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Advances in the Application of Plant Growth-Promoting Rhizobacteria in Phytoremediation of Heavy Metals

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Reviews of Environmental Contamination and Toxicology Volume 223

Abstract

Rapid industrialization and modernization around the world have produced the unfortunate consequence of releasing toxic wastes to the environment. Metal pollutants are derived mainly from industrial and agricultural activities. The former includes activities such as waste disposal, chemical manufacturing, and metal pollutants from vehicle exhaust, and the latter involves activities such as the use of agrochemicals, long-term application of sewage sludge, and wastewater to agricultural soils. Such releases have adversely affected human health and have produced toxic effects on plants and the soil microorganisms associated with them. Toxic metal contaminants from wastes or other products accumulate in the agricultural soils to which they are applied, threaten food security, and pose health risks to living organisms by their transfer within the food chain. Once heavy metals reach the soil, they are absorbed by plants and may be taken up by animals and humans through consumption of contaminated food or drinking water. They may even be inhaled as particulate contaminants, and due to their persistent nature, they may accumulate in both plants and animals over time.

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References

  • Abeles FB, Morgan PW, Sltveit ME Jr (1992) Ethylene in plant biology. Academic, New York, p 414

    Google Scholar 

  • Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38:2882–2889

    CAS  Google Scholar 

  • Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181

    CAS  Google Scholar 

  • Antoun H, Beauchamp CJ, Goussard N, Chabot R, Llande R (2004) Potential of Rhizobium and Bradyrhizobioum species as plant growth promoting rhizobacteria on non-legumes: effect on radishes. Plant Soil 204:57–67

    Google Scholar 

  • Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32(11): 1559–1570

    CAS  Google Scholar 

  • Babalola OO, Akindolire AM (2011) Identification of native rhizobacteria peculiar to selected food crops in Mmabatho municipality of South Africa. Biol Agric Hort 27(3–4):294–309

    Google Scholar 

  • Babalola OO, Osir EO, Sanni AI, Odhiambo GD, Bulimo WD (2003) Amplification of 1-amino- cyclopropane-1-carboxylic (ACC) deaminase from plant growth promoting bacteria in Striga-infested soil. Afr J Biotechnol 2:157–160

    CAS  Google Scholar 

  • Babalola OO, Berner DK, Amusa NA (2007) Evaluation of some bacterial isolates as germination stimulants of Striga hermonthica. Afr J Agric Res 2(1):27–30

    Google Scholar 

  • Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608

    CAS  Google Scholar 

  • Bayliss C, Bent E, Culham DE, MacLellan S, Clarke AJ, Brown GL, Wood JM (1997) Bacterial genetic loci implicated in the Pseudomonas putida GR12-2R3-canola mutualism: identification of an exudate-inducible sugar transporter. Can J Microbiol 43:809–818

    CAS  Google Scholar 

  • Belimov AA, Dietz KJ (2000) Effect of associative bacteria on element composition of barley seedlings grown in solution culture at toxic cadmium concentrations. Microbiol Res 155:113–121

    CAS  Google Scholar 

  • Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C, Preisfeld A, Dietz KJ, Stepanok VV (2001) Characterisation of plant growth-promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47:642–652

    CAS  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth promoting rhizobacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    CAS  Google Scholar 

  • Bestwick RK, Ferro AJ (1998) Reduced ethylene synthesis and delayed fruit ripening in transgenic tomatoes expressing S-adenosylmethionine hydrolase. US Patent 5, 723,746

    Google Scholar 

  • Boller T (1991) Ethylene in pathogenesis and disease resistance. In: Suttle JC, Mattoo AK (eds) The plant hormone ethylene. CRC Press, Boca Raton, FL, pp 293–314

    Google Scholar 

  • Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    CAS  Google Scholar 

  • Braud A, Jezequel K, Vieille E, Tritter A, Lebeau T (2006) Changes in extractability of Cr and Pb in a polycontaminated soil after bioaugmentation with microbial producers of biosurfactants, organic acids and siderophores. Water Air Soil Pollut: Focus 6:261–279

    CAS  Google Scholar 

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

    Google Scholar 

  • Brown GE Jr, Foster AL, Ostergren JD (1999) Mineral surfaces and bioavailability of heavy metals: a molecular-scale perspective. Proc Natl Acad Sci U S A 96:3388–3395

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Cakmakci R, Donmez F, Aydm A, Sahin F (2006) Growth promotion of plants by plant growth promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol Biochem 38:1482–1487

    CAS  Google Scholar 

  • Canbolat MY, Bilen S, Cakmakci R, Sahin F, Aydin A (2006) Effect of plant growth promoting bacteria and soil compaction on barley seedling growth, nutrient uptake, soil properties and rhizosphere microflora. Biol Fertil Soils 42:350–357

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Dat JF, Van Breusegem F, Vandenabeele S, Vranova E, Van Montague M, Inze D (2000) Dual action of active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    CAS  Google Scholar 

  • DellAmico E, Cavalca L, Andreoni V (2005) Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria. FEMS Microbiol Ecol 52:153–162

    CAS  Google Scholar 

  • Diaz J, Bernal A, Pomar F, Merino F (2001) Induction of skhikimate dehydrogenase and peroxidase in pepper (Capsicum annuum L.) seedlings in response to copper stress and its relation to lignification. Plant Sci 161:179–188

    CAS  Google Scholar 

  • Gadd GM (1992) Metals and microorganisms: a problem of definition. FEMS Microbiol Lett 100:197–204

    CAS  Google Scholar 

  • Giller KE, McGrath SP, Hirsch PR (1989) Absence of nitrogen fixation in clover grown on soil subject to long-term contamination with heavy metals is due to survival of only ineffective Rhizobium. Soil Biol Biochem 21:841–848

    CAS  Google Scholar 

  • Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial process in agricultural soils: a review. Soil Biol Biochem 30:1389–1414

    CAS  Google Scholar 

  • Giovanelli J, Mudd SH, Dakto AH (1980) Sulphur amino acids in plants. In: Miflin BJ (ed) Amino acids and derivatives, the biochemistry of plants: a comprehensive treatise, vol 5. Academic, New York, pp 453–505

    Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117

    CAS  Google Scholar 

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

    Google Scholar 

  • Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J Theor Biol 190:63–68

    CAS  Google Scholar 

  • Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-­containing soil bacteria. Eur J Plant Pathol 119:329–339

    CAS  Google Scholar 

  • Gorhe V, Paszkowski U (2006) Contribution of arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122

    Google Scholar 

  • Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395–412

    CAS  Google Scholar 

  • Grichko VP, Glick BR (2001) Amelioration of flooding stress by ACC deaminase containing plant growth promoting rhizobacteria. Plant Physiol Biochem 39:11–17

    CAS  Google Scholar 

  • Grill E, Winnacker E-L, Zenk MH (1987) Phytochelatins, a class of heavy-metal-binding peptides from plants are functionally analogous to metallothioneins. Proc Natl Acad Sci U S A 84:439–443

    CAS  Google Scholar 

  • Hallberg KB, Johnson DB (2005) Microbiology of a wetland ecosystem constructed to remediate mine drainage from a heavy metal mine. Sci Total Environ 338:53–66

    CAS  Google Scholar 

  • Han J, Sun L, Dong X, Cai Z, Sun X, Yang H, Wang Y, Song W (2005) Characterization of a novel plant growth-promoting bacteria strain Delftia tsuruhatensis HR4 both as a diazotroph and a potential biocontrol agent against various plant pathogens. Syst Appl Microbiol 28:66–76

    CAS  Google Scholar 

  • Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168:293–303

    CAS  Google Scholar 

  • Honma M, Shimomura T (1978) Metabolism of 1-amino-cyclopropane-1-carboxylic acid. Agric Biol Chem 42:1825–1831

    CAS  Google Scholar 

  • Hou W, Chen X, Song G, Wang Q, Chang CC (2007) Effects of copper and cadmium on heavy metal polluted water body restoration by duckweed (Lemna minor). Plant Physiol 107:1059–1066

    Google Scholar 

  • Iturbe-Ormaetxe I, Matamoros MA, Rubio MC, Dalton DA, Becana M (2001) The antioxidants of legume nodule mitochondria. Mol Plant Microbe Interact 14:1189–1196

    CAS  Google Scholar 

  • Jia YJ, Ito H, Matsui H, Honma M (2000) 1-aminocyclop- ropane-1-carboxylate (ACC) deaminase induced by ACC synthesized and accumulated in Penicillium citrinum intracellular spaces. Biosci Biotechnol Biochem 64:299–305

    CAS  Google Scholar 

  • Jimenez A, Hernandez JA, del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    CAS  Google Scholar 

  • John P (1991) How plant molecular biologists revealed a surprising relationship between two enzymes, which took an enzyme out of a membrane where it was not located, and put it into the soluble phase where it could be studied. Plant Mol Biol Rep 9:192–194

    Google Scholar 

  • Kagi JHR (1991) Overview of metallothionein. Methods Enzymol 205:613–626

    CAS  Google Scholar 

  • Kao PH, Huang CC, Hseu ZY (2006) Response of microbial activities to heavy metals in a neutral loamy soil treated with biosolid. Chemosphere 64:63–70

    CAS  Google Scholar 

  • Kayser G, Korckritz T, Markert B (2001) Bioleaching for the decontamination of heavy metals polluted soils with Thiobacillus spp. Wasser Boden 53:54–58

    CAS  Google Scholar 

  • Kende H (1989) Enzymes of ethylene biosynthesis. Plant Physiol 91:1–4

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Khan MS, Zaidi A, Aamil M (2002) Biocontrol of fungal pathogens by the use of plant growth promoting rhizobacteria and nitrogen fixing microorganisms. Indian J Bot Soc 81:255–263

    Google Scholar 

  • Khan MS, Zaidi A, Wani PA (2007) Role of phosphate solubilizing microorganisms in sustainable agriculture:a review. Agron Sustain Dev 27:29–43

    Google Scholar 

  • Kim JH, Kim WT, Kang BG (2001) IAA and N6-benzyladenine inhibit ethylene-regulated expression of ACC oxidase and synthase genes in mungbean hypocotyls. Plant Cell Physiol 42:1056–1061

    CAS  Google Scholar 

  • Kloepper JW, Schroth MN (1978) Plant growth promoting rhizobacteria on radishes, fourth international conference on plant pathogen bacteria, vol 2. Angers, France, pp 879–882

    Google Scholar 

  • Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120

    CAS  Google Scholar 

  • Lasat MM, Pence NS, Garvin DF, Ebbs SD, Kochian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Bot 51:71–79

    CAS  Google Scholar 

  • Laurie SH, Manthey JA (1994) The chemistry and role of metal ion chelation in plant uptake processes. In: Manthey JA, Crowley DE, Luster DG (eds) Biochemistry of metal micronutrients in the rhizosphere. Lewis Publishers, Boca Raton, pp 165–182

    Google Scholar 

  • Ledin M (2000) Accumulation of metals by microorganisms-processes and importance for soil system. Earth Sci Rev 51:1–31

    CAS  Google Scholar 

  • Lena QM, Rao GN (1997) Heavy metals in the environment. J Environ Qual 26:264

    Google Scholar 

  • Li K, Ramakrishna W (2011) Effect of multiple metal resistant bacteria from contaminated lake sediments on metal accumulation and plant growth. J Hazard Mater 189:531–539

    CAS  Google Scholar 

  • Lippmann B, Leinhos V, Bergmann H (1995) Influence of auxin producing rhizobacteria on root morphology and nutrient accumulation of crops. 1. Changes in root morphology and nutrient accumulation in maize (Zea-mays L.) caused by inoculation with indole-3-acetic acid (IAA) producing Pseudomonas and Acinetobacter strains or IAA applied exogenously. Angew Bot 69:31–36

    CAS  Google Scholar 

  • Lloyd JR, Lovley DR (2001) Microbial detoxification of metals and radionuclides. Curr Opin Biotechnol 12:248–253

    CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    CAS  Google Scholar 

  • Ma Y, Rajkumar M, Freitas H (2009) Inoculation of plant growth promoting bacteria Achromobacter xylosoxidans strain Ax10 for improvement of copper phytoextraction by Brassica juncea. J Environ Manage 90:831–837

    Google Scholar 

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

    CAS  Google Scholar 

  • Macek T, Macková M, Kas J (2000) Exploitation of plants for the removal of organics in environmental remediation. Biotechnol Adv 18:23–34

    CAS  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Ryu JH, Sa TM (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane- 1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224:268–278

    CAS  Google Scholar 

  • McGrath SP, Chaudri AM, Giller KE (1995) Long-term effects of metals in sewage sludge on soils, microorganisms and plants. J Ind Microbiol 14:94–104

    CAS  Google Scholar 

  • Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153–162

    CAS  Google Scholar 

  • Minami R, Uchiyama K, Murakami T, Kawai J, Mikami K, Yamada T, Yokoi D, Ito H, Matsui H, Honma M (1998) Properties, sequence, and synthesis in Escherichia coli of 1-aminocyclopropane-1-carboxylate deaminase from Hansenula saturnus. J Biochem 123:1112–1118

    CAS  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta K (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039

    CAS  Google Scholar 

  • Morgan PW, Drew CD (1997) Ethylene and plant responses to stress. Physiol Plant 100:620–630

    CAS  Google Scholar 

  • Newman LA, Reynolds CM (2004) Phytodegradation of organic compounds. Curr Opin Biotechnol 15:225–230

    CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy metal resistance. Appl Microbiol Biotechnol 51:730–750

    CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    CAS  Google Scholar 

  • Noordman WH, Reissbrodt R, Bongers RS, Rademaker ILW, Bockelmann W, Smit G (2006) Growth stimulation of Brevibacterium sp. by siderophores. J Appl Microbiol 101:637–646

    CAS  Google Scholar 

  • Ochiai EI (1977) Bioinorganic chemistry: an introduction. Allyn and Bacon, Boston, pp 218–262

    Google Scholar 

  • Olson JW, Mehta NS, Maier RJ (2001) Requirement of nickel metabolism protein HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori. Mol Microbiol 39:176–182

    CAS  Google Scholar 

  • Penrose DM, Glick BR (2001) Levels of 1-aminocyclopropane-1-carboxylic acid (ACC) in exudates and extracts of canola seeds treated with plant growth-promoting bacteria. Can J Microbiol 47:368–372

    CAS  Google Scholar 

  • Pishchik VN, Vorobev NI, Provorov NA (2005) Experimental and mathematical simulation of population dynamics of rhizospheric bacteria under conditions of cadmium stress. Microbiology 74:735–740

    CAS  Google Scholar 

  • Pollard JA, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566

    CAS  Google Scholar 

  • Ponmurugan PGC (2006) In vitro production of growth regulators and phosphatase activity by phosphate solubilizing bacteria. Afr J Biotechnol 5:340–350

    Google Scholar 

  • Rajkumar M, Freitas H (2008) Effects of inoculation of plant-growth promoting bacteria on Ni uptake by Indian mustard. Biores Technol 99:3491–3498

    CAS  Google Scholar 

  • Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 62:741–748

    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

    CAS  Google Scholar 

  • Reed MLE, Glick BR (2004) Applications of free living plant growth promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25

    Google Scholar 

  • Roane TM, Pepper IL (2000) Microorganisms and metal pollution. In: Maier RM, Pepper IL, Gerba CB (eds) Environmental microbiology. Academic, London, p 55

    Google Scholar 

  • Romkens P, Bouwman L, Japenga J, Draaisma C (2002) Potentials and drawbacks of chelate-enhanced phytoremediation of soils. Environ Pollut 116:109–121

    CAS  Google Scholar 

  • Salt DE (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 33:713–717

    CAS  Google Scholar 

  • Salt DE, Kramer U (1999) Mechanisms of metal hyperaccumulation in plants. In: Raskin I, Enslely BD (eds) Phytoremediaton of toxic metals: using plants to clean-up the environment. John Wiley and Sons, New York, pp 231–246

    Google Scholar 

  • Salt DE, Rauser WE (1995) Mg ATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol 107:1293–1301

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy-metal induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    CAS  Google Scholar 

  • Seth CS, Chaturvedi PK, Misra V (2007) Toxic effect of arsenate and cadmium alone and in combination on giant duckweed (Spirodela polyrrhiza L.) in response to its accumulation. Environ Toxicol 22:539–549

    CAS  Google Scholar 

  • Seth CS, Chaturvedi PK, Misra V (2008) The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotoxicol Environ Saf 71:76–85

    CAS  Google Scholar 

  • Shaw BP, Sahu SK, Mishra RK (2004) Heavy metal induced oxidative damage in terrestrial plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystems. Narosa Publishing House, New Delhi, India, pp 84–126

    Google Scholar 

  • Sheng XF, Xia JJ (2006) Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium resistant bacteria. Chemosphere 64:1036–1042

    CAS  Google Scholar 

  • Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008) 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

    CAS  Google Scholar 

  • Sirko A, Brodzik R (2000) Plant ureases: roles and regulation. Acta Biochim Pol 47:1189–1195

    CAS  Google Scholar 

  • Skorzynska-Polit E, Drazkiewicz M, Krupa Z (2010) Lipid peroxidation and antioxidative response in Arabidopsis thaliana exposed to cadmium and copper. Acta Physiol Plant 32:169–175

    CAS  Google Scholar 

  • Sposito FG (2000) The chemistry of soils. In: Maier RM, Pepper IL, Gerba CB (eds) Environmental microbiology. Academic, London, p 406

    Google Scholar 

  • Sudo E, Itouga M, Yoshida-Hatanaka K, Ono Y, Sakakibara H (2008) Gene expression and sensitivity in response to copper stress in rice leaves. J Exp Bot 59:3465–3474

    CAS  Google Scholar 

  • Suresh B, Ravishankar GA (2004) Phytoremediation- a novel and promising approach for environmental clean-up. Crit Rev Biotechnol 24:97–124

    CAS  Google Scholar 

  • Tak HI, Inam A, Inam A (2010) Effects of urban wastewater on the growth, photosynthesis and yield of chickpea under different levels of nitrogen. Urban Water J 7:187–195

    CAS  Google Scholar 

  • Tank N, Saraf M (2003) Phosphate solubilization, exopolysaccharide production and indole acetic acid secretion by rhizobacteria isolated from Trigonella graecum. Indian J Microbiol 43:37–40

    Google Scholar 

  • Timmis KN, Pieper DH (1999) Bacteria designed for bioremediation. Trends Biotechnol 17:200–204

    CAS  Google Scholar 

  • Tinker PB (1984) The role of microorganisms in mediating and facilitating the uptake of plant nutrients from soil. Plant Soil 76:77–91

    CAS  Google Scholar 

  • Tomsett AB, Thurman DA (1988) Molecular biology of metal tolerances of plants. Plant Cell Environ 11:383–394

    CAS  Google Scholar 

  • Traina SJ, Laperche V (1999) Contaminant bioavailability in soils, sediments, and aquatic environments. Proc Natl Acad Sci U S A 96:3365–3371

    CAS  Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Netrusov AI (2005) Auxin production by bacteria associated with orchid roots. Microbiology 74:46–53

    CAS  Google Scholar 

  • Umrania VV (2006) Bioremediation of toxic heavy metals using acidothermophilic autotrophes. Bioresour Technol 97:1237–1242

    CAS  Google Scholar 

  • Van Steveninck RFM, Van Steveninck ME, Wells AJ, Fernando DR (1990) Zinc tolerance and the binding of zinc as zinc phytate in Lemna minor. X-ray microanalytical evidence. J Plant Physiol 137:140–146

    Google Scholar 

  • Vangronsveld J, Clijsters H (1994) Toxic effects of metals. In: Farago MG (ed) Plants and the chemical elements. VHC-Verbgsgesellschaft, Weinheim, Germany, p 149

    Google Scholar 

  • Vivas A, Biru B, Ruiz-Lozano JM, Azcon R (2006) Two bacterial strains isolated from Zn-polluted soil enhance plant growth and micorrhizal efficiency under Zn toxicity. Chemosphere 52:1523–1533

    Google Scholar 

  • Vogel JP, Woeste KE, Theologis A, Kieber JJ (1998) Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc Natl Acad Sci U S A 95:4766–4771

    CAS  Google Scholar 

  • Vogeli-Lange R, Wagner GJ (1990) Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves: implication of a transport function for cadmium binding peptides. Plant Physiol 92:1086–1093

    CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007) Synergistic effects of the inoculation with nitrogen fixing and phosphate solubilizing rhizobacteria on the performance of field grown chickpea. J Plant Nutr Soil Sci 170:283–287

    CAS  Google Scholar 

  • Welch RM (1995) Micronutrient nutrition of plants. Crit Rev Plant Sci 14:49–82

    CAS  Google Scholar 

  • Wenzel WW, Bunkowski M, Puschenreiter M, Horak O (2003) Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil. Environ Pollut 123:131–138

    CAS  Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189

    CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    CAS  Google Scholar 

  • Yu X, Liu X, Zhu TH, Liu GH, Mao C (2012) Co-inoculation with phosphate-solubilizing and nitrogen-fixing bacteria on solubilization of rock phosphate and their effect on growth promotion and nutrient uptake by walnut. Eur J Soil Biol 50:112–117

    CAS  Google Scholar 

  • Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ 101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997

    CAS  Google Scholar 

  • Zhuang XL, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413

    Google Scholar 

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Acknowledgements

The first author is thankful to the North-West University for the award of postdoctoral fellowship. This work is based on research supported by the National Research Foundation.

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Tak, H.I., Ahmad, F., Babalola, O.O. (2013). Advances in the Application of Plant Growth-Promoting Rhizobacteria in Phytoremediation of Heavy Metals. In: Whitacre, D. (eds) Reviews of Environmental Contamination and Toxicology Volume 223. Reviews of Environmental Contamination and Toxicology, vol 223. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5577-6_2

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