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Diazotrophs-assisted phytoremediation of heavy metals: a novel approach

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Abstract

Heavy metals, which have severe toxic effects on plants, animals, and human health, are serious pollutants of the modern world. Remediation of heavy metal pollution is utmost necessary. Among different approaches used for such remediation, phytoremediation is an emerging technology. Research is in progress to enhance the efficiency of this plant-based technology. In this regard, the role of rhizospheric and symbiotic microorganisms is important. It was assessed by enumeration of data from the current studies that efficiency of phytoremediation can be enhanced by assisting with diazotrophs. These bacteria are very beneficial because they bring metals to more bioavailable form by the processes of methylation, chelation, leaching, and redox reactions and the production of siderophores. Diazotrophs also posses growth-promoting traits including nitrogen fixation, phosphorous solubilization, phytohormones synthesis, siderophore production, and synthesis of ACC-deaminase which may facilitate plant growth and increase plant biomass, in turn facilitating phytoremediation technology. Thus, the aim of this review is to highlight the potential of diazotrophs in assisting phytoremediation of heavy metals in contaminated soils. The novel current assessment of literature suggests the winning combination of diazotroph with phytoremediation technology.

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References

  • Abdelatey LM, Khalil WK, Ali TH, Mahrous KF (2011) Heavy metal resistance and gene expression analysis of metal resistance genes in gram-positive and gram-negative bacteria present in egyptian soils. J Appl Sci Environ San 6:201–211

    CAS  Google Scholar 

  • Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. University of Georgia, Aitken, pp 15–20

    Book  Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881

    Article  CAS  Google Scholar 

  • Altinozlu H, Karagoz A, Polat T, Unver I (2012) Nickel hyperaccumulation by natural plants in Turkish serpentine soils. Turk J Bot 36:269–280

    CAS  Google Scholar 

  • Banasova V, Horak O, Nadubinska M, Ciamporova M (2008) Heavy metal content in Thlaspi caerulescens J. et C. Presl growing on metalliferous and non-metalliferous soils in Central Slovakia. Int J Environ Pollut 33:133–145

    Article  CAS  Google Scholar 

  • Bani A, Pavlova D, Echevarria G, Mullai A, Reeves RD, Morel JL, Sulce S (2010) Nickel hyperaccumulation by the species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Bot Serbica 34:3–14

    Google Scholar 

  • Beskoski VP, Gojgic-Cvijovic G, Milic J, Ilic M, Miletic S, Solevic T, Vrvic MM (2011) Ex situ bioremediation of a soil contaminated by mazut (heavy residual fuel oil)—a field experiment. Chemosphere 83:34–40

    Article  CAS  Google Scholar 

  • Boopathy R (2000) Factors limiting bioremediation technologies. Bioresour Technol 74:63–67

    Article  CAS  Google Scholar 

  • Braud A, Jezequel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286

    Article  Google Scholar 

  • Burd GI, Dixon DG, Glick RR (2000) Plant growth promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245

    Article  CAS  Google Scholar 

  • Carrasco JA, Armario P, Pajuelo E, Burgos A, Caviedes MA, López R, Chamber MA, Palomares AJ (2005) Isolation and characterization of symbiotically effective Rhizobium resistant to arsenic and heavy metals after the toxic spill at the Aznalcollar pyrite mine. Soil Biol Biochem 37:1131–1140

    Article  CAS  Google Scholar 

  • Chaudhary HJ, Peng G, Hu M, He Y, Yang L, Luo Y, Tan Z (2012) Genetic diversity of endophytic diazotrophs of the wild rice, Oryza alta and identification of the new diazotroph, Acinetobacter oryzae sp. nov. Microb Ecol 63:813–821

    Article  CAS  Google Scholar 

  • Chehregani A, Malayeri B (2007) Removal of heavy metals by native accumulator plants. Int J Agric Biol 9:462–465

    CAS  Google Scholar 

  • Chen WM, Wu CH, James EK, Chang JS (2008) Metal biosorption capability of Cupriavidus taiwanensis and its effects on heavy metal removal by nodulated Mimosa. J Hazard Mater 151:364–371

    Article  CAS  Google Scholar 

  • Daniels R, Vanderleyden J, Michiels J (2004) Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 28:261–289

    Article  CAS  Google Scholar 

  • Dary M, Chamber-Perez M, Palomares A, Pajuelo E (2010) In situ phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177:323–330

    Article  CAS  Google Scholar 

  • de-Bashan LE, Hernandez JP, Bashan Y (2012) The potential contribution of plant growth promoting bacteria to reduce environmental degradation—a comprehensive evaluation. Appl Soil Ecol 61:171–189

    Article  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Döbereiner J, Day JM (1976) Associative symbioses in tropical grasses: characterization of microorganisms and dinitrogen-fixing sites. In: Newton WE, Nyman CJ (eds) Proc. 1 Intern. Symp. on Nitrogen Fixation. Washignton State University Press, Washignton, pp 518–538

    Google Scholar 

  • Döbereiner J, Pedrosa FO (1987) Nitrogen-fixing bacteria in nonleguminous crop plants, 1st edn. Springer, New York

    Google Scholar 

  • Döbereiner J, Day JM, Dart PJ (1972) Nitrogenase activity and oxygen sensitivity of the Paspalum notatum—Azotobacter paspali association. J Gen Microbiol 71:103–116

    Article  Google Scholar 

  • Doble M, Kumar A (2005) Biotreatment of industrial effluents. Elsvier, Butterworth-Heinemann, UK, pp 1–5

    Book  Google Scholar 

  • Duruibe JO, Ogwuegbu MOC, Egwurugwu JN (2007) Heavy metal pollution and human biotoxic effects. Int J Phys Sci 2:112–118

    Google Scholar 

  • Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11:271–279

    Article  CAS  Google Scholar 

  • Gadd GM (2004) Microbial influence on metal mobility and application to bioremediation. Geoderma 122:109–119

    Article  CAS  Google Scholar 

  • Gadd GM (2009) Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. J Chem Technol Biotechnol 84:13–28

    Article  CAS  Google Scholar 

  • Garcia-Salgado S, Garcia-Casillas D, Quijano-Nieto MA, Bonilla-Simon MM (2012) Arsenic and heavy metal uptake and accumulation in native plant species from soils polluted by mining activities. Water Air Soil Pollut 223:559–572

    Article  CAS  Google Scholar 

  • Ghosh M, Singh S (2005) A review on phytoremediation of heavy metals and utilization of it’s by products. Asian J Energy Environ 3:214–231

    Google Scholar 

  • Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393

    Article  CAS  Google Scholar 

  • Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374

    Article  CAS  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:1–15

    Article  Google Scholar 

  • Graham PH, Vance CP (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crop Res 65:93–106

    Article  Google Scholar 

  • Hadi F, Bano A (2010) Effect of diazotrophs (Rhizobium and Azotobacter) on growth of maize (Zea mays L.) and accumulation of Lead (Pb) in different plant parts. Pak J Bot 42:4363–4370

    Google Scholar 

  • Handelsman J, Stabb EV (1996) Biocontrol of soil borne plant pathogens. Plant Cell 8:1855–1869

    Article  CAS  Google Scholar 

  • Hayat R, Sheirdil RA, Iftikhar-ul-Hassan M, Ahmed I (2013) Characterization and identification of compost bacteria based on 16S rRNA gene sequencing. Ann Microbiol 63:905–912

    Article  Google Scholar 

  • Hussain A, Abbas N, Arshad F, Akram M, Khan ZI, Ahmad K, Mansha M, Mirzaei F (2013) Effects of diverse doses of Lead (Pb) on different growth attributes of Zea-Mays L. Agric Sci 4:262–265

    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

    Article  CAS  Google Scholar 

  • Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2008) Promotion of metal accumulation in nodule of Astragalus sinicus by the expression of the iron-regulated transporter gene in Mesorhizobium huakuii subsp. rengei B3. J Biosci Bioeng 105:642–648

    Article  CAS  Google Scholar 

  • Iqbal M, Khan AG, Anwar-ul-hassan AM (2012) Soil physical health indices, soil organic carbon, nitrate contents and wheat growth as influenced by irrigation and nitrogen rates. Int J Agric Biol 14:1–10

    CAS  Google Scholar 

  • Jabeen R, Ahmad A, Iqbal M (2009) Phytoremediation of heavy metals: physiological and molecular mechanisms. Bot Rev 75:339–364

    Article  Google Scholar 

  • Jiang C, Sheng X, Qian M, Wang Q (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164

    Article  CAS  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Joshi PM, Juwarkar AA (2009) In vivo studies to elucidate the role of extracellular polymeric substances from Azotobacter in immobilization of heavy metals. Environ Sci Technol 43:5884–5889

    Article  CAS  Google Scholar 

  • Juwarkar AA, Nair A, Dubey KV, Singh SK, Devotta S (2007) Biosurfactant technology for remediation of cadmium and lead contaminated soils. Chemosphere 10:1996–2002

    Article  Google Scholar 

  • Kalve S, Sarangi BK, Pandey RA, Chakrabarti T (2011) Arsenic and chromium hyperaccumulation by an ecotype of Pteris vittata- prospective for phytoextraction from contaminated water and soil. Curr Sci 100:888–894

    CAS  Google Scholar 

  • Kamran MA, Mufti R, Mubariz N, Syed JH, Bano A, Javed MT, Chaudhary HJ (2014) The potential of the flora from different regions of Pakistan in phytoremediation: a review. Environ Sci Pollut Res 21:801–812

    Article  Google Scholar 

  • Khan AG (2005) Role of soil microbes in the rhizosphere of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364

    Article  CAS  Google Scholar 

  • Khan S, Hesham AE, Qiao M, Rehman S, He JZ (2010) Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res 17:288–296

    Article  CAS  Google Scholar 

  • Kidd P, Barcelo J, Bernal MP, Navari-Izzo F, Poschenrieder C, Shilev S et al (2009) Trace element behaviour at the root–soil interface: implications in phytoremediation. Environ Exp Bot 67:243–259

    Article  CAS  Google Scholar 

  • Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant–microbe interaction. Mol Plant-Microbe Interact 17:6–15

    Article  CAS  Google Scholar 

  • Kumar KV, Srivastava S, Singh N, Behl HM (2009) Role of metal resistant plant growth promoting bacteria in ameliorating fly ash to the growth of Brassica juncea. J Hazard Mater 170:51–57

    Article  CAS  Google Scholar 

  • Küpper H, Lombi E, Zhao FJ, Wieshammer G, McGrath SP (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300

  • Laskar F, Sharma GD, Deb B (2013) Characterization of plant growth promoting traits of diazotrophic bacteria and their inoculating effects on growth and yield of rice crops. Biotechnology 2:3–5

    Google Scholar 

  • Li Y-M, Chaney R, Brewer E, Roseberg R, Angle JS, Baker A, Reeves R, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115

    Article  CAS  Google Scholar 

  • Lombi E, Zhao F, Dunham S, McGrath S (2001) Phytoremediation of heavy metal-contaminated soils:natural hyperaccumulation versus chemically enhanced phytoextraction. J Environ Qual 30:1919–1926

    Article  CAS  Google Scholar 

  • Lovley DR (2000) Fe(III) and Mn(IV) reduction. In: Lovley DR (ed) Environmental microbe–metal interactions. Am Soc Microbiol, Washington, pp. 3–30

  • Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011a) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Luo Y, Freitas H (2011b) Inoculation of endophytic bacteria on host and non-host plants—effects on plant growth and Ni uptake. J Hazard Mater 195:230–237

    Article  CAS  Google Scholar 

  • Neubauer U, Furrer G, Schulin R (2002) Heavy metal sorption on soil minerals affected by the siderophore desferrioxamine B: the role of Fe(III) (hydr)oxides and dissolved Fe(III). Eur J Soil Sci 53:45–55

    Article  CAS  Google Scholar 

  • Nie L, Shah S, Burd GI, Dixon DG, Glick BR (2002) Phytoremediation of arsenate contaminated soil by transgenic canola and the plant growth-promoting bacterium Enterobacter cloacae CAL2. Plant Physiol Biochem 40:355–361

    Article  CAS  Google Scholar 

  • Nonnoi F, Chinnaswamy A, García de la Torre VS, Coba de la Peña T, Lucas MM, Pueyo JJ (2012) Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes Medicago spp. and Trifolium spp. growing in mercury-contaminated soils. Appl Soil Ecol 61:49–59

    Article  Google Scholar 

  • Omura Y, Shimotsuura Y, Fukuoka A, Fukuoka H, Nomoto T (1996) Significant mercury deposits in internal organs following the removal of dental amalgam, & development of pre-cancer on the gingiva and the sides of the tongue and their represented organs as a result of inadvertent exposure to strong curing light (used to solidify synthetic dental filling material) & effective treatment: a clinical case report, along with organ representation areas for each tooth. Acupunct Electrother Res 21:133–160

    CAS  Google Scholar 

  • Pandey VC (2012) Phytoremediation of heavy metals from fly ash pond by Azolla caroliniana. Ecotoxicol Environ Saf 82:8–12

    Article  CAS  Google Scholar 

  • Park JD (2010) Heavy metal poisoning. Hanyang Med Rev 30:319–325

    Article  CAS  Google Scholar 

  • Pavel VL, Sobariu DL, Tudorache Fertu ID, Statescu F, Gaverilescu M (2013) Symbiosis in the environment biomanagement of soils contaminated with heavy metals. Eur J Sci Theol 9:211–224

    Google Scholar 

  • Pedraza RO (2008) Recent advances in nitrogen-fixing acetic acid bacteria. Int J Food Microbiol 125:25–35

    Article  CAS  Google Scholar 

  • Rai PK (2008) Technical note: phytoremediation of Hg and Cd from industrial effluents using an aquatic free floating macrophyte Azolla pinnata. Int J Phytoremed 10:430–439

    Article  CAS  Google Scholar 

  • Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160

    Article  CAS  Google Scholar 

  • Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Raju PN, Evans HJ, Seidler RJ (1972) An asymbiotic nitrogen-fixing bacterium from the root environment of corn. Proc Natl Acad Sci 69:3474–3478

    Article  CAS  Google Scholar 

  • Razi SS, Sen SP (1996) Amelioration of water stress effects on wetland rice by urea-N, plant growth regulators, and foliar spray of a diazotrophic bacterium Klebsiella sp. Biol Fertil Soils 23:454–458

    Article  CAS  Google Scholar 

  • Ribeiro de Souza SC, López A, de Andrade S, Anjos de Souza L, Schiavinato MA (2012) Lead tolerance and phytoremediation potential of Brazilian leguminous tree species at the seedling stage. J Environ Manag 110:299–307

    Article  CAS  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560

    Article  CAS  Google Scholar 

  • Sakakibara M, Ohmori Y, Ha NTH, Sano S, Sera K (2011) Phytoremediation of heavy metal‐contaminated water and sediment by Eleocharis acicularis. Clean Soil Air Water 39:735–741

    Article  CAS  Google Scholar 

  • Sarma H (2011) Metal hyperaccumulation in plants: a review focusing on phytoremediation technology. J Environ Sci Technol 4:118–138

    Article  CAS  Google Scholar 

  • Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854

    Article  CAS  Google Scholar 

  • Sheng X, He L, Wang Q, Ye H, Jiang C (2008a) Effects of inoculation of biosurfactant-producing Bacillus sp. J119 on plant growth and cadmium uptake in a cadmium-amended soil. J Hazard Mater 155:17–22

    Article  CAS  Google Scholar 

  • Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008b) Characterization of heavy metal-resistant endophytic bacteria from rape Brassica napus roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170

    Article  CAS  Google Scholar 

  • Smith SR, Jaffe DM, Skinner MA (1997) Case report of metallic mercury injury. Pediatr Emerg Care 13:114–116

    Article  CAS  Google Scholar 

  • Sriprang R, Hayashi M, Ono H, Takagi M, Hirata K, Murooka Y (2003) Enhanced accumulation of Cd 2+ by a Mesorhizobium sp. transformed with a gene from Arabidopsis thaliana coding for phytochelatin synthase. Appl Environ Microbiol 69:1791–1796

    Article  Google Scholar 

  • Tien TM, Gaskins MH, Hubbell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum). Appl Environ Microbiol 37:1016–1024

    CAS  Google Scholar 

  • Van Ginneken L, Meers E, Guisson R, Ruttens A, Elst K, Tack FM, Vangronsveld J, Diels L, Dejonghe W (2007) Phytoremediation for heavy metal‐contaminated soils combined with bioenergy production. J Environ Eng Landsc Manag 15:227–236

    Google Scholar 

  • Van Hullebusch ED, Lens PNL, Tabak HH (2005) Developments in bioremediation of soils and sediments polluted with metals and radionuclides. 3. Influence of chemical speciation and bioavailability on contaminants immobilization/mobilization bio-processes. Rev Environ Sci Biotechnol 4:185–212

    Article  Google Scholar 

  • Venkatesh NM, Vedaraman N (2012) Remediation of soil contaminated with copper using rhamnolipids produced from Pseudomonas aeruginosa MTCC 2297 using waste frying rice bran oil. Ann Microbiol 62:85–91

    Article  CAS  Google Scholar 

  • Vidali M (2001) Bioremediation. An overview. Pure Appl Chem 73:1163–1172

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007a) Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by greengram plants. Chemosphere 70:36–45

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007b) Impact of zinc-tolerant plant growth-promoting rhizobacteria on lentil grown on zinc-amended soil. Agron Sustain Dev 28:449–455

    Article  Google Scholar 

  • Wani PA, Khan MS, Zaidi (2008) Effect of metal-tolerant plant growth-promoting Rhizobium on the performance of pea grown in metal-amended soil. Arch Environ Contam Toxicol 55:33–42

    Article  CAS  Google Scholar 

  • Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (Phytoremediation) of soil. Plant Soil 321:385–408

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    Article  CAS  Google Scholar 

  • Wu CH, Wood TK, Mulchandani A, Chen W (2006a) Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl Environ Microbiol 72:1129–1134

    Article  CAS  Google Scholar 

  • Wu S, Cheung K, Luo Y, Wong M (2006b) Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 140:124–135

    Article  CAS  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soil: a review of sources, chemistry, risks and best available strategies for bioremediation. ISRN Ecol 2011:1–20

    Article  Google Scholar 

  • Yan-de J, Zhen-li H, Xiao-e (2007) Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J Zhejiang Univ Sci B 8:192–207

    Google Scholar 

  • Yang X, Feng Y, Hi Z, Stofella PJ (2005) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol 18:339–353

    Article  CAS  Google Scholar 

  • Yang S, Deng H, Li M (2008) Manganese uptake and accumulation in a woody hyperaccumulator, Schima superba. Plant Soil Environ 54:441–446

    CAS  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    CAS  Google Scholar 

  • Zhang X, Xia H, Li Z, Zhuang P, Gao B (2011) Identification of a new potential Cd-hyperaccumulator Solanum photeinocarpum by soil seed bank-metal concentration gradient method. J Hazard Mater 189:414–419

    Article  CAS  Google Scholar 

  • Zhao F, Dunham S, McGrath S (2002) Arsenic hyperaccumulation by different fern species. New Phytol 156:27–31

    Article  CAS  Google Scholar 

  • Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43

    Article  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge Prof. Elena Maestri (Editor-ESPR) as well as two anonymous reviewers for their valuable feedback for our work. We are very grateful to Prof. Bernard R. Glick from Department of Biology, University of Waterloo, for the critical reading and improvement of our manuscript. We are also thankful to Dr. Abid Hussain, Faculty of Agriculture and Food Sciences, Department of Arid Land Agriculture, King Faisal University, The Kingdom of Saudi Arabia.

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  1. Department of Plant Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad, 45320, Pakistan

    Abid Ullah, Hafsa Mushtaq, Muhammad Farooq Hussain Munis & Hassan Javed Chaudhary

  2. Department of Zoology, University of Malakand, Chakdara, Dir Lower, 18550, Khyber Pakhtunkhwa, Pakistan

    Hazrat Ali

  3. Department of Botany, Government College University, Faisalabad, 38000, Pakistan

    Muhammad Tariq Javed

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  1. Abid Ullah
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  2. Hafsa Mushtaq
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Correspondence to Hassan Javed Chaudhary.

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Ullah, A., Mushtaq, H., Ali, H. et al. Diazotrophs-assisted phytoremediation of heavy metals: a novel approach. Environ Sci Pollut Res 22, 2505–2514 (2015). https://doi.org/10.1007/s11356-014-3699-5

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