Abstract
Contamination by heavy metals including As, Cd, Co, Cu, Fe, Hg, Mn, Ni and Zn in agricultural fields is a global safety issue. Indeed, excessive accumulations of metals have detrimental effects on life by altering cell components such as lipids, proteins, enzymes and DNA. Phytoremediation appears as a solution to remove metals from contaminated sites, yet metal uptake is usually low in most common plants. Therefore, genetically engineered plants have been designed for higher efficiency of metal accumulation. Here, we review metal phytoremediation by genetically engineered plants with focus on metal uptake and transport, mechanisms involving phytochelatin and metallothionein proteins, toxicity, plant species, methods of gene transfer and gene editing.



Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Abbreviations
- AtPCs1:
-
Arabidopsis thaliana phytochelatin synthase 1
- AtACBP1:
-
Arabidopsis thaliana acyl-CoA-binding domain-containing protein 1
- bphC:
-
Biphenyl-2,3-diol 1,2-dioxygenase
- cad1–3:
-
Arabidopsis thaliana knockout mutant for phytochelatin synthase 1
- CarMT:
-
Cicer arietinum metallothionein
- CCoAOMT:
-
Caffeoyl-CoA O-methyltransferase
- CePCs:
-
Caenorhabditis elegans phytochelatin synthase 1
- chv:
-
Chromosomal virulence
- CKX2:
-
Cytokinin dehydrogenase 2
- COR15a:
-
Cold regulated 15 a promoter
- IlMT2b:
-
Iris lactea var. chinensis metallothionein 2b
- Lm-SAP:
-
Lobularia maritima stress-associated protein
- MAN3:
-
Endo-1,4-β-Mannanase 3
- merC:
-
Mercury transporter
- Met:
-
Metallothionein
- MsYSL:
-
Miscanthus sacchariflorus yellow stripe-like
- OsARM1:
-
Oryza sativa arsenite-responsive myeloblastosis 1
- OsMyb4:
-
Oryza sativa myeloblastosis 4
- OsMT2c:
-
Oryza sativa metallothionein 2c
- PCs1:
-
Phytochelatin synthase 1
- PtoHMA5:
-
Populus tomentosa heavy metal ATPase 5
- PtPCs:
-
Populus tomentosa phytochelatin synthase
- PjHMT:
-
Prosopis juliflora heavy metal ATPase peptide
- PtoEXPA12:
-
Populus tomentosa alpha expansin 12
- PtPCs:
-
Populus tomentosa phytochelatin synthase
- ricMT:
-
Rice metallothionein
- SaCAD:
-
Sedum alfredii cinnamyl alcohol dehydrogenase
- SsMT2:
-
Suaeda salsa metallothionein 2
- VcPCs1:
-
Vicia sativa phytochelatin synthase 1
- vir:
-
Virulence
- VsCCoAOMT:
-
Vicia sativa caffeoyl-CoA O-methyltransferase
- XCD1:
-
XVE system-induced cadmium-tolerance 1
References
Abid M et al (2016) Arsenic(V) biosorption by charred orange peel in aqueous environments. Int J Phytoremediat 18:442–449. https://doi.org/10.1080/15226514.2015.1109604
Agnihotri A, Seth CS (2019) Chapter 11—Transgenic Brassicaceae: a promising approach for phytoremediation of heavy metals. In: Prasad MNV (ed) Transgenic plant technology for remediation of toxic metals and metalloids. Academic Press, New York, pp 239–255. https://doi.org/10.1016/B978-0-12-814389-6.00011-0
Ahmad MM, Ali A, Siddiqui S, Kamaluddin, Abdin MZ (2017) Methods in Transgenic Technology. In: Abdin MZ, Kiran U, Kamaluddin, Ali A (eds) Plant Biotechnology: Principles and Applications. Springer, Singapore, pp 93–115. https://doi.org/10.1007/978-981-10-2961-5_4
Akguc N, Ozyigit II, Yarci C (2008) Pyracantha coccinea roem. (Rosaceae) as a biomonitor for Cd, Pb and Zn in Mugla Province (TURKEY). Pak J Bot 40:1767–1776
Akguc N, Ozyigit II, Yasar U, Leblebici Z, Yarci C (2010) Use of Pyracantha coccinea Roem. as a possible biomonitor for the selected heavy metals. Int J Environ Sci Technol 7:427–434. https://doi.org/10.1007/bf03326152
Alagić SČ, Jovanović VPS, Mitić VD, Cvetković JS, Petrović GM, Stojanović GS (2016) Bioaccumulation of HMW PAHs in the roots of wild blackberry from the Bor region (Serbia): phytoremediation and biomonitoring aspects. Sci Total Environ 562:561–570. https://doi.org/10.1016/j.scitotenv.2016.04.063
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91:869–881
Alok A, Sharma S, Kumar J, Verma S, Sood H (2017) Engineering in plant genome using agrobacterium: progress and future. In: Kalia VC, Saini AK (eds) Metabolic engineering for bioactive compounds: strategies and processes. Springer, Singapore, pp 91–111. https://doi.org/10.1007/978-981-10-5511-9_5
Anh BTK, Ha NTH, Danh LT, Van Minh V, Kim DD (2017) Phytoremediation applications for metal-contaminated soils using terrestrial plants in Vietnam. In: Ansari AA, Gill SS, Gill R, Lanza GR, Newman L (eds) Phytoremediation: management of environmental contaminants, vol 5. Springer, Cham, pp 157–181. https://doi.org/10.1007/978-3-319-52381-1_6
Anjum NA, Aref IM, Duarte AC, Pereira E, Ahmad I, Iqbal M (2014) Glutathione and proline can coordinately make plants withstand the joint attack of metal(loid) and salinity stresses. Front Plant Sci 5:662. https://doi.org/10.3389/fpls.2014.00662
Arslan M, Imran A, Khan QM, Afzal M (2017) Plant-bacteria partnerships for the remediation of persistent organic pollutants. Environ Sci Pollut Res 24:4322–4336
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. https://doi.org/10.1080/07352680590952496
Asgari Lajayer B, Ghorbanpour M, Nikabadi S (2017) Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants. Ecotoxicol Environ Saf 145:377–390. https://doi.org/10.1016/j.ecoenv.2017.07.035
Atia FAM, Al-Ghouti MA, Al-Naimi F, Abu-Dieyeh M, Ahmed T, Al-Meer SH (2019) Removal of toxic pollutants from produced water by phytoremediation: applications and mechanistic study. J Water Process Eng 32:100990. https://doi.org/10.1016/j.jwpe.2019.100990
Auer C (2008) Ecological risk assessment and regulation for genetically-modified ornamental plants. Crit Rev Plant Sci 27:255–271
Bai J, Wang X, Wang R, Wang J, Le S, Zhao Y (2019) Overexpression of three duplicated BnPCS genes enhanced Cd accumulation and translocation in Arabidopsis thaliana mutant cad1–3. Bull Environ Contam Toxicol 102:146–152. https://doi.org/10.1007/s00128-018-2487-1
Bañuelos GS, Ajwa HA, Terry N, Zayed A (1997) Phytoremediation of selenium laden soils: a new technology. J Soil Water Conserv 52:426–430
Barampuram S, Zhang ZJ (2011) Recent advances in plant transformation. Methods Mol Biol (Clifton, NJ) 701:1–35. https://doi.org/10.1007/978-1-61737-957-4_1
Barber SA (1962) A diffusion and mass-flow concept of soil nutrient availability. Soil Sci 93:39–49
Basharat Z, Novo LAB, Yasmin A (2018) Genome editing weds CRISPR: what is in it for phytoremediation? Plants 7:51
Baxter I et al (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132:618–628. https://doi.org/10.1104/pp.103.021923
Belouchi A, Kwan T, Gros P (1997) Cloning and characterization of the OsNramp family from Oryza sativa, a new family of membrane proteins possibly implicated in the transport of metal ions. Plant Mol Biol 33:1085–1092. https://doi.org/10.1023/a:1005723304911
Berni R et al (2018) Reactive oxygen species and heavy metal stress in plants: impact on the cell wall and secondary metabolism. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2018.10.017
Bhaya D, Davison M, Barrangou R (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 45:273–297. https://doi.org/10.1146/annurev-genet-110410-132430
Bibikova M, Carroll D, Segal DJ, Trautman JK, Smith J, Kim YG, Chandrasegaran S (2001) Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol 21:289–297. https://doi.org/10.1128/mcb.21.1.289-297.2001
Boch J et al (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509–1512. https://doi.org/10.1126/science.1178811
Bondada BR, Tu S, Ma LQ (2004) Absorption of foliar-applied arsenic by the arsenic hyperaccumulating fern (Pteris vittata L.). Sci Total Environ 332:61–70. https://doi.org/10.1016/j.scitotenv.2004.05.001
Boudet AM (2007) Evolution and current status of research in phenolic compounds. Phytochemistry 68:2722–2735
Bradshaw JE (2016) Genetically modified crops. In: Bradshaw JE (ed) Plant breeding: past, present and future. Springer, Berlin. https://doi.org/10.1007/978-3-319-23285-0
Brune B, Hartzell P, Nicotera P, Orrenius S (1991) Spermine prevents endonuclease activation and apoptosis in thymocytes. Exp Cell Res 195:323–329
Cameselle C, Gouveia S, Urréjola S (2019) Benefits of phytoremediation amended with DC electric field. Application to soils contaminated with heavy metals. Chemosphere 229:481–488. https://doi.org/10.1016/j.chemosphere.2019.04.222
Cetintas VB, Kotmakcı M, Kaymaz BT (2017) From the immune response to the genome design; CRISPR-Cas9 system: review. Turkiye Klinikleri J Med Sci 37:27–42. https://doi.org/10.5336/medsci.2016-54153
Chand S, Yaseen M, Rajkumari Patra DD (2015) Application of heavy metal rich tannery sludge on sustainable growth, yield and metal accumulation by clarysage (Salvia sclarea L.). Int J Phytoremediat 17:1171–1176. https://doi.org/10.1080/15226514.2015.1045128
Chandra R, Yadav S (2010) Potential of Typha angustifolia for phytoremediation of heavy metals from aqueous solution of phenol and melanoidin. Ecol Eng 36:1277–1284. https://doi.org/10.1016/j.ecoleng.2010.06.003
Chaurasia N, Mishra Y, Rai LC (2008) Cloning expression and analysis of phytochelatin synthase (pcs) gene from Anabaena sp. PCC 7120 offering multiple stress tolerance in Escherichia coli. Biochem Biophys Res Commun 376:225–230. https://doi.org/10.1016/j.bbrc.2008.08.129
Chen L, Guo Y, Yang L, Wang Q (2008) Synergistic defensive mechanism of phytochelatins and antioxidative enzymes in Brassica chinensis L. against Cd stress. Chin Sci Bull 53:1503. https://doi.org/10.1007/s11434-008-0062-6
Chen J et al (2015a) MAN3 gene regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis thaliana. New Phytol 205:570–582. https://doi.org/10.1111/nph.13101
Chen YK, Liu YX, Ding YN, Wang XT, Xu JC (2015b) Overexpression of PtPCS enhances cadmium tolerance and cadmium accumulation in tobacco. Plant Cell Tissue Organ 121:389–396
Chen SS, Han XJ, Fang J, Lu ZC, Qiu WM, Liu MY, Sang J, Jiang J, Zhuo RY (2017) Sedum alfredii sanramp6 metal transporter contributes to cadmium accumulation in transgenic arabidopsis thaliana. Sci Rep-Uk 7
Chen H, Zhang C, Guo H, Hu Y, He Y, Jiang D (2018) Overexpression of a Miscanthus sacchariflorus yellow stripe-like transporter MsYSL1 enhances resistance of Arabidopsis to cadmium by mediating metal ion reallocation. Plant Growth Regul 85:101–111. https://doi.org/10.1007/s10725-018-0376-6
Cherian S, Oliveira MM (2005) Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Technol 39:9377–9390
Choppala G et al (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391. https://doi.org/10.1080/07352689.2014.903747
Christian ML et al (2012) Targeting G with TAL effectors: a comparison of activities of TALENs constructed with NN and NK repeat variable di-residues. Plos One 7:e45383. https://doi.org/10.1371/journal.pone.0045383
Christie PJ (2004) Type IV secretion: the agrobacterium VirB/D4 and related conjugation systems. Biochim Biophys Acta 1694:219–234. https://doi.org/10.1016/j.bbamcr.2004.02.013
Clemens S, Antosiewicz DM, Ward JM, Schachtman DP, Schroeder JI (1998) The plant cDNA mediates the uptake of calcium and cadmium in yeast. Proc Natl Acad Sci 95:12043–12048. https://doi.org/10.1073/pnas.95.20.12043
Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18:3325–3333. https://doi.org/10.1093/emboj/18.12.3325
Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315. https://doi.org/10.1016/S1360-1385(02)02295-1
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182. https://doi.org/10.1146/annurev.arplant.53.100301.135154
Cong L et al (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823. https://doi.org/10.1126/science.1231143
Cosio C, Martinoia E, Keller C (2004) Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiol 134:716–725. https://doi.org/10.1104/pp.103.031948
Curie C et al (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11. https://doi.org/10.1093/aob/mcn207
Cutillas-Barreiro L et al (2016) Lithological and land-use based assessment of heavy metal pollution in soils surrounding a cement plant in SW Europe. Sci Total Environ 562:179–190. https://doi.org/10.1016/j.scitotenv.2016.03.198
DalCorso G (2012) Heavy metal toxicity in plants. In: Furini A (ed) Plants and heavy metals. Springer, Heidelberg, pp 1–26
DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol 50:1268–1280
DalCorso G, Manara A, Furini A (2013) An overview of heavy metal challenge in plants: from roots to shoots. Metallomics 5:1117–1132
DalCorso G, Fasani E, Manara A, Visioli G, Furini A (2019) Heavy metal pollutions: state of the art and innovation in phytoremediation. Int J Mol Sci 20:3412
Das N, Bhattacharya S, Maiti MK (2016) Enhanced cadmium accumulation and tolerance in transgenic tobacco overexpressing rice metal tolerance protein gene osmtp1 is promising for phytoremediation. Plant Physiol Bioch 105:297–309
De Farias V et al (2009) Phytodegradation potential of Erythrina crista-galli L., Fabaceae, in petroleum-contaminated soil. Appl Biochem Biotechnol 157:10–22. https://doi.org/10.1007/s12010-009-8531-1
Demarco CF, Afonso TF, Pieniz S, Quadro MS, Camargo FAD, Andreazza R (2019) Phytoremediation of heavy metals and nutrients by the Sagittaria montevidensis into an anthropogenic contaminated site at Southern of Brazil. Int J Phytoremediat 21:1145–1152. https://doi.org/10.1080/15226514.2019.1612843
Deng D, Yan C, Wu J, Pan X, Yan N (2014) Revisiting the TALE repeat. Protein Cell 5:297–306. https://doi.org/10.1007/s13238-014-0035-2
Deng L et al (2016) Long-term field phytoextraction of zinc/cadmium contaminated soil by Sedum plumbizincicola under different agronomic strategies. Int J Phytoremediat 18:134–140. https://doi.org/10.1080/15226514.2015.1058328
Dharupaneedi SP, Nataraj SK, Nadagouda M, Reddy KR, Shukla SS, Aminabhavi TM (2019) Membrane-based separation of potential emerging pollutants. Sep Purif Technol 210:850–866. https://doi.org/10.1016/j.seppur.2018.09.003
Dixit R et al (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7:2189
Doty SL, Shang TQ, Wilson AM, Moore AL, Newman LA, Strand SE, Gordon MP (2003) Metabolism of the soil and groundwater contaminants, ethylene dibromide and trichloroethylene, by the tropical leguminous tree, Leuceana leucocephala. Water Res 37:441–449
Dreier B, Beerli RR, Segal DJ, Flippin JD, Barbas CF 3rd (2001) Development of zinc finger domains for recognition of the 5′-ANN-3′ family of DNA sequences and their use in the construction of artificial transcription factors. J Biol Chem 276:29466–29478. https://doi.org/10.1074/jbc.m102604200
Du J, Yang JL, Li CH (2012) Advances in metallotionein studies in forest trees. Plant Omics 5:46–51
Du ZY, Chen MX, Chen QF, Gu JD, Chye ML (2015) Expression of arabidopsis acyl-coa-binding proteins atacbp1 and atacbp4 confers pb(ii) accumulation in brassica juncea roots. Plant Cell Environ 38:101–117
Dubey S, Shri M, Gupta A, Rani V, Chakrabarty D (2018) Toxicity and detoxification of heavy metals during plant growth and metabolism. Environ Chem Lett 16:1169–1192. https://doi.org/10.1007/s10311-018-0741-8
Dubey AK et al (2019) Over-expression of CarMT gene modulates the physiological performance and antioxidant defense system to provide tolerance against drought stress in Arabidopsis thaliana L. Ecotoxicol Environ Saf 171:54–65. https://doi.org/10.1016/j.ecoenv.2018.12.050
Durai S, Mani M, Kandavelou K, Wu J, Porteus MH, Chandrasegaran S (2005) Zinc finger nucleases: custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Res 33:5978–5990. https://doi.org/10.1093/nar/gki912
Eapen S, D’Souza SF (2005) Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol Adv 23:97–114. https://doi.org/10.1016/j.biotechadv.2004.10.001
Eapen S, Suseelan KN, Tivarekar S, Kotwal SA, Mitra R (2003) Potential for rhizofiltration of uranium using hairy root cultures of Brassica juncea and Chenopodium amaranticolor. Environ Res 91:127–133
Eapen S, Singh S, D’Souza SF (2007) Advances in development of transgenic plants for remediation of xenobiotic pollutants. Biotechnol Adv 25:442–451. https://doi.org/10.1016/j.biotechadv.2007.05.001
Ellstrand NC, Schierenbeck KA (2006) Hybridization as a stimulus for the evolution of invasiveness in plants? Euphytica 148:35–46
Ely CS, Smets BF (2017) Bacteria from wheat and cucurbit plant roots metabolize PAHs and aromatic root exudates: implications for rhizodegradation. Int J Phytoremediat 19:877–883. https://doi.org/10.1080/15226514.2017.1303805
Fan W et al (2018) Two mulberry phytochelatin synthase genes confer zinc/cadmium tolerance and accumulation in transgenic Arabidopsis and tobacco. Gene 645:95–104
Farid M et al (2020) Efficacy of Zea mays L. for the management of marble effluent contaminated soil under citric acid amendment; morpho-physiological and biochemical response. Chemosphere 240:124930. https://doi.org/10.1016/j.chemosphere.2019.124930
Fasani E, Manara A, Martini F, Furini A, DalCorso G (2018) The potential of genetic engineering of plants for the remediation of soils contaminated with heavy metals. Plant Cell Environ 41:1201–1232
Favas PJ, Pratas J, Prasad MN (2012) Accumulation of arsenic by aquatic plants in large-scale field conditions: opportunities for phytoremediation and bioindication. Sci Total Environ 433:390–397. https://doi.org/10.1016/j.scitotenv.2012.06.091
Feng Z et al (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA 111:4632–4637. https://doi.org/10.1073/pnas.1400822111
Feng NX et al (2017) Efficient phytoremediation of organic contaminants in soils using plant-endophyte partnerships. Sci Total Environ 583:352–368
Ferraz P, Fidalgo F, Almeida A, Teixeira J (2012) Phytostabilization of nickel by the zinc and cadmium hyperaccumulator Solanum nigrum L. Are metallothioneins involved? Plant Physiol Biochem PPB 57:254–260. https://doi.org/10.1016/j.plaphy.2012.05.025
Filiz E, Ozyigit II, Saracoglu IA, Uras ME, Sen U, Yalcin B (2019a) Abiotic stress-induced regulation of antioxidant genes in different Arabidopsis ecotypes: microarray data evaluation. Biotechnol Biotechnol Equip 33:128–143. https://doi.org/10.1080/13102818.2018.1556120
Filiz E, Saracoglu IA, Ozyigit II, Yalcin B (2019b) Comparative analyses of phytochelatin synthase (PCS) genes in higher plants. Biotechnol Biotechnol Equip 33:178–194. https://doi.org/10.1080/13102818.2018.1559096
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18
Gasic K, Korban SS (2006) Heavy metal stress. In: Madhava Rao KV, Raghavendra AS, Janardhan Reddy K (eds) Physiology and molecular biology of stress tolerance in plants. Springer, Dordrecht, pp 219–254. https://doi.org/10.1007/1-4020-4225-6_8
Gatliff EG (1994) Vegetative remediation process offers advantages over traditional pump-and-treat technologies. Remediat J 4:343–352. https://doi.org/10.1002/rem.3440040307
Gaur N, Flora G, Yadav M, Tiwari A (2014) A review with recent advancements on bioremediation-based abolition of heavy metals. Environ Sci Process Impacts 16:180–193. https://doi.org/10.1039/c3em00491k
Gelvin SB (2012) Traversing the cell: agrobacterium T-DNA’s journey to the host genome front. Plant Sci 3:52. https://doi.org/10.3389/fpls.2012.00052
Gerhardt KE, Huang XD, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30
Gerhardt KE, Gerwing PD, Greenberg BM (2017) Opinion: taking phytoremediation from proven technology to accepted practice. Plant Sci 256:170–185
Ghori Z, Iftikhar H, Bhatti MF, Nasar um M, Sharma I, Kazi AG, Ahmad P (2016) Chapter 15-Phytoextraction: the use of plants to remove heavy metals from soil. In: Ahmad P (ed) Plant metal interaction. Elsevier, Amsterdam, pp 385–409. https://doi.org/10.1016/B978-0-12-803158-2.00015-1
Ghori N-H, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol. https://doi.org/10.1007/s13762-019-02215-8
Gomes MAD, Hauser-Davis RA, de Souza AN, Vitoria AP (2016) Metal phytoremediation: general strategies, genetically modified plants and applications in metal nanoparticle contamination. Ecotoxicol Environ Saf 134:133–147
Gong Y, Chen JP, Pu RP (2019) The enhanced removal and phytodegradation of sodium dodecyl sulfate (SDS) in wastewater using controllable water hyacinth. Int J Phytoremediat 21:1080–1089. https://doi.org/10.1080/15226514.2019.1606779
Gonzalez H, Fernandez-Fuego D, Bertrand A, Gonzalez A (2019) Effect of pH and citric acid on the growth, arsenic accumulation, and phytochelatin synthesis in Eupatorium cannabinum L., a promising plant for phytostabilization. Environ Sci Pollut Res 26:26242–26253. https://doi.org/10.1007/s11356-019-05657-2
Gosal SS, Wani SH (2018) Plant genetic transformation and transgenic crops: methods and applications. In: Gosal SS, Wani SH (eds) Biotechnologies of crop improvement, volume 2: transgenic approaches. Springer, Cham, pp 1–23. https://doi.org/10.1007/978-3-319-90650-8_1
Grennan AK (2011) Metallothioneins, a diverse protein family. Plant Physiol 155:1750–1751. https://doi.org/10.1104/pp.111.900407
Gu C-S, Liu L-Q, Deng Y-M, Zhu X-D, Huang S-Z, Lu X-Q (2015) The heterologous expression of the Iris lactea var chinensis type 2 metallothionein IlMT2b gene enhances copper tolerance in Arabidopsis thaliana. Bull Environ Contam Toxicol 94:247–253. https://doi.org/10.1007/s00128-014-1444-x
Gul I, Manzoor M, Silvestre J, Rizwan M, Hina K, Kallerhoff J, Arshad M (2019) EDTA-assisted phytoextraction of lead and cadmium by Pelargonium cultivars grown on spiked soil. Int J Phytoremediat 21:101–110. https://doi.org/10.1080/15226514.2018.1474441
Gullner G, Komives T, Rennenberg H (2001) Enhanced tolerance of transgenic poplar plants overexpressing gamma-glutamylcysteine synthetase towards chloroacetanilide herbicides. J Exp Bot 52:971–979. https://doi.org/10.1093/jexbot/52.358.971
Gunarathne V, Mayakaduwa S, Ashiq A, Weerakoon SR, Biswas JK, Vithanage M (2019) Transgenic plants: benefits, applications, and potential risks in phytoremediation. Transgenic plant technology for remediation of toxic metals and metalloids. Elsevier, Amsterdam, pp 89–102
Gurlebeck D, Thieme F, Bonas U (2006) Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. J Plant Physiol 163:233–255. https://doi.org/10.1016/j.jplph.2005.11.011
Han K-H, Meilan R, Ma C, Strauss SH (2000) An Agrobacterium tumefaciens transformation protocol effective on a variety of cottonwood hybrids (genus Populus). Plant Cell Rep 19:315–320. https://doi.org/10.1007/s002990050019
Hanikenne M (2003) Chlamydomonas reinhardtii as a eukaryotic photosynthetic model for studies of heavy metal homeostasis and tolerance. New Phytol 159:331–340. https://doi.org/10.1046/j.1469-8137.2003.00788.x
Hansen D, Duda PJ, Zayed A, Terry N (1998) Selenium removal by constructed wetlands: role of biological volatilization. Environ Sci Technol 32:591–597. https://doi.org/10.1021/es970502l
Hassan Z, Aarts MGM (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72:53–63. https://doi.org/10.1016/j.envexpbot.2010.04.003
He Z, Shentu J, Yang X, Baligar VC, Zhang T, Stoffella PJ (2015) Heavy metal contamination of soils: sources, indicators, and assessment. J Environ Indic 9:17–18
He YJ et al (2017) Metabolism of Ibuprofen by Phragmites australis: uptake and phytodegradation. Environ Sci Technol 51:4576–4584. https://doi.org/10.1021/acs.est.7b00458
He X et al (2019) Polyaspartate and liquid amino acid fertilizer are appropriate alternatives for promoting the phytoextraction of cadmium and lead in Solanum nigrum L. Chemosphere 237:124483. https://doi.org/10.1016/j.chemosphere.2019.124483
Headley JV, Peru KM, Du JL, Gurprasad N, McMartin DW (2008) Evaluation of the apparent phytodegradation of pentachlorophenol by Chlorella pyrenoidosa. J Environ Sci Health Part A Toxic/Hazard Subst Environ Eng 43:361–364. https://doi.org/10.1080/10934520701795491
Heckenroth A, Rabier J, Dutoit T, Torre F, Prudent P, Laffont-Schwob I (2016) Selection of native plants with phytoremediation potential for highly contaminated Mediterranean soil restoration: tools for a non-destructive and integrative approach. J Environ Manag 183:850–863
Henry JR (2000) An overview of the phytoremediation of lead and mercury. Office of Solid Waste and Emergency Response, Technology Innovation Office, Washington, DC
Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66:2901–2911. https://doi.org/10.1093/jxb/erv063
Hernández A, Loera N, Contreras M, Fischer L, Sánchez D (2019) Comparison between Lactuca sativa L and Lolium perenne: phytoextraction capacity of Ni, Fe, and Co from galvanoplastic industry. Energy technology 2019. Springer, Cham, pp 137–147
Higuchi K, Kanazawa K, Nishizawa N-K, Chino M, Mori S (1994) Purification and characterization of nicotianamine synthase from Fe-deficient barley roots. Plant Soil 165:173–179. https://doi.org/10.1007/bf00008059
Hoffman FO, Garten CT, Huckabee JW, Lucas DM (1982) Interception and retention of technetium by vegetation and soil. J Environ Qual 11:134–141. https://doi.org/10.2134/jeq1982.00472425001100010030x
Hooda V (2007) Phytoremediation of toxic metals from soil and waste water. J Environ Biol 28:367–376
Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:37. https://doi.org/10.1155/2012/872875
Huang G-Y, Wang Y-S (2009) Expression analysis of type 2 metallothionein gene in mangrove species (Bruguiera gymnorrhiza) under heavy metal stress. Chemosphere 77:1026–1029. https://doi.org/10.1016/j.chemosphere.2009.07.073
Huang X et al (2019) Insights into heavy metals leakage in chelator-induced phytoextraction of Pb- and Tl-contaminated soil. Int J Environ Res Public Health 16:1328
Jabeen R, Ahmad A, Iqbal M (2009) Phytoremediation of heavy metals: physiological and molecular mechanisms. Bot Rev 75:339–364. https://doi.org/10.1007/s12229-009-9036-x
Jadia CD, Fulekar MH (2008) Phytoremediation: the application of vermicompost to remove zinc, cadmium, copper, nickel and lead by sunflower plant. Environ Eng Manag J 7:547–558
Jadia CD, Fulekar MH (2009) Phytoremediation of heavy metals: recent techniques. Afr J Biotechnol 8:921–928
Jan AT, Ali A, Rizwanul Haq QM (2015) Chapter 3-Phytoremediation: a promising strategy on the crossroads of remediation. In: Hakeem KR, Sabir M, Öztürk M, Mermut AR (eds) Soil remediation and plants. Academic Press, San Diego, pp 63–84. https://doi.org/10.1016/B978-0-12-799937-1.00003-6
Jha P, Jobby R, Desai NS (2016) Remediation of textile azo dye acid red 114 by hairy roots of Ipomoea carnea Jacq. and assessment of degraded dye toxicity with human keratinocyte cell line. J Hazard Mater 311:158–167. https://doi.org/10.1016/j.jhazmat.2016.02.058
Jiali H, Hong L, Chaofeng M, Yanli Z, Andrea P, Heinz R, Xingqi C, Zhi-Bin L (2015) Overexpression of bacterial γ-glutamylcysteine synthetase mediates changes in cadmium influx, allocation and detoxification in poplar. New Phytol 205:240–254. https://doi.org/10.1111/nph.13013
Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31:233–239. https://doi.org/10.1038/nbt.2508
Jin S, Xu C, Li G, Sun D, Li Y, Wang X, Liu S (2017) Functional characterization of a type 2 metallothionein gene, SsMT2, from alkaline-tolerant Suaeda salsa. Sci Rep UK 7:17914. https://doi.org/10.1038/s41598-017-18263-4
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821. https://doi.org/10.1126/science.1225829
Joung JK, Sander JD (2013) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14:49–55. https://doi.org/10.1038/nrm3486
Kado CI (2014) Historical account on gaining insights on the mechanism of crown gall tumorigenesis induced by Agrobacterium tumefaciens. Front Microbiol 5:340–340. https://doi.org/10.3389/fmicb.2014.00340
Kagalkar AN, Jadhav MU, Bapat VA, Govindwar SP (2011) Phytodegradation of the triphenylmethane dye Malachite Green mediated by cell suspension cultures of Blumea malcolmii Hook. Biores Technol 102:10312–10318. https://doi.org/10.1016/j.biortech.2011.08.101
Kang JW (2014) Removing environmental organic pollutants with bioremediation and phytoremediation. Biotechnol Lett 36:1129–1139
Karenlampi S, Schat H, Vangronsveld J, Verkleij JA, van der Lelie D, Mergeay M, Tervahauta AI (2000) Genetic engineering in the improvement of plants for phytoremediation of metal polluted soils. Environ Pollut (Barking, Essex: 1987) 107:225–231
Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:648–651. https://doi.org/10.1126/science.1144956
Keeran NS, Ganesan G, Parida AK (2017) A novel heavy metal ATPase peptide from prosopis juliflora is involved in metal uptake in yeast and tobacco. Transgenic Res 26:247–261
Kelishadi R, Moeini R, Poursafa P, Farajian S, Yousefy H, Okhovat-Souraki AA (2014) Independent association between air pollutants and vitamin D deficiency in young children in Isfahan, Iran. Paediatr Int Child Health 34:50–55. https://doi.org/10.1179/2046905513y.0000000080
Khalid N, Noman A, Aqeel M, Masood A, Tufail A (2019) Phytoremediation potential of Xanthium strumarium for heavy metals contaminated soils at roadsides. Int J Environ Sci Technol 16:2091–2100. https://doi.org/10.1007/s13762-018-1825-5
Khan K (2010) Gene transfer technologies and their applications: roles in human diseases. Asian J Exp Biol Sci 1:208–221
Kikkert JR, Vidal JR, Reisch BI (2004) Stable transformation of plant cells by particle bombardment/biolistics. In: Peña L (ed) Transgenic plants: methods and protocols. Humana Press, Totowa, pp 61–78. https://doi.org/10.1385/1-59259-827-7:061
Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44
Kotnik T, Frey W, Sack M, Haberl Meglic S, Peterka M, Miklavcic D (2015) Electroporation-based applications in biotechnology. Trends Biotechnol 33:480–488. https://doi.org/10.1016/j.tibtech.2015.06.002
Kotnik T, Rems L, Tarek M, Miklavcic D (2019) Membrane electroporation and electropermeabilization: mechanisms and models. In: Dill KA (ed) Annual review of biophysics, vol 48. Annual Reviews, Palo Alto, pp 63–91. https://doi.org/10.1146/annurev-biophys-052118-115451
Kotoky R, Pandey P (2019) Rhizosphere mediated biodegradation of benzo(A)pyrene by surfactin producing soil bacilli applied through Melia azadirachta rhizosphere. Int J Phytoremediat. https://doi.org/10.1080/15226514.2019.1663486
Koutavarapu R et al (2020) ZnO nanosheets-decorated Bi2WO6 nanolayers as efficient photocatalysts for the removal of toxic environmental pollutants and photoelectrochemical solar water oxidation. J Environ Manag 265:110504. https://doi.org/10.1016/j.jenvman.2020.110504
Kramer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272. https://doi.org/10.1016/j.febslet.2007.04.010
Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51. https://doi.org/10.1007/s11738-010-0581-z
Krzeslowska M et al (2016) Pectinous cell wall thickenings formation—a common defense strategy of plants to cope with Pb. Environ Pollut (Barking, Essex: 1987) 214:354–361. https://doi.org/10.1016/j.envpol.2016.04.019
Kshirsagar S, Aery NC (2007) Phytostabilization of mine waste: growth and physiological responses of Vigna unguiculata (L.) Walp. J Environ Biol 28:651–654
Kühnlenz T, Westphal L, Schmidt H, Scheel D, Clemens S (2015) Expression of Caenorhabditis elegans PCS in the AtPCS1-deficient Arabidopsis thaliana cad1-3 mutant separates the metal tolerance and non-host resistance functions of phytochelatin synthases. Plant Cell Environ 38:2239–2247. https://doi.org/10.1111/pce.12534
Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact 17:6–15. https://doi.org/10.1094/mpmi.2004.17.1.6
Kumar S, Trivedi PK (2016) Chapter 25-Heavy metal stress signaling in plants. In: Ahmad P (ed) Plant metal interaction. Elsevier, Amsterdam, pp 585–603. https://doi.org/10.1016/B978-0-12-803158-2.00025-4
Kumar R et al (2016) Chapter 13-Detoxification and tolerance of heavy metals in plants. In: Ahmad P (ed) Plant metal interaction. Elsevier, Amsterdam, pp 335–359. https://doi.org/10.1016/B978-0-12-803158-2.00013-8
Kumar N, Jeena N, Kumar N, Gangola S, Singh H (2019) Chapter 15-Phytoremediation facilitating enzymes: an enzymatic approach for enhancing remediation process. In: Bhatt P (ed) Smart bioremediation technologies. Academic Press, New York, pp 289–306. https://doi.org/10.1016/B978-0-12-818307-6.00015-9
Kvesitadze G, Khatisashvili G, Sadunishvili T, Ramsden JJ (2006) Uptake, translocation and effects of contaminants in plants. In: Biochemical mechanisms of detoxification in higher plants: basis of phytoremediation. Springer, Berlin, pp 55–102. https://doi.org/10.1007/3-540-28997-6_2
Latef AAA (2013) Growth and some physiological activities of pepper (Capsicum annuum L.) in response to cadmium stress and mycorrhizal symbiosis. J Agric Sci Technol Iran 15:1437–1448
Le Faucheur S, Behra R, Sigg L (2005) Phytochelatin induction, cadmium accumulation, and algal sensitivity to free cadmium ion in Scenedesmus vacuolatus. Environ Toxicol Chem 24:1731–1737
Le Gall H, Philippe F, Domon J-M, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4:112
LeDuc DL et al (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and Indian mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383. https://doi.org/10.1104/pp.103.026989
Lee J-E, Ezura H (2016) Genome-editing technologies and their use in tomato. In: Ezura H, Ariizumi T, Garcia-Mas J, Rose J (eds) Functional genomics and biotechnology in Solanaceae and Cucurbitaceae crops. Springer, Berlin, pp 239–250. https://doi.org/10.1007/978-3-662-48535-4_14
Leigh MB, Fletcher JS, Fu X, Schmitz FJ (2002) Root turnover: an important source of microbial substrates in rhizosphere remediation of recalcitrant contaminants. Environ Sci Technol 36:1579–1583
Leung HM, Ye ZH, Wong MH (2007) Survival strategies of plants associated with arbuscular mycorrhizal fungi on toxic mine tailings. Chemosphere 66:905–915. https://doi.org/10.1016/j.chemosphere.2006.06.037
Li Y, Wei GY, Chen J (2004) Glutathione: a review on biotechnological production. Appl Microbiol Biot 66:233–242
Li XX, Zhang X, Wang XL, Cui ZJ (2019) Phytoremediation of multi-metal contaminated mine tailings with Solanum nigrum L. and biochar/attapulgite amendments. Ecotoxicol Environ Saf 180:517–525. https://doi.org/10.1016/j.ecoenv.2019.05.033
Liedschulte V, Wachter A, An ZG, Rausch T (2010) Exploiting plants for glutathione (GSH) production: uncoupling GSH synthesis from cellular controls results in unprecedented GSH accumulation. Plant Biotechnol J 8:807–820
Lin Z-Q, Schemenauer RS, Cervinka V, Zayed A, Lee A, Terry N (2000) Selenium volatilization from a soil—plant system for the remediation of contaminated water and soil in the San Joaquin Valley. J Environ Qual 29:1048–1056. https://doi.org/10.2134/jeq2000.00472425002900040003x
Lin CH, Lerch RN, Kremer RJ, Garrett HE (2011) Stimulated rhizodegradation of atrazine by selected plant species. J Environ Qual 40:1113–1121. https://doi.org/10.2134/jeq2010.0440
Liu D, Mao Z, An Z, Ma L, Lu Z (2013) Significant improved Escherichia coli tolerant to Cd2+, Zn2+ and Cu2+ expressing Streptococcus thermophilus StGCS-GS, compared to Arabidopsis thaliana AtGCS and AtGS. Annu Microbiol 64:961–967
Liu D, An Z, Mao Z, Ma L, Lu Z (2015a) Enhanced Heavy Metal Tolerance and Accumulation by Transgenic Sugar Beets Expressing Streptococcus thermophilus StGCS-GS in the Presence of Cd, Zn and Cu Alone or in Combination. Plos One 10:e0128824. https://doi.org/10.1371/journal.pone.0128824
Liu J, Shi X, Qian M, Zheng L, Lian C, Xia Y, Shen Z (2015b) Copper-induced hydrogen peroxide upregulation of a metallothionein gene, OsMT2c, from Oryza sativa L. confers copper tolerance in Arabidopsis thaliana. J Hazard Mater 294:99–108. https://doi.org/10.1016/j.jhazmat.2015.03.060
Liu P, Cai W-J, Yu L, Yuan B-F, Feng Y-Q (2015c) Determination of phytochelatins in rice by stable isotope labeling coupled with liquid chromatography-mass spectrometry. J Agric Food Chem 63:5935–5942. https://doi.org/10.1021/acs.jafc.5b01797
Liu LW, Li W, Song WP, Guo MX (2018) Remediation techniques for heavy metal-contaminated soils: principles and applicability. Sci Total Environ 633:206–219
Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A (2018) Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants (vol 8, 1897, 2017). Front Plant Sci. https://doi.org/10.3389/fpls.2018.00391
Lombi E, Tearall KL, Howarth JR, Zhao F-J, Hawkesford MJ, McGrath SP (2002) Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 128:1359–1367. https://doi.org/10.1104/pp.010731
Lu H, Zhang Y, Liu B, Liu J, Ye J, Yan C (2011) Rhizodegradation gradients of phenanthrene and pyrene in sediment of mangrove (Kandelia candel (L.) Druce). J Hazard Mater 196:263–269. https://doi.org/10.1016/j.jhazmat.2011.09.031
Lucero ME, Mueller W, Hubstenberger J, Phillips GC, O’Connell MA (1999) Tolerance to nitrogenous explosives and metabolism of TNT by cell suspensions of Datura innoxia. In Vitro Cell Dev Biol Plant 35:480–486. https://doi.org/10.1007/s11627-999-0072-3
Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13. https://doi.org/10.1016/j.envexpbot.2009.10.011
Magalhães MOL, Amaral Sobrinho NMBd, Santos FSd, Mazur N (2011) Potencial de duas espécies de eucalipto na fitoestabilização de solo contaminado com zinco. Rev Ciênc Agron 42:805–812
Makhzoum AB, Sharma P, Bernards MA, Trémouillaux-Guiller J (2013) Hairy roots: an ideal platform for transgenic plant production and other promising applications. In: Gang DR (ed) Phytochemicals, plant growth, and the environment. Springer, New York, pp 95–142. https://doi.org/10.1007/978-1-4614-4066-6_6
Mali P et al (2013) RNA-guided human genome engineering via Cas9. Science (New York, NY) 339:823–826. https://doi.org/10.1126/science.1232033
Malik B, Pirzadah TB, Tahir I, Dar TuH, Rehman RU (2015) Chapter 6-Recent trends and approaches in phytoremediation. In: Hakeem KR, Sabir M, Öztürk M, Mermut AR (eds) Soil remediation and plants. Academic Press, San Diego, pp 131–146. https://doi.org/10.1016/B978-0-12-799937-1.00006-1
Manzoor M et al (2019) Metal tolerant bacteria enhanced phytoextraction of lead by two accumulator ornamental species. Chemosphere 227:561–569. https://doi.org/10.1016/j.chemosphere.2019.04.093
Maqbool F et al (2012) Rhizodegradation of petroleum hydrocarbons by Sesbania cannabina in bioaugmented soil with free and immobilized consortium. J Hazard Mater 237–238:262–269. https://doi.org/10.1016/j.jhazmat.2012.08.038
Mari S, Lebrun M (2006) Metal immobilization: where and how? In: Tamas MJ, Martinoia E (eds) Molecular biology of metal homeostasis and detoxification: from microbes to man. Springer, Berlin, pp 273–298. https://doi.org/10.1007/4735_103
Marois E, Van den Ackerveken G, Bonas U (2002) The xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol Plant Microbe Interact MPMI 15:637–646. https://doi.org/10.1094/mpmi.2002.15.7.637
Márquez-Escobar VA, González-Ortega O, Rosales-Mendoza S (2018) Plant transformation strategies. In: MacDonald J (ed) Prospects of plant-based vaccines in veterinary medicine. Springer, Cham, pp 23–42. https://doi.org/10.1007/978-3-319-90137-4_2
Maser P et al (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667
Mendel R, Hänsch R (2017) Gene transfer to higher plants. In: Singh RP, Singh US (eds) Molecular methods in plant pathology. CRC Press, Boca Raton, pp 189–202. https://doi.org/10.1201/9780203746523-14
Meyer C-L et al (2015) Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri. J Exp Bot 66:3215–3227. https://doi.org/10.1093/jxb/erv144
Mishra S, Dubey RS (2006) Heavy metal uptake and detoxification mechanisms in plants. Int J Agric Res 1:122–141. https://doi.org/10.3923/ijar.2006.122.141
Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MNV (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44:25–37. https://doi.org/10.1016/j.plaphy.2006.01.007
Misra S, Gedamu L (1989) Heavy metal tolerant transgenic Brassica napus L and Nicotiana tabacum L plants. Theor Appl Genet 78:161–168. https://doi.org/10.1007/bf00288793
Moon JY, Belloeil C, Ianna ML, Shin R (2019) Arabidopsis CNGC family members contribute to heavy metal ion uptake in plants. Int J Mol Sci 20:413
Mosoarca G, Vancea C, Popa S, Boran S (2018) Adsorption, bioaccumulation and kinetics parameters of the phytoremediation of cobalt from wastewater using Elodea canadensis. Bull Environ Contam Toxicol 100:733–739. https://doi.org/10.1007/s00128-018-2327-3
Mudgal V, Madaan N, Mudgal A (2010) Heavy metals in plants: phytoremediation: plants used to remediate heavy metal pollution. Agric Biol J N Am 1:40–46
Muthusaravanan S et al (2018) Phytoremediation of heavy metals: mechanisms, methods and enhancements. Environ Chem Lett 16:1339–1359. https://doi.org/10.1007/s10311-018-0762-3
Myśliwa-Kurdziel B, Prasad MNV, Strzałtka K (2004) Photosynthesis in heavy metal stressed plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystems. Springer, Berlin, pp 146–181. https://doi.org/10.1007/978-3-662-07743-6_6
Nahar N, Rahman A, Nawani NN, Ghosh S, Mandal A (2017) Phytoremediation of arsenic from the contaminated soil using transgenic tobacco plants expressing ACR2 gene of Arabidopsis thaliana. J Plant Physiol 218:121–126
Nanasato Y et al (2016) Biodegradation of gamma-hexachlorocyclohexane by transgenic hairy root cultures of Cucurbita moschata that accumulate recombinant bacterial LinA. Plant Cell Rep 35:1963–1974. https://doi.org/10.1007/s00299-016-2011-1
Nedelkoska TV, Doran PM (2000) Hyperaccumulation of cadmium by hairy roots of Thlaspi caerulescens. Biotechnol Bioeng 67:607–615
Nehnevajova E, Ramireddy E, Stolz A, Gerdemann-Knörck M, Novák O, Strnad M, Schmülling T (2019) Root enhancement in cytokinin-deficient oilseed rape causes leaf mineral enrichment, increases the chlorophyll concentration under nutrient limitation and enhances the phytoremediation capacity. BMC Plant Biol 19:83. https://doi.org/10.1186/s12870-019-1657-6
Nguemte PM, Wafo GVD, Djocgoue PF, Noumsi IMK, Ngnien AW (2018) Potentialities of six plant species on phytoremediation attempts of fuel oil-contaminated soils. Water Air Soil Pollut 229:18. https://doi.org/10.1007/s11270-018-3738-9
Ning Y, Liu N, Song Y, Luo J, Li T (2019) Enhancement of phytoextraction of Pb by compounded activation agent derived from fruit residue. Int J Phytoremediat. https://doi.org/10.1080/15226514.2019.1633266
Olson PE, Fletcher JS (2000) Ecological recovery of vegetation at a former industrial sludge basin and its implications to phytoremediation. Environ Sci Pollut Res 7:195–204. https://doi.org/10.1007/bf02987348
Osma E, Ozyigit II, Leblebici Z, Demir G, Serin M (2012) Determination of heavy metal concentrations in tomato (Lycopersicon esculentum Miller) grown in different station types. Rom Biotechnol Lett 17:6962–6974
Ozturk A, Yarci C, Ozyigit II (2017) Assessment of heavy metal pollution in Istanbul using plant (Celtis australis L.) and soil assays. Biotechnol Biotechnol Equip 31:948–954. https://doi.org/10.1080/13102818.2017.1353922
Ozyigit II (2012) Agrobacterium tumefaciens and its use in plant biotechnology. In: Ashraf M, Öztürk M, Ahmad MSA, Aksoy A (eds) Crop production for agricultural improvement. Springer, Dordrecht, pp 317–361. https://doi.org/10.1007/978-94-007-4116-4_12
Ozyigit II (2020) Gene transfer to plants by electroporation: methods and applications. Mol Biol Rep 47:3195–3210. https://doi.org/10.1007/s11033-020-05343-4
Ozyigit II, Dogan I (2015) Chapter 9-Plant–microbe interactions in phytoremediation. In: Hakeem KR, Sabir M, Öztürk M, Mermut AR (eds) Soil remediation and plants. Academic Press, San Diego, pp 255–285. https://doi.org/10.1016/B978-0-12-799937-1.00009-7
Ozyigit II, Dogan I, Artam Tarhan E (2013) Agrobacterium rhizogenes-mediated transformation and its biotechnological applications in crops. In: Hakeem KR, Ahmad P, Ozturk M (eds) Crop improvement: new approaches and modern techniques. Springer, Boston, pp 1–48. https://doi.org/10.1007/978-1-4614-7028-1_1
Ozyigit II, Dogan I, Igdelioglu S, Filiz E, Karadeniz S, Uzunova Z (2016) Screening of damage induced by lead (Pb) in rye (Secale cereale L.)—a genetic and physiological approach. Biotechnol Biotechnol Equip 30:489–496. https://doi.org/10.1080/13102818.2016.1151378
Ozyigit II, Uyanik OL, Sahin NR, Yalcin IE, Demir G (2017) Monitoring the pollution level in Istanbul coast of the Sea of Marmara using algal species Ulva lactuca L. Pol J Environ Stud 26:773–778. https://doi.org/10.15244/pjoes/66177
Ozyigit II, Yalcin B, Turan S, Saracoglu IA, Karadeniz S, Yalcin IE, Demir G (2018) Investigation of heavy metal level and mineral nutrient status in widely used medicinal plants’ leaves in Turkey: insights into health implications. Biol Trace Elem Res 182:387–406. https://doi.org/10.1007/s12011-017-1070-7
Pabo CO, Peisach E, Grant RA (2001) Design and selection of novel Cys2His2 zinc finger proteins. Annu Rev Biochem 70:313–340. https://doi.org/10.1146/annurev.biochem.70.1.313
Pal R, Rai JP (2010) Phytochelatins: peptides involved in heavy metal detoxification. Appl Biochem Biotechnol 160:945–963. https://doi.org/10.1007/s12010-009-8565-4
Pala Z, Shukla V, Alok A, Kudale S, Desai N (2016) Enhanced production of an anti-malarial compound artesunate by hairy root cultures and phytochemical analysis of Artemisia pallens Wall. 3 Biotech 6:182. https://doi.org/10.1007/s13205-016-0496-5
Pandey VC, Pandey DN, Singh N (2015) Sustainable phytoremediation based on naturally colonizing and economically valuable plants. J Clean Prod 86:37–39. https://doi.org/10.1016/j.jclepro.2014.08.030
Pandey AK, Gautam A, Dubey RS (2019) Transport and detoxification of metalloids in plants in relation to plant-metalloid tolerance Plant. Gene 17:100171. https://doi.org/10.1016/j.plgene.2019.100171
Pandotra P et al (2018) Plant-bacterial partnership: a major pollutants remediation approach. In: Oves M, Zain Khan M, Ismail IMI (eds) Modern age environmental problems and their remediation. Springer, Cham, pp 169–200. https://doi.org/10.1007/978-3-319-64501-8_10
Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136:3814–3823
Peer WA, Baxter IR, Richards EL, Freeman JL, Murphy AS (2006) Phytoremediation and hyperaccumulator plants. In: Tamas MJ, Martinoia E (eds) Molecular biology of metal homeostasis and detoxification: from microbes to man. Springer, Berlin, pp 299–340. https://doi.org/10.1007/4735_100
Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J Cell Mol Biol 32:539–548
Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39. https://doi.org/10.1146/annurev.arplant.56.032604.144214
Pilon-Smits EAH, de Souza MP, Hong G, Amini A, Bravo RC, Payabyab ST, Terry N (1999) Selenium volatilization and accumulation by twenty aquatic plant species. J Environ Qual 28:1011–1018. https://doi.org/10.2134/jeq1999.00472425002800030035x
Pitzschke A, Hirt H (2010) New insights into an old story: agrobacterium-induced tumour formation in plants by plant transformation. EMBO J 29:1021–1032. https://doi.org/10.1038/emboj.2010.8
Pivetz B (2001) Phytoremediation of contaminated soil and ground water at hazardous waste sites. U.S. Environmental Protection Agency, Washington, DC
Pratas J, Favas PJ, Paulo C, Rodrigues N, Prasad MN (2012) Uranium accumulation by aquatic plants from uranium-contaminated water in Central Portugal. Int J Phytoremediat 14:221–234. https://doi.org/10.1080/15226514.2011.587849
Qiu W, Song X, Han X, Liu M, Qiao G, Zhuo R (2018) Overexpression of sedum alfredii cinnamyl alcohol dehydrogenase increases the tolerance and accumulation of cadmium in arabidopsis. Environ Exp Bot 155:566–577. https://doi.org/10.1016/j.envexpbot.2018.08.003
Quig D (1998) Cysteine metabolism and metal toxicity. Altern Med Rev J Clin Ther 3:262–270
Rai PK (2019) Heavy metals/metalloids remediation from wastewater using free floating macrophytes of a natural wetland. Environ Technol Innov 15:100393. https://doi.org/10.1016/j.eti.2019.100393
Raina M et al (2018) Genetic engineering and environmental risk. In: Oves M, Zain Khan M, Ismail IMI (eds) Modern age environmental problems and their remediation. Springer, Cham, pp 69–82. https://doi.org/10.1007/978-3-319-64501-8_4
Raldugina GN et al (2018) Expression of rice OsMyb4 transcription factor improves tolerance to copper or zinc in canola plants. Biol Plant 62:511–520
Ramasahayam S, Jaligama S, Atwa SM, Salley JT, Thongdy M, Blaylock BL, Meyer SA (2017) Megakaryocyte expansion and macrophage infiltration in bone marrow of rats subchronically treated with MNX, N-nitroso environmental degradation product of munitions compound RDX (hexahydro-1,3,5-trinitro-1,3,5-triazine). J Appl Toxicol 37:913–921. https://doi.org/10.1002/jat.3439
Raskin I, Smith RD, Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8:221–226. https://doi.org/10.1016/S0958-1669(97)80106-1
Rauser WE (1995) Phytochelatins and related peptides (structure, biosynthesis, and function). Plant Physiol 109:1141–1149. https://doi.org/10.1104/pp.109.4.1141
Rea PA, Vatamaniuk OK, Rigden DJ (2004) Weeds, worms, and more. Papain’s long-lost cousin, phytochelatin synthase. Plant Physiol 136:2463–2474. https://doi.org/10.1104/pp.104.048579
Reddy CV, Reddy IN, Akkinepally B, Harish VVN, Reddy KR, Jaesool S (2019) Mn-doped ZrO2 nanoparticles prepared by a template-free method for electrochemical energy storage and abatement of dye degradation. Ceram Int 45:15298–15306. https://doi.org/10.1016/j.ceramint.2019.05.020
Reddy CV, Reddy IN, Harish VVN, Reddy KR, Shetti NP, Shim J, Aminabhavi TM (2020) Efficient removal of toxic organic dyes and photoelectrochemical properties of iron-doped zirconia nanoparticles. Chemosphere 239:124766. https://doi.org/10.1016/j.chemosphere.2019.124766
Robinson NJ, Tommey AM, Kuske C, Jackson PJ (1993) Plant metallothioneins. Biochem J 295:1–10
Roy SK et al (2017) Proteome characterization of copper stress responses in the roots of sorghum. Biometals 30:765–785. https://doi.org/10.1007/s10534-017-0045-7
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 USA 93:3182–3187. https://doi.org/10.1073/pnas.93.8.3182
Rui HY, Chen C, Zhang XX, Shen ZG, Zhang FQ (2016) Cd-induced oxidative stress and lignification in the roots of two Vicia sativa L. varieties with different Cd tolerances. J Hazard Mater 301:304–313
Ruppert L, Lin ZQ, Dixon RP, Johnson KA (2013) Assessment of solid phase microfiber extraction fibers for the monitoring of volatile organoarsinicals emitted from a plant-soil system. J Hazard Mater 262:1230–1236. https://doi.org/10.1016/j.jhazmat.2012.06.046
Saad RB, Hsouna AB, Saibi W, Hamed KB, Brini F, Ghneim-Herrera T (2018) A stress-associated protein, LmSAP, from the halophyte Lobularia maritima provides tolerance to heavy metals in tobacco through increased ROS scavenging and metal detoxification processes. J Plant Physiol 231:234–243. https://doi.org/10.1016/j.jplph.2018.09.019
Sabir M, Waraich EA, Hakeem KR, Öztürk M, Ahmad HR, Shahid M (2015) Chapter 4-Phytoremediation: mechanisms and adaptations. In: Hakeem KR, Sabir M, Öztürk M, Mermut AR (eds) Soil remediation and plants. Academic Press, San Diego, pp 85–105. https://doi.org/10.1016/B978-0-12-799937-1.00004-8
Saleh HM (2012) Water hyacinth for phytoremediation of radioactive waste simulate contaminated with cesium and cobalt radionuclides. Nucl Eng Des 242:425–432. https://doi.org/10.1016/j.nucengdes.2011.10.023
Saleh HM, Moussa HR, Mahmoud HH, El-Saied FA, Dawoud M, Abdel Wahed RS (2020) Potential of the submerged plant Myriophyllum spicatum for treatment of aquatic environments contaminated with stable or radioactive cobalt and cesium. Prog Nucl Energy 118:103147. https://doi.org/10.1016/j.pnucene.2019.103147
Salido AL, Hasty KL, Lim JM, Butcher DJ (2003) Phytoremediation of arsenic and lead in contaminated soil using Chinese brake ferns (Pteris vittata) and Indian mustard (Brassica juncea). Int J Phytoremediat 5:89–103. https://doi.org/10.1080/713610173
San Miguel A, Ravanel P, Raveton M (2013) A comparative study on the uptake and translocation of organochlorines by Phragmites australis. J Hazard Mater 244:60–69. https://doi.org/10.1016/j.jhazmat.2012.11.025
Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32:347–355. https://doi.org/10.1038/nbt.2842
Sangeeta M, Maiti SK (2010) Phytoremediation of metal enriched mine waste: a review. Am Eurasian J Agric Environ Sci 9:560–575
Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Sardesai N, Subramanyam S (2018) Agrobacterium: a genome-editing tool-delivery system. Curr Top Microbiol Immunol 418:463–488. https://doi.org/10.1007/82_2018_101
Sarwar N, Saifullah, Malhi SS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937
Sarwar N et al (2017) Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171:710–721. https://doi.org/10.1016/j.chemosphere.2016.12.116
Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, von Wiren N (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281:25532–25540. https://doi.org/10.1074/jbc.m601062200
Schiavon M, Pittarello M, Pilon-Smits EAH, Wirtz M, Hell R, Malagoli M (2012) Selenate and molybdate alter sulfate transport and assimilation in Brassica juncea L. Czern.: implications for phytoremediation. Environ Exp Bot 75:41–51
Schnoor JL, Licht LA, McCutcheon SC, Wolfe NL, Carreira LH (1995) Phytoremediation of organic and nutrient contaminants. Environ Sci Technol 29:318a–323a. https://doi.org/10.1021/es00007a747
Segal DJ (2002) The use of zinc finger peptides to study the role of specific factor binding sites in the chromatin environment. Methods (San Diego, Calif) 26:76–83. https://doi.org/10.1016/s1046-2023(02)00009-9
Seth CS (2012) A review on mechanisms of plant tolerance and role of transgenic plants in environmental clean-up. Bot Rev 78:32–62. https://doi.org/10.1007/s12229-011-9092-x
Shah K, Nongkynrih JM (2007) Metal hyperaccumulation and bioremediation. Biol Plant 51:618–634. https://doi.org/10.1007/s10535-007-0134-5
Shah K, Pathak L (2019) Chapter 15-Transgenic energy plants for phytoremediation of toxic metals and metalloids. In: Prasad MNV (ed) Transgenic plant technology for remediation of toxic metals and metalloids. Academic Press, New York, pp 319–340. https://doi.org/10.1016/B978-0-12-814389-6.00015-8
Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Rev Environ Contam Toxicol 232:1–44. https://doi.org/10.1007/978-3-319-06746-9_1
Shan Q, Wang Y, Li J, Gao C (2014) Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc 9:2395–2410. https://doi.org/10.1038/nprot.2014.157
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52
Sharma DC, Sharma CP (1996) Chromium uptake and toxicity effects on growth and metabolic activities in wheat, Triticum aestivum L. cv. UP 2003. Indian J Exp Biol 34:689–691
Sharma SS, Dietz K-J, Mimura T (2016) Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant Cell Environ 39:1112–1126. https://doi.org/10.1111/pce.12706
Shukla D, Trivedi PK, Nath P, Tuteja N (2016) Metallothioneins and phytochelatins: role and perspectives in heavy metal(loid)s stress tolerance in crop plants. In: Tuteja N, Gill SS (eds) Abiotic stress response in plants. Wiley, New York. https://doi.org/10.1002/9783527694570.ch12
Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436
Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci. https://doi.org/10.3389/fpls.2015.01143
Singh V, Pandey B, Suthar S (2019) Phytotoxicity and degradation of antibiotic ofloxacin in duckweed (Spirodela polyrhiza) system. Ecotoxicol Environ Saf 179:88–95. https://doi.org/10.1016/j.ecoenv.2019.04.018
Slater A, Scott NW, Fowler MR (2008) Plant biotechnology: the genetic manipulation of plants. Ann Bot 94:646
Solanki R, Dhankhar R (2011) Biochemical changes and adaptive strategies of plants under heavy metal stress. Biologia 66:195–204. https://doi.org/10.2478/s11756-011-0005-6
Soleimani M, Akbar S, Hajabbasi MA (2011) Enhancing phytoremediation efficiency in response to environmental pollution stress. In: Hemanth KN, Kambiranda V, Kambiranda D (eds) Plants and environment. IntechOpen, London. https://doi.org/10.5772/22267
Sorrentino MC, Capozzi F, Amitrano C, Giordano S, Arena C, Spagnuolo V (2018) Performance of three cardoon cultivars in an industrial heavy metal-contaminated soil: effects on morphology, cytology and photosynthesis. J Hazard Mater 351:131–137
Souza TDd, Borges AC, Braga AF, Veloso RW, Teixeira de Matos A (2019) Phytoremediation of arsenic-contaminated water by Lemna valdiviana: an optimization study. Chemosphere 234:402–408. https://doi.org/10.1016/j.chemosphere.2019.06.004
Subramanyam K, Subramanyam K, Sailaja KV, Srinivasulu M, Lakshmidevi K (2011) Highly efficient Agrobacterium-mediated transformation of banana cv. Rasthali (AAB) via sonication and vacuum infiltration. Plant Cell Rep 30:425–436. https://doi.org/10.1007/s00299-010-0996-4
Subramoni S, Nathoo N, Klimov E, Yuan Z-C (2014) Agrobacterium tumefaciens responses to plant-derived signaling molecules Front. Plant Sci 5:322–322. https://doi.org/10.3389/fpls.2014.00322
Sun J, Pan L, Tsang DCW, Zhan Y, Zhu L, Li X (2018a) Organic contamination and remediation in the agricultural soils of China: a critical review. Sci Total Environ 615:724–740. https://doi.org/10.1016/j.scitotenv.2017.09.271
Sun L et al (2018b) Overexpression of PtABCC1 contributes to mercury tolerance and accumulation in Arabidopsis and poplar. Biochem Biophys Res Commun 497:997–1002. https://doi.org/10.1016/j.bbrc.2018.02.133
Surriya O, Sarah Saleem S, Waqar K, Gul Kazi A (2015) Chapter 1-Phytoremediation of soils: prospects and challenges. In: Hakeem KR, Sabir M, Öztürk M, Mermut AR (eds) Soil remediation and plants. Academic Press, San Diego, pp 1–36. https://doi.org/10.1016/B978-0-12-799937-1.00001-2
Susarla S, Medina VF, McCutcheon SC (2002) Phytoremediation: an ecological solution to organic chemical contamination. Ecol Eng 18:647–658
Takahashi R, Bashir K, Ishimaru Y, Nishizawa NK, Nakanishi H (2012) The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7:1605–1607. https://doi.org/10.4161/psb.22454
Tavangar T, Karimi M, Rezakazemi M, Reddy KR, Aminabhavi TM (2020) Textile waste, dyes/inorganic salts separation of cerium oxide-loaded loose nanofiltration polyethersulfone membranes. Chem Eng J 385:123787. https://doi.org/10.1016/j.cej.2019.123787
Thakur R, Shankar J (2017) Strategies for gene expression in prokaryotic and eukaryotic system. In: Kalia VC, Saini AK (eds) Metabolic engineering for bioactive compounds: strategies and processes. Springer, Singapore, pp 223–247. https://doi.org/10.1007/978-981-10-5511-9_11
Thomas TJ, Kulkarni GD, Greenfield NJ, Shirahata A, Thomas T (1996) Structural specificity effects of trivalent polyamine analogues on the stabilization and conformational plasticity of triplex DNA. Biochem J 319(Pt 2):591–599. https://doi.org/10.1042/bj3190591
Tommasini R, Vogt E, Fromenteau M, Hörtensteiner S, Matile P, Amrhein N, Martinoia E (1998) An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J 13:773–780. https://doi.org/10.1046/j.1365-313X.1998.00076.x
Tue NM et al (2014) Dioxin-related compounds in breast milk of women from Vietnamese e-waste recycling sites: levels, toxic equivalents and relevance of non-dietary exposure. Ecotoxicol Environ Saf 106:220–225
Uhlik O, Wald J, Strejcek M, Musilova L, Ridl J et al (2012) Identification of bacteria utilizing biphenyl, benzoate, and naphthalene in long-term contaminated soil. Plos One 7:e40653. https://doi.org/10.1371/journal.pone.0040653
Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. A review. Environ Chem Lett 8:1–17. https://doi.org/10.1007/s10311-009-0268-0
Van Aken B (2008) Transgenic plants for phytoremediation: helping nature to clean up environmental pollution. Trends Biotechnol 26:225–227. https://doi.org/10.1016/j.tibtech.2008.02.001
Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206. https://doi.org/10.1111/j.1365-3040.1990.tb01304.x
Van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JAC, Hooykaas PJJ (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 119:1047–1056. https://doi.org/10.1104/pp.119.3.1047
Van Huysen T, Abdel-Ghany S, Hale KL, LeDuc D, Terry N, Pilon-Smits EA (2003) Overexpression of cystathionine-gamma-synthase enhances selenium volatilization in Brassica juncea. Planta 218:71–78. https://doi.org/10.1007/s00425-003-1070-z
Vatamaniuk OK, Bucher EA, Ward JT, Rea PA (2001) A new pathway for heavy metal detoxification in animals: phytochelatin synthase is required for Cd tolerance in Caenorhabditis elegans. J Biol Chem 276:20817–20820. https://doi.org/10.1074/jbc.C100152200
Vatamaniuk OK, Mari S, Lang A, Chalasani S, Demkiv LO, Rea PA (2004) Phytochelatin synthase, a dipeptidyltransferase that undergoes multisite acylation with γ-glutamylcysteine during catalysis: stoichiometric and site-directed mutagenic analysis of Arabidopsis thaliana PCS1-catalyzed phytochelatin synthesis. J Biol Chem 279:22449–22460. https://doi.org/10.1074/jbc.m313142200
Verkleij JAC, Sneller FEC, Schat H (2003) Metallothioneins and phytochelatins: ecophysiological aspects. In: Abrol YP, Ahmad A (eds) Sulphur in plants. Springer, Dordrecht, pp 163–176. https://doi.org/10.1007/978-94-017-0289-8_9
Vetterlein D, Szegedi K, Ackermann J, Mattusch J, Neue HU, Tanneberg H, Jahn R (2007) Competitive mobilization of phosphate and arsenate associated with goethite by root activity. J Environ Qual 36:1811–1820
Vijgen J et al (2011) Hexachlorocyclohexane (HCH) as new stockholm convention POPs-a global perspective on the management of Lindane and its waste isomers. Environ Sci Pollut Res 18:152–162
Viktorova J et al (2017) Native phytoremediation potential of Urtica dioica for removal of PCBs and heavy metals can be improved by genetic manipulations using constitutive CaMV 35S promoter (vol 11, e0167927, 2016). Plos One 12:e0187053
Vladimirov IA, Matveeva TV, Lutova LA (2015) Opine biosynthesis and catabolism genes of Agrobacterium tumefaciens and Agrobacterium rhizogenes. Russ J Genet 51:121–129. https://doi.org/10.1134/s1022795415020167
Wan X, Lei M, Chen T (2016) Cost–benefit calculation of phytoremediation technology for heavy-metal-contaminated soil. Sci Total Environ 563:796–802. https://doi.org/10.1016/j.scitotenv.2015.12.080
Wang FZ, Chen MX, Yu LJ, Xie LJ, Yuan LB, Qi H, Xiao M, Guo WX, Chen Z, Yi KK, Zhang JH, Qiu RL, Shu WS, Xiao S, Chen QF (2017) Osarm1, an r2r3 myb transcription factor, is involved in regulation of the response to arsenic stress in rice. Front Plant Sci 8:16. https://doi.org/10.3389/fpls.2017.01868
Wang XT, Zhi JK, Liu XR, Zhang H, Liu HB, Xu JC (2018) Transgenic tobacco plants expressing a P1B-ATPase gene from Populus tomentosa Carr. (PtoHMA5) demonstrate improved cadmium transport. Int J Biol Macromol 113:655–661
Wang W-W, Ke Cheng L, Hao JW, Guan X, Tian X-J (2019) Phytoextraction of initial cutting of Salix matsudana for Cd and Cu. Int J Phytoremediat 21:84–91. https://doi.org/10.1080/15226514.2016.1183574
Wei X, Lyu S, Yu Y, Wang Z, Liu H, Pan D, Chen J (2017) Phylloremediation of air pollutants: exploiting the potential of plant leaves and leaf-associated microbes. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01318
White PM Jr, Wolf DC, Thoma GJ, Reynolds CM (2003) Influence of organic and inorganic soil amendments on plant growth in crude oil-contaminated soil. Int J Phytoremediat 5:381–397. https://doi.org/10.1080/15226510309359044
Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331–338. https://doi.org/10.1038/nature10886
Wiessner A, Kappelmeyer U, Kaestner M, Schultze-Nobre L, Kuschk P (2013) Response of ammonium removal to growth and transpiration of Juncus effusus during the treatment of artificial sewage in laboratory-scale wetlands. Water Res 47:4265–4273. https://doi.org/10.1016/j.watres.2013.04.045
Williams LE, Mills RF (2005) P(1B)-ATPases—an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502. https://doi.org/10.1016/j.tplants.2005.08.008
Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochem Biophys Acta 1465:104–126
Xia Y, Liu J, Wang Y, Zhang XX, Shen ZG, Hu ZB (2018) Ectopic expression of Vicia sativa Caffeoyl-CoA O-methyltransferase (VsCCoAOMT) increases the uptake and tolerance of cadmium in Arabidopsis. Environ Exp Bot 145:47–53
Yadav A, Raj A, Purchase D, Ferreira LFR, Saratale GD, Bharagava RN (2019) Phytotoxicity, cytotoxicity and genotoxicity evaluation of organic and inorganic pollutants rich tannery wastewater from a common effluent treatment plant (CETP) in Unnao district, India using Vigna radiata and Allium cepa. Chemosphere 224:324–332. https://doi.org/10.1016/j.chemosphere.2019.02.124
Yang B, Zhu W, Johnson LB, White FF (2000) The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proc Natl Acad Sci USA 97:9807–9812. https://doi.org/10.1073/pnas.170286897
Yang X, Feng Y, He Z, Stoffella PJ (2005a) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol Organ Soc Miner Trace Elem (GMS) 18:339–353. https://doi.org/10.1016/j.jtemb.2005.02.007
Yang X, Feng Y, He ZL, Stoffella PJ (2005b) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol 18:339–353. https://doi.org/10.1016/j.jtemb.2005.02.007
Yang WD, Yang Y, Ding ZL, Yang XE, Zhao FL, Zhu ZQ (2019a) Uptake and accumulation of cadmium in flooded versus non-flooded Salix genotypes: implications for phytoremediation. Ecol Eng 136:79–88. https://doi.org/10.1016/j.ecoleng.2019.06.001
Yang Y et al (2019b) Phytoextraction of Cd from a contaminated soil by tobacco and safe use of its metal-enriched biomass. J Hazard Mater 363:385–393. https://doi.org/10.1016/j.jhazmat.2018.09.093
Yifru DD, Nzengung VA (2008) Organic carbon biostimulates rapid rhizodegradation of perchlorate. Environ Toxicol Chem 27:2419–2426. https://doi.org/10.1897/08-008.1
Yin L, Wang S, Chen D, Deng X, Cao B, Qi L (2016) Silicon-moderated K-deficiency-induced leaf chlorosis by decreasing putrescine accumulation in sorghum. Ann Bot 118:305–315. https://doi.org/10.1093/aob/mcw111
Yuan H-M, Liu W-C, Jin Y, Lu Y-T (2013) Role of ROS and auxin in plant response to metal-mediated stress. Plant Signal Behav 8:e24671–e24671. https://doi.org/10.4161/psb.24671
Yuksek A (2018) İslam hukukunna göre helal gıda ve GDO’lu ürünler (Genetiği değiştirilmiş organizmalar)
Yusuf M, Fariduddin Q, Hayat S, Ahmad A (2011) Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86:1–17
Zamani J, Hajabbasi MA, Mosaddeghi MR, Soleimani M, Shirvani M, Schulin R (2018) Experimentation on degradation of petroleum in contaminated soils in the root zone of maize (Zea mays L.) inoculated with Piriformospora indica. Soil Sediment Contam 27:13–30. https://doi.org/10.1080/15320383.2018.1422693
Zehra A et al (2020) Assessment of sunflower germplasm for phytoremediation of lead-polluted soil and production of seed oil and seed meal for human and animal consumption. J Environ Sci 87:24–38. https://doi.org/10.1016/j.jes.2019.05.031
Zenk MH (1996) Heavy metal detoxification in higher plants—a review. Gene 179:21–30
Zhan J, Zhang QP, Li TX, Yu HY, Zhang XZ, Huang HG (2019) Effects of NTA on Pb phytostabilization efficiency of Athyrium wardii (Hook.) grown in a Pb-contaminated soil. J Soil Sediment 19:3576–3584. https://doi.org/10.1007/s11368-019-02308-4
Zhang HM et al (1988) Transgenic rice plants produced by electroporation-mediated plasmid uptake into protoplasts. Plant Cell Rep 7:379–384. https://doi.org/10.1007/bf00269517
Zhang BY, Zheng JS, Sharp RG (2010) Phytoremediation in engineered wetlands: mechanisms and applications. Procedia Environ Sci 2:1315–1325. https://doi.org/10.1016/j.proenv.2010.10.142
Zhang G et al (2014) The CCoAOMT1 gene from jute (Corchorus capsularis L.) is involved in lignin biosynthesis in Arabidopsis thaliana. Gene 546:398–402
Zhang Y et al (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617. https://doi.org/10.1038/ncomms12617
Zhang H, Lv S, Xu H, Hou D, Li Y, Wang F (2017) H2O2 is involved in the metallothionein-mediated rice tolerance to copper and cadmium toxicity. Int J Mol Sci 18:2083. https://doi.org/10.3390/ijms18102083
Zhang X, Rui H, Zhang F, Hu Z, Xia Y, Shen Z (2018) Overexpression of a functional Vicia sativa PCS1 homolog increases cadmium tolerance and phytochelatins synthesis in Arabidopsis. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00107
Zhao H, Wang L, Zhao F-J, Wu L, Liu A, Xu W (2019a) SpHMA1 is a chloroplast cadmium exporter protecting photochemical reactions in the Cd hyperaccumulator Sedum plumbizincicola. Plant Cell Environ 42:1112–1124. https://doi.org/10.1111/pce.13456
Zhao R, Yang T, Shi C, Zhou M, Chen G, Shi F (2019b) Effects of urban–rural atmospheric environment on heavy metal accumulation and resistance characteristics of Pinus tabulaeformis in Northern China. Bull Environ Contam Toxicol 102:432–438. https://doi.org/10.1007/s00128-019-02548-7
Zhou G, Xu Y, Li J, Yang L, Liu JY (2006) Molecular analyses of the metallothionein gene family in rice (Oryza sativa L.). J Biochem Mol Biol 39:595–606
Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012) Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 35:86–99. https://doi.org/10.1111/j.1365-3040.2011.02418.x
Zhou MX, Ghnaya T, Dailly H, Cui GL, Vanpee B, Han RM, Lutts S (2019) The cytokinin trans-zeatine riboside increased resistance to heavy metals in the halophyte plant species Kosteletzkya pentacarpos in the absence but not in the presence of NaCl. Chemosphere 233:954–965. https://doi.org/10.1016/j.chemosphere.2019.06.023
Zupan J, Muth TR, Draper O, Zambryski P (2000) The transfer of DNA from agrobacterium tumefaciens into plants: a feast of fundamental insights. Plant J Cell Mol Biol 23:11–28
Acknowledgements
Authors are grateful to Bio-Rad Laboratories for providing the original pictures of Helios® Gene Gun and Gene Pulser Xcell™ Electroporation systems, Prof. Dr. Şule Arı from Istanbul University, Assoc. Prof. Dr. Semra Hasançebi from Trakya University and Assoc. Prof. Dr. Ali Yüksek from Ondokuz Mayis University for sharing some pictures of their previous studies.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ozyigit, I.I., Can, H. & Dogan, I. Phytoremediation using genetically engineered plants to remove metals: a review. Environ Chem Lett 19, 669–698 (2021). https://doi.org/10.1007/s10311-020-01095-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10311-020-01095-6
