Application of plant tissue cultures in phytoremediation research: incentives and limitations. Biotechnol Bioeng 103:60–76

    CAS  PubMed  Google Scholar 

  • Dushenkov V, Nanda Kumar PBA, Motto H, Raskin I (1995) Rhizofiltration: the use of plants to remove heavy metals from aqueous streams. Environ Sci Technol 29:1239–1245

    CAS  PubMed  Google Scholar 

  • Eapen S, D’souza SF (2005) Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol Adv 23:97–114

    CAS  PubMed  Google Scholar 

  • Eapen S, Suseelan K, Tivarekar S, Kotwal S, Mitra R (2003) Potential for rhizofiltration of uranium using hairy root cultures of Brassica juncea and Chenopodium amaranticolor. Environ Res 91:127–133

    CAS  PubMed  Google Scholar 

  • EPA (1998) A citizen’s guide to phytoremediation. EPA, Washington, DC, EPA publication 542-F-98-011

    Google Scholar 

  • Evans K, Gatehouse J, Lindsay W, Shi J, Tommey A, Robinson N (1992) Expression of the pea metallothionein-like gene PsMTa in Escherichia coli and Arabidopsis thaliana and analysis of trace metal ion accumulation: implications for PsMTa function. Plant Mol Biol 20:1019–1028

    CAS  PubMed  Google Scholar 

  • Flocco CG, Giulietti AM (2007) In vitro hairy root cultures as a tool for phytoremediation research. In: Willey N (ed) Phytoremediation methods in biotechnology. Humana, Totowa, NJ

    Google Scholar 

  • Freisinger E (2011) Structural features specific to plant metallothioneins. J Biol Inorg Chem 16:1035–1045

    CAS  PubMed  Google Scholar 

  • Gasic K, Korban SS (2007) Transgenic Indian mustard (Brassica juncea) plants expressing an Arabidopsis phytochelatin synthase (AtPCS1) exhibit enhanced As and Cd tolerance. Plant Mol Biol 64:361–369

    CAS  PubMed  Google Scholar 

  • Gelvin SB (2000) Agrobacterium and plant genes involved in T-DNA transfer and integration. Annu Rev Plant Physiol Plant Mol Biol 51:223–256

    CAS  PubMed  Google Scholar 

  • Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “Gene-Jockeying” tool. Microbiol Mol Biol Rev 67:16–37

    PubMed Central  CAS  PubMed  Google Scholar 

  • George EF, Hall MA, De Klerk GJ (2008) Plant propagation by tissue culture, 3rd edn. Springer, Berlin

    Google Scholar 

  • Georgiev MI, Agostini E, Ludwig-Müller J, Xu J (2012) Genetically transformed roots: from plant disease to biotechnological resource. Trends Biotechnol 30:528–537

    CAS  PubMed  Google Scholar 

  • Gifford S, Dunstan RH, O’Connor W, Koller CE, MacFarlane GR (2006) Aquatic zooremediation: deploying animals to remediate contaminated aquatic environments. Trends Biotechnol 25:60–65

    PubMed  Google Scholar 

  • Giri A, Narasu L (2000) Transgenic hairy roots: recent trends and applications. Biotechnol Adv 18:1–22

    CAS  PubMed  Google Scholar 

  • Gisbert C, Ros R, De Haro A, Walker DJ, Pilar Bernal M, Serrano R, Navarro-Aviñó J (2003) A plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochem Biophys Res Commun 303:440–445

    CAS  PubMed  Google Scholar 

  • Golan-Goldhirsh A, Barazani O, Nepovim A, Soudek P, Smrcek S, Dufkova L, Krenkova S, Yrjala K, Schröders P, Vanek T (2004) Plant response to heavy metals and organic pollutants in cell culture and at whole plant level. J Soils Sedim 4:133–140

    CAS  Google Scholar 

  • Guerinot ML, Salt DE (2001) Fortified foods and phytoremediation. Two sides of the same coin. Plant Physiol 125:164–167

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guo J, Dai X, Xu W, Ma M (2008) Overexpressing gsh1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026

    CAS  PubMed  Google Scholar 

  • Gupta AK, Verma SK, Khan K, Verma RK (2013) Phytoremediation using aromatic plants: a sustainable approach for remediation of heavy metals polluted sites. Environ Sci Technol 47:10115–10116

    CAS  PubMed  Google Scholar 

  • Ha H, Olson J, Bian L, Rogerson PA (2014) Analysis of heavy metal sources in soil using Kriging interpretation on principle components. Environ Sci Technol 48:4999. doi:10.1021/es405083f

    CAS  PubMed  Google Scholar 

  • Häggman H, Raybould A, Borem A, Fox T, Handley L, Hertzberg M, Lu M-Z, Macdonald P, Oguchi T, Pasquali G, Pearson L, Peter G, Quemada H, Séguin A, Tattersall K, Ulian E, Walter C, McLean M (2013) Genetically engineered trees for plantation forests: key considerations for environmental risk assessment. Plant Biotechnol J 11:785–798

    PubMed Central  PubMed  Google Scholar 

  • Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613

    CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Fujita M (2013) Heavy metals in the environment current status, toxic effects on plants and phytoremediation. In: Anjum NA, Pereira ME, Ahmad I, Duarte AC, Umar S, Khan NA (eds) Phytotechnologies: remediation of environmental contaminants. CRC Press Taylor & Francis Group, Boca Raton, FL, pp 7–74

    Google Scholar 

  • Hasegawa I, Terada E, Sunairi M, Wakita H, Shinmachi F, Noguchi A, Nakajima M, Yazaki J (1997) Genetic improvement of heavy metal tolerance in plants by transfer of the yeast metallothionein gene (CUP1). Plant Soil 196:277–281

    CAS  Google Scholar 

  • Hassinen VH, Tervahauta AI, Schat H, Kärenlampi SO (2011) Plant metallothioneins – metal chelators with ROS scavenging activity. Plant Biol 13:225–232

    CAS  PubMed  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    CAS  PubMed  Google Scholar 

  • He YK, Sun JG, Feng XZ, Czakó M, Márton L (2001) Differential mercury volatilization by tobacco organs expressing a modified bacterial merA gene. Cell Res 11:231–236

    CAS  PubMed  Google Scholar 

  • Herzig R, Guadagnini M, Rehnert A, Erismann KH (2003) Phytoextraction efficiency of in vitro bred tobacco variants using a non-GMO approach. In: Vanek T, Schwitzguebel JP (eds) Phytoremediation inventory – COST Action 837 view. UOCHB AVČR, Prague

    Google Scholar 

  • Hills MJ, Hall L, Arnison PJ, Good AG (2007) Genetic use restriction technologies (GURTs): strategies to impede transgene movement. Trends Plant Sci 12:177–183

    CAS  PubMed  Google Scholar 

  • Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hsieh J, Chen C, Chiu M, Chein M, Chang J, Endo G, Huang CC (2009) Expressing a bacterial mercuric ion binding protein in plant for phytoremediation of heavy metals. J Hazard Mater 161:920–925

    CAS  PubMed  Google Scholar 

  • Hu ZR, Du M (2006) Hairy root and its application in plant genetic engineering. J Integr Plant Biol 48:121–127

    CAS  Google Scholar 

  • Huysen T, Terry N, Pilon-Smits EAH (2004) Exploring the selenium phytoremediation potential of transgenic Brassica juncea overexpressing ATP sulfurylase or cystathionine-γ-synthase. Int J Phytorem 6:111–118

    Google Scholar 

  • Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2007) Bioremediation of cadmium contaminated soil using symbiosis between leguminous plant and recombinant rhizobia with the MTL4 and the PCS genes. Chemosphere 66:1670–1676

    CAS  PubMed  Google Scholar 

  • James CA, Strand SE (2009) Phytoremediation of small organic contaminants using transgenic plants. Curr Opin Biotech 20:237–241

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jan VV, Demacedo CC, Kinet JM, Bouharmont J (1997) Selection of Al-resistant plants from a sensitive rice cultivar using somaclonal variation, in vitro and hydroponic cultures. Euphytica 97:303–310

    Google Scholar 

  • Jarup L (2003) Hazards of heavy metal contamination. Brit Med Bull 68:167–182

    PubMed  Google Scholar 

  • Joner EJ (2013) Effects of biotic and abiotic amendments on phytoremediation efficiency applied to metal-polluted soils. In: Anjum NA, Pereira ME, Ahmad I, Duarte AC, Umar S, Khan NA (eds) Phytotechnologies: remediation of environmental contaminants. CRC Press Taylor & Francis Group, Boca Raton, FL, pp 283–288

    Google Scholar 

  • Kartosentono S, Nuraida A, Indrayanto G, Noor CZ (2001) Phytoremediation of Sr2+and its influence on the growth, Ca2+ and solasodine content of shoot culture of Solanum laciniatum. Biotechnol Lett 23:153–155

    CAS  Google Scholar 

  • Kawashima CG, Noji M, Nakamura M, Ogra Y, Suzuki KT, Saito K (2004) Heavy metal tolerance of transgenic tobacco plants over-expressing cysteine synthase. Biotechnol Lett 26:153–157

    CAS  PubMed  Google Scholar 

  • Kim J, Wyskiyzuk BE, Weathers PJ (2002) Secondary metabolism of hairy root cultures in bioreactors. In Vitro Cell Dev Biol Plant 38:1–10

    CAS  Google Scholar 

  • Kim S, Takahashi M, Higuchi K, Tsunoda K, Nakanishi H, Yoshimura E, Mori S, Nishizawa N (2005) Increased nicotianamine biosynthesis confers enhanced tolerance of high levels of metals, in particular nickel, to plants. Plant Cell Physiol 46:1809–1818

    CAS  PubMed  Google Scholar 

  • Koprivova A, Kopriva S, Jäger D, Will B, Jouanin L, Rennenberg H (2002) Evaluation of transgenic poplars over-expressing enzymes of glutathione synthesis for phytoremediation of cadmium. Plant Biol 4:664–670

    CAS  Google Scholar 

  • Korenkov V, Hirschi K, Crutchfield JD, Wagner GJ (2007a) Enhancing tonoplast Cd/H antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L. Planta 226:1379–1387

    CAS  PubMed  Google Scholar 

  • Korenkov V, Park S, Cheng N, Sreevidya C, Lachmansingh J, Morris J, Hirschi K, Wagner GJ (2007b) Enhanced Cd2+ -selective root-tonoplast-transport in tobaccos expressing Arabidopsis cation exchangers. Planta 225:403–411

    CAS  Google Scholar 

  • 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. Biotech Adv 27:799–810

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1239–1245

    PubMed  Google Scholar 

  • Chen L, Marmey P, Taylor NJ, Brizard J, Espinoza C, D’Cruz P, Huet H, Zhang S, Kochko A, Beachy RN, Fauquet CM (1998) Expression and inheritance of multiple transgenes in rice plants. Nat Biotechnol 16:1060–1064

    CAS  PubMed  Google Scholar 

  • LeDuc DL, AbdelSamie M, Móntes-Bayon M, Wu CP, Reisinger SJ, Terry N (2006) Overexpressing both ATP sulfurylase and selenocysteine methyltransferase enhances selenium phytoremediation traits in Indian mustard. Environ Pollut 144:70–76

    CAS  PubMed  Google Scholar 

  • LeDuc DL, Tarun AS, Montes-Bayon M, Meija J, Malit MF, Wu CP, AbdelSamie M, Chiang C, Tagmount A, deSouza M, Neuhierl B, Böck A, Caruso J, Terry N (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and Indian mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lee JH (2013) An overview of phytoremediation as a potentially promising technology for environmental pollution control. Biotechnol Bioprocess Eng 18:431–439

    CAS  Google Scholar 

  • Lee M, Phillips RL (1988) The chromosomal basis of somaclonal variation. Annu Rev Plant Physiol Plant Mol Biol 39:413–437

    Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Leszczyszyn OI, Imam HT, Blindauer CA (2013) Diversity and distribution of plant metallothioneins: a review of structure, properties and functions. Metallomics 5:1146–1169

    CAS  PubMed  Google Scholar 

  • Leszczyszyn OI, Schmid R, Blindauer CA (2007) Toward a property/function relationship for metallothioneins: histidine coordination and unusual cluster composition in a zinc-metallothionein from plants. Prot Struct Funct Bioinform 68:922–935

    CAS  Google Scholar 

  • Li JC, Guo JB, Xu WZ, Ma M (2007) RNA Interference-mediated silencing of phytochelatin synthase gene reduce cadmium accumulation in rice seeds. J Integr Plant Biol 49:1032–1037

    CAS  Google Scholar 

  • Li Y, Dhankher OP, Carreira L, Lee D, Chen A, Schroeder JI, Balish RS, Meagher RB (2004) Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell Physiol 45:1787–1797

    CAS  PubMed  Google Scholar 

  • Li YM, Chaney RL, Angle JS, Baker AJM (2000) Phytoremediation of heavy metal contaminated soils. Environ Sci Poll Con Ser 22:837–857

    CAS  Google Scholar 

  • Linacre NA, Whiting SN, Baker AJM, Scott Angle J, Ades PK (2003) Transgenics and phytoremediation: the need for an integrated risk assessment, management, and communication strategy. Int J Phytorem 5:181–185

    Google Scholar 

  • Lodewyckx C, Taghavi S, Mergeay M, Vangronsveld J, Clijsters H, van der Lelie D (2001) The effect of recombinant heavy metal resistant endophytic bacteria in heavy metal uptake by their host plant. Int J Phytorem 3:181–185

    Google Scholar 

  • Luo S, Wan Y, Xiao X, Guo H, Chen L, Xi Q, Chen J (2011) Isolation and characterization of endophytic bacterium LRE07 from cadmium hyperaccumulator Solanum nigrum L. and its potential for remediation. Appl Microbiol Biotechnol 89:1637–1644

    CAS  PubMed  Google Scholar 

  • Ma JF, Nomoto K (1996) Effective regulation of iron acquisition in graminaceous plants. The role of mugineic acids as phytosiderophores. Physiol Planta 97:609–617

    CAS  Google Scholar 

  • Macek T, Kotrba P, Suchova M, Skacel F, Demmerova K, Rumi T (1994) Accumulation of cadmium by hairy root cultures of Solanum niger. Biotechnol Lett 16:621–624

    CAS  Google Scholar 

  • Macek T, Macková M, Pavlíková D, Száková J, Truksa M, Cundy A, Kotrba P, Yancey N, Scouten WH (2002) Accumulation of cadmium by transgenic tobacco. Acta Biotechnol 22:101–106

    CAS  Google Scholar 

  • Martin S, Griswold W (2009) Human health effects of heavy metals. Environ Sci Technol Brief Cit 15:1–6

    Google Scholar 

  • Martínez M, Bernal P, Almela C, Vélez D, García-Agustín P, Serrano R et al (2006) An engineered plant that accumulates higher levels of heavy metals than Thlaspi caerulescens, with yields of 100 times more biomass in mine soils. Chemosphere 64:478–485

    PubMed  Google Scholar 

  • McCullen CA, Binns AN (2006) Agrobacterium tumefaciens and plant cell interactions and activities required for interkingdom macromolecular transfer. Annu Rev Cell Dev Biol 22:101–127

    CAS  PubMed  Google Scholar 

  • Mejáre M, Bülow L (2001) Metal binding proteins and peptides in bioremediation and phytoremediation of heavy metals. Trends Biotechnol 19:67–73

    PubMed  Google Scholar 

  • Menn F-M, Easter JP, Sayler GS (2000) Genetically engineered microorganisms and bioremediation. In: Klein J (ed) Biotechnology, vol 11b. Wiley, New York, NY, pp 441–463

    Google Scholar 

  • Merlot S, Hannibal L, Martins S, Martinelli L, Amir H, Lebrun M, Thomine S (2014) The metal transporter PgIREG1 from the hyperaccumulator Psychotria gabriellae is a candidate gene for nickel tolerance and accumulation. J Exp Bot 65:1551–1564

    CAS  PubMed  Google Scholar 

  • Metzger L, Fouchault I, Glad C, Prost R, Tepfer D (1992) Estimation of cadmium availability using transformed roots. Plant Soil 143:249–257

    CAS  Google Scholar 

  • Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol Adv 29:645–653

    CAS  PubMed  Google Scholar 

  • Misra S, Gedamu L (1989) Heavy metal tolerant transgenic Brassica napus L. and Nicotiana tabaccum L. plants. Theor Appl Genet 78:161–168

    CAS  PubMed  Google Scholar 

  • Nedelkoska T, Doran PM (2000a) Hyperaccumulation of cadmium by hairy roots of Thlaspi caerulescens. Biotechnol Bioeng 67:607–615

    CAS  PubMed  Google Scholar 

  • Nedelkoska T, Doran PM (2000b) Characteristics of heavy metal uptake by plant species with potential for phytoremediation and phytomining. Miner Eng 13:549–561

    CAS  Google Scholar 

  • Nedelkoska TV, Doran PM (2001) Hyperaccumulation of nickel by hairy roots of Alyssum species: comparison with whole regenerated plants. Biotechnol Prog 17:752–759

    CAS  PubMed  Google Scholar 

  • Nehnevajova E, Herzig R, Erismann KH, Schwitzguébel JP (2007) In vitro breeding of Brassica juncea L. to enhance metal accumulation and extraction properties. Plant Cell Rep 26:429–437

    CAS  PubMed  Google Scholar 

  • Newman LA, Reynolds CM (2005) Bacteria and phytoremediation: new uses for endophytic bacteria in plants. Trends Biotechnol 23:6–8

    CAS  PubMed  Google Scholar 

  • Ontañon OM, González PS, Ambrosio LF, Paisio CE, Agostini E (2014) Rhizoremediation of phenol and chromium by the synergistic combination of a native bacterial strain and Brassica napus hairy roots. Int Biodeter Biodegrad 88:192–198

    Google Scholar 

  • Pal R, Rai JPN (2010) Phytochelatins: peptides involved in heavy metal detoxification. Appl Biochem Biotechnol 160:945–963

    CAS  PubMed  Google Scholar 

  • Palmer CM, Guerinot ML (2009) Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol 5:333–340

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pan A, Yang M, Tie F, Li L, Chen Z, Ru B (1994) Expression of mouse metallothionein-I gene confers cadmium resistance in transgenic tobacco plants. Plant Mol Biol 24:341–351

    CAS  PubMed  Google Scholar 

  • Paoletti C, Flamm E, Yan W, Meek S, Renckens S, Fellouse M, Kuiperf H (2008) GMO risk assessment around the world: some examples. Trends Food Sci Technol 19:S70–S78

    Google Scholar 

  • Pavlíková D, Macek T, MacKová M, Száková J, Balík J (2004) Cadmium tolerance and accumulation in transgenic tobacco plants with a yeast metallothionein combined with a polyhistidine tail. Int Biodeter Biodegrad 54:233–237

    Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    CAS  PubMed  Google Scholar 

  • Pilon-Smits EAH, Hwang S, Lytle CM, Zhu Y, Tai JC, Bravo RC, Chen Y, Leustek T, Terry N (1999) Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol 119:123–132

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pilon-Smits EA, Pilon M (2002) Phytoremediation of metals using transgenic plants. Crit Rev Plant Sci 21:439–456

    CAS  Google Scholar 

  • Pilon-Smits EAH, LeDuc DL (2009) Phytoremediation of selenium using transgenic plants. Curr Opin Biotechnol 20:207–212

    CAS  PubMed  Google Scholar 

  • Pitzschke A (2013) From bench to barn: plant model research and its applications in agriculture. Adv Genet Eng 2:110. doi:10.4172/2169-0111.1000110

    Google Scholar 

  • Pomponi M, Censi V, DiGirolamo V, DePaolis A, di Toppi LS, Aromolo R, Costantino P, Cardarelli M (2006) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta 223:180–190

    CAS  PubMed  Google Scholar 

  • Prado JR, Segers G, Voelker T, Carson D, Dobert R, Phillips J, Cook K, Cornejo C, Monken J, Grapes L, Reynolds T, Martino-Catt S (2014) Genetically engineered crops: from idea to product. Annu Rev Plant Biol 65:769–790

    CAS  PubMed  Google Scholar 

  • Rajkumar M, Sandhya S, Prasad MN, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574

    CAS  PubMed  Google Scholar 

  • 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 180:169–181

    CAS  PubMed  Google Scholar 

  • Raskin I (1996) Plant genetic engineering may help with environmental cleanup [commentary]. Proc Natl Acad Sci U S A 93:3164–3166

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rugh CL, Senecoff JF, Meagher RB, Merkle SA (1998) Development of Transgenic yellow poplar for mercury phytoremediation. Nat Biotechnol 16:925–928

    CAS  PubMed  Google Scholar 

  • Rugh CL, Wilde HD, Stack NM, Thompson DM, Summers AO, Meagher RB (1996) Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modified bacterial merA gene. Proc Natl Acad Sci U S A 93:3182–3187

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ruiz ON, Daniell H (2009) Genetic engineering to enhance mercury phytoremediation. Curr Opin Biotech 20:213–219

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ruiz ON, Hussein HS, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol 132:1344–1352

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9

    CAS  PubMed  Google Scholar 

  • Salt DE, Prince RE, Pickering IJ, Raskin I (1995) Mechanism of cadmium mobility and accumulation ion Indian mustard. Plant Physiol 109:1427–1433

    PubMed Central  CAS  PubMed  Google Scholar 

  • Santos-Díaz MS (2013) Metal remediation via in vitro root cultures. In: Gupta DK (ed) Plant-based remediation processes, vol 35, Soil biology. Springer, Berlin, pp 101–116

    Google Scholar 

  • Sasaki Y, Hayakawa T, Inoue C, Miyazaki A, Silver S, Kusano T (2006) Generation of mercury hyperaccumulating plants through transgenic expression of the bacterial mercury membrane transport protein MerC. Transgenic Res 15:615–625

    CAS  PubMed  Google Scholar 

  • Schenk PM, Carvalhais LC, Kazan K (2012) Unraveling plant–microbe interactions: can multi-species transcriptomics help. Trends Biotechnol 30:177–184

    CAS  PubMed  Google Scholar 

  • Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK, Tsay YF, Sanders D (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sessitsch A, Puschenreiter M (2008) Endophytes and rhizosphere bacteria of plants growing in heavy metal-containing soils. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Springer, New York, NY, pp 317–332

    Google Scholar 

  • Shanks JV, Morgan J (1999) Plant ‘hairy root’ culture. Curr Opin Biotech 10:151–155

    CAS  PubMed  Google Scholar 

  • Shaul O, Hilgemann DW, de-Almeida-Engler J, Van Montagu N, Inze D, Galili G (1999) Cloning and characterization of a novel Mg2+ ⁄H+ exchanger. EMBO J 18:3973–3980

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shukla D, Kesari R, Tiwari M, Dwivedi S, Tripathi RD, Nath P, Trivedi PK (2013) Expression of Ceratophyllum demersum phytochelatin synthase CdPCS1 in Escherichia coli and Arabidopsis enhances heavy metal(loid)s accumulation. Protoplasma 250:1263–1272

    CAS  PubMed  Google Scholar 

  • Sone Y, Nakamura R, Pan-Hou H, Sato MH, Itoh T, Kiyono M (2013) Increase methylmercury accumulation in Arabidopsis thaliana expressing bacterial broad-spectrum mercury transporter MerE. AMB Exp 3:52

    Google Scholar 

  • Song W, Sohn EJ, Martinoia E, Lee YJ, Yang Y, Jasinski M, Forestier C, Hwang I, Lee Y (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotechnol 21:914–919

    CAS  PubMed  Google Scholar 

  • Soudek P, Petrová S, Benešová D, Vanĕk T (2011) Uranium uptake and stress responses of in vitro cultivated hairy root culture of Armoracia rusticana. Agrochimica 60:15–28

    Google Scholar 

  • Straczek A, Wannijn J, Van Hees M, Thijs H, Tiry Y (2009) Tolerance of hairy roots of carrots to U chronic exposure in standardized in vitro device. Environ Exp Bot 65:82–89

    CAS  Google Scholar 

  • Subroto MA, Priambodo S, Indrasti NS (2007) Accumulation of zinc by hairy root cultures of Solanum nigrum. Biotechnology 6:344–348

    CAS  Google Scholar 

  • Sunitha MSL, Prashant S, Anilkumar S, Rao S, Narasu ML, Kavi Kishore PB (2013) Cellular and molecular mechanisms of heavy metal tolerance in plants: a brief overview of transgenic plants overexpressing phytochelatin synthase and metallothionein genes. Plant Cell Biotech Mol Biol 14:33–48

    Google Scholar 

  • Takahashi M, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotechnol 19:466–469

    CAS  PubMed  Google Scholar 

  • Talano MA, Oller ALW, González P, González SO, Agostini E (2014) Effects of arsenate on tobacco hairy root and seedling growth, and its removal. In Vitro Cell Dev Biol Plant 50:217–225

    CAS  Google Scholar 

  • Tangahu BV, Abdullah SRS, 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, Article ID: 939161, pp 1–31

    Google Scholar 

  • Thomas JC, Davies EC, Malick FK, Endreszl C, Williams CR, Abbas M, Petrella S, Swisher K, Perron M, Edwards R, Osenkowski P, Urbanczyk N, Wiesend WN, Murray KS (2003) Yeast metallothionein in transgenic tobacco promotes copper uptake from contaminated soils. Biotechnol Prog 19:273–280

    CAS  PubMed  Google Scholar 

  • Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci U S A 97:4991–4996

    PubMed Central  CAS  PubMed  Google Scholar 

  • Uriu-Adams JY, Keen CL (2005) Copper oxidative stress and human health. Mol Aspects Med 26:268–298

    CAS  PubMed  Google Scholar 

  • van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JA, Hooykaas PJ (1999) Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119:1047–1055

    PubMed Central  PubMed  Google Scholar 

  • Van Huysen T, Abdel-Ghany S, Hale KL, LeDuc D, Terry N, Pilon-Smits EAH (2003) Overexpression of cystathionine-γ-synthase enhances selenium volatilization in Brassica juncea. Planta 218:71–78

    PubMed  Google Scholar 

  • Viehweger K (2014) How plants cope with heavy metals. Bot Stud 55:35–46

    Google Scholar 

  • Wang H-L, Tian C-Y, Jiang L, Wang L (2014) Remediation of heavy metals contaminated saline soils: a halophyte choice? Environ Sci Technol 48:21–22

    CAS  PubMed  Google Scholar 

  • Weyens N, Lelie D, Taghavi S, Newman L, Vangronsveld J (2009a) Exploiting plant–microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598

    CAS  PubMed  Google Scholar 

  • Weyens N, Lelie D, Taghavi S, Vangronsveld J (2009b) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotech 20:248–254

    CAS  PubMed  Google Scholar 

  • Zhang Y, Liu J (2011) Transgenic alfalfa plants co-expressing glutathione S-transferase (GST) and human CYP2E1 show enhanced resistance to mixed contaminates of heavy metals and organic pollutants. J Haza Mat 189:357–362

    CAS  Google Scholar 

  • Zhou ML, Tang YX, Wu YM (2013) Plant hairy roots for remediation of aqueous pollutants. Plant Mol Biol Rep 31:1–8

    Google Scholar 

  • Zhu YL, Pilon-Smits EA, Jouanin L, Terry N (1999a) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:73–80

    CAS  Google Scholar 

  • Zhu YL, Pilon-Smits EA, Tarun AS, Weber SU, Jouanin L, Terry N (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol 121:1169–1178

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ziemienowicz A (2014) Agrobacterium-mediated plant transformation: factors, applications and recent advances. Biocatal Agric Biotechnol 3:95. doi:10.1016/j.bcab.2013.10.004

    Google Scholar 

Download references

Acknowledgment

UBJ thanks University Grants Commission, New Delhi, India, for providing Dr D. S. Kothari postdoctoral fellowship, and VAB thanks Indian National Science Academy, New Delhi, India, for providing INSA Senior Scientist Fellowship.

Author information

Authors and Affiliations

  1. Department of Biotechnology, Shivaji University Vidyanagar, Kolhapur, MS 416004, India

    Umesh B. Jagtap & Vishwas A. Bapat

Authors
  1. Umesh B. Jagtap
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vishwas A. Bapat
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vishwas A. Bapat .

Editor information

Editors and Affiliations

  1. Institut für Allgemeine Botanik und Pflanzenphysiologie, Universität Jena, Jena, Germany

    Irena Sherameti

  2. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Ajit Varma

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Jagtap, U.B., Bapat, V.A. (2015). Genetic Engineering of Plants for Heavy Metal Removal from Soil. In: Sherameti, I., Varma, A. (eds) Heavy Metal Contamination of Soils. Soil Biology, vol 44. Springer, Cham. https://doi.org/10.1007/978-3-319-14526-6_22

Download citation

Publish with us

Policies and ethics

Search

Navigation