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Metal-Legume-Microbe Interactions: Toxicity and Remediation

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Microbes for Legume Improvement

Abstract

Heavy metals discharged from various sources accumulate within soils and disrupt ecosystems. The toxic metals are taken up by beneficial soil microbiota and growing plants and cause potential human risks via food chain. Also, heavy metals seriously affect the microbial compositions and their physiological functions. Among plant species, legumes play an important role in human dietary systems and supply nitrogen to legumes through symbiosis with rhizobia. Metals when present in legume habitat act as a devastating stress factor and restrict the growth of rhizobia, legumes, and legume-Rhizobium symbiosis. Several physical and chemical methods have been developed to remediate heavy metal-polluted soils, but these methods are unacceptable due to their high cost, and they are not environmentally friendly. Therefore, the use of metal-tolerant/metal-detoxifying microbes collectively called bioremediation offers a sustainable and low-cost option to clean up polluted soils. Besides remediation, the metal-tolerant microbes also promote plant growth by other direct or indirect means. Owing to the importance of legumes in maintaining soil fertility and human health, there is greater emphasis to identify the metal-resistant/metal-tolerant rhizobia and legume plants. The present chapter gives an in-depth insight into the impact of metals on rhizobia-legume symbiosis. Also, the role of metal-tolerant rhizobia in metal toxicity abatement is highlighted.

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References

  • Alamgir M (2016) The effects of soil properties to the extent of soil contamination with metals. In: Environmental remediation technologies for metal-contaminated soils. Springer, Tokyo, pp 1–19

    Google Scholar 

  • Bajkic S, Narancic T, Dokic L, Dordevic D, Nikodinovic-Runic J, Morić I, Vasiljević B (2013) Microbial diversity and isolation of multiple metal-tolerant bacteria from surface and underground pits within the copper mining and smelting complex bor. Arch Biol Sci 65:375–386

    Article  Google Scholar 

  • Balestrasse KB, Gallego SM, Tomaro ML (2006) Oxidation of the enzymes involved in nitrogen assimilation plays an important role in the cadmium-induced toxicity in soybean plants. Plant Soil 284:187–194

    Article  CAS  Google Scholar 

  • Belimov AA, Safroonova VI, Mimura T (2002) Response of spring rape to inoculation with plant growth promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase depends on nutrient status of the plant. Can J Microbiol 48:189–199

    Article  CAS  PubMed  Google Scholar 

  • Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Kirkham MB, Scheckel K (2014) Remediation of heavy metal(loid)s contaminated soils–to mobilize or to immobilize? J Hazard Mater 266:141–166

    Article  CAS  PubMed  Google Scholar 

  • Bramhachari PV, Nagaraju GP (2017) Extracellular polysaccharide production by bacteria as a mechanism of toxic heavy metal biosorption and biosequestration in the marine environment. In: Naik MM, Dubey SK (eds) Marine pollution and microbial remediation. Springer, Singapore, pp 67–85

    Chapter  Google Scholar 

  • Carpena RO, Vázquez S, Esteban E, Fernández-Pascual M, de Felipe MR, Zornoza P (2003) Cadmium-stress in white lupin: effects on nodule structure and functioning. Plant Physiol Biochem 41:911–919

    Article  CAS  Google Scholar 

  • Chaudhari J, Patel K, Patel V (2016) Exploring the toxic effects of Pb and Ni on stem anatomy of Pisum Sativum L. Int J Chem Environ Biol Sci 4:28–32

    Google Scholar 

  • Chaudhary P, Dudeja SS, Kapoor KK (2004) Effectivity of host Rhizobium leguminosarum symbiosis in soils receiving sewage water containing heavy metals. Microbiol Res 159:121–127

    Article  CAS  PubMed  Google Scholar 

  • Chaudri AM, Allain CMG, Barbosa-Jefferson VL, Nicholson FA, Chambers BJ, McGrath SP (2000) A study of the impacts of Zn and Cu on two rhizobial species in soils of a long-term field experiment. Plant Soil 221:167–179

    Article  CAS  Google Scholar 

  • Chiboub M, Saadani O, Fatnassi IC, Abdelkrim S, Abid G, Jebara M, Jebara SH (2016) Characterization of efficient plant-growth-promoting bacteria isolated from Sulla coronaria resistant to cadmium and to other heavy metals. C R Biol 339:391–398

    Article  PubMed  Google Scholar 

  • Chubukova OV, Postrigan BN, Baimiev AK, Chemeris AV (2015) The effect of cadmium on the efficiency of development of legume-Rhizobium symbiosis. Biol Bull Russ Acad Sci 42:458–462

    Article  CAS  Google Scholar 

  • Cunningham SD, Berti WR, Huang JW (1995) Phytoremediation of contaminated soils. Trends Biotechnol 13:393–397

    Article  CAS  Google Scholar 

  • de Jesus MN, da Costa Neto VP, de Araújo ASF, Figueiredo MDVB, Bonifacio A, Rodrigues AC (2016) Bradyrhizobium sp. inoculation ameliorates oxidative protection in cowpea subjected to long-term composted tannery sludge amendment. Eur J Soil Biol 76:35–45

    Article  Google Scholar 

  • Deepika KV, Raghuram M, Kariali E, Bramhachari PV (2016) Biological responses of symbiotic Rhizobium radiobacter strain VBCK1062 to the arsenic contaminated rhizosphere soils of mung bean. Ecotoxicol Environ Saf 134:1–10

    Article  CAS  Google Scholar 

  • Deicke M, Bellenger JP, Wichard T (2013) Direct quantification of bacterial molybdenum and iron metallophores with ultra-high-performance liquid chromatography coupled to time-of-flight mass spectrometry. J Chromatogr A 1298:50–60

    Article  CAS  PubMed  Google Scholar 

  • Delgadillo J, Lafuente A, Doukkali B, Redondo-Gómez S, Mateos-Naranjo E, Caviedes MA, Pajuelo E, Rodríguez-Llorente ID (2015) Improving legume nodulation and Cu rhizostabilization using a genetically modified rhizobia. Environ Technol 36:1237–1245

    Article  CAS  PubMed  Google Scholar 

  • Duan J, Muller KM, Charles TC, Vesely S, Glick BR (2009) 1-aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from southern Saskatchewan. Microb Ecol 57:421–422

    Article  Google Scholar 

  • Dubey D, Pandey A (2011) Effect of nickel (Ni) on chlorophyll, lipid peroxidation and antioxidant enzymes activities in black gram (Vigna mungo) leaves. Int J Sci Nat 2:395–401

    CAS  Google Scholar 

  • El Aafi N, Saidi N, Maltouf AF, Perez-Palacios P, Dary M, Brhada F, Pajuelo E (2015) Prospecting metal-tolerant rhizobia for phytoremediation of mining soils from Morocco using Anthyllis vulneraria L. Environ Sci Pollut Res 22:4500–4512

    Article  CAS  Google Scholar 

  • El-Deeb SM, Al-Sheri FS (2005) Role of some chemical compounds on the detoxification of Rhizobium leguminosarum biovar vicia by some heavy metals. Pak J Biol Sci 8:1693–1698

    Article  CAS  Google Scholar 

  • Fahr M, Laplaze L, Bendaou N, Hocher V, El Mzibri M, Bogusz D, Smouni A (2013) Effect of lead on root growth. Front Plant Sci 4:175

    Article  PubMed  PubMed Central  Google Scholar 

  • Fatnassi IC, Chiboub M, Jebara M, Jebara SH (2014) Bacteria associated with different legume species grown in heavy-metal contaminated soils. Int J Agric Policy Res 2:460–467

    Google Scholar 

  • Fatnassi IC, Chiboub M, Saadani O, Jebara M, Jebara SH (2015a) Phytostabilization of moderate copper contaminated soils using co-inoculation of Vicia faba with plant growth promoting bacteria. J Basic Microbiol 55:303–311

    Article  CAS  PubMed  Google Scholar 

  • Fatnassi IC, Chiboub M, Saadani O, Jebara M, Jebara SH (2015b) Impact of dual inoculation with Rhizobium and PGPR on growth and antioxidant status of Vicia faba L. under copper stress. C R Biol 338:241–254

    Article  PubMed  Google Scholar 

  • Furukawa K, Ramesh A, Zhou Z, Weinberg Z, Vallery T, Winkler WC, Breaker RR (2015) Bacterial riboswitches cooperatively bind Ni2+ or Co2+ ions and control expression of heavy metal transporters. Mol Cell 57:1088–1098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    Article  CAS  Google Scholar 

  • Garg N, Aggarwal N (2012) Effect of mycorrhizal inoculations on heavy metal uptake and stress alleviation of Cajanus cajan (L.) Millsp. genotypes grown in cadmium and lead contaminated soils. Plant Growth Regul 66:9–26

    Article  CAS  Google Scholar 

  • Ghnaya T, Mnassri M, Ghabriche R, Wali M, Poschenrieder C, Lutts S, Abdelly C (2015) Nodulation by Sinorhizobiummeliloti originated from a mining soil alleviates Cd toxicity and increases Cd-phytoextraction in Medicago sativa L. Front Plant Sci 6:863

    Article  PubMed  PubMed Central  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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gramss G, Voigt KD (2015) Regulation of the mineral concentrations in pea seeds from uranium mine and reference soils diverging extremely in their heavy metal load. Sci Hortic 194:255–266

    Article  CAS  Google Scholar 

  • Gunatilake SK (2015) Methods of removing heavy metals from industrial wastewater. J Multidiscip Eng Sci Stud (JMESS) 1:2912–1309

    Google Scholar 

  • Gupta P, Jain M, Sarangthem J, Gadre R (2013) Inhibition of 5-aminolevulinic acid dehydratase by mercury in excised greening maize leaf segments. Plant Physiol Biochem 62:63–69

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Wang R, Yang Z, Zhan Y, Ma Y, Ping S, Zhang L, Lin M, Yan Y (2015) 1-aminocyclopropane-1-carboxylate deaminase from Pseudomonas stutzeri A1501 facilitates the growth of rice in the presence of salt or heavy metals. J Microbiol Biotechnol 25:1119–1128

    Article  CAS  PubMed  Google Scholar 

  • Hao X, Xie P, Zhu YG, Taghavi S, Wei G, Rensing C (2015) Copper tolerance mechanisms of Mesorhizobium amorphae and its role in aiding phytostabilization by Robinia pseudoacacia in copper contaminated soil. Environ Sci Technol 49:2328–2340

    Article  CAS  PubMed  Google Scholar 

  • Hardiman RT, Banin A, Jacoby B (1984) The effect of soil type and degree of metal contamination upon uptake of Cd, Pb and Cu in bush beans (Phaseolus vulgaris L.) Plant Soil 81:17–27

    Article  CAS  Google Scholar 

  • Hosam EAF, Hamuda B, Orosz E, Hamuda Y, Tóth N, Kecskés M (2009) Vicia fabaRhizobium leguminosarum system symbiotic relationship under stress of soil pH and aluminium. Tájökológiai Lapok 7:301–318

    Google Scholar 

  • Imada EL, de Oliveira ALM, Hungria M, Rodrigues EP (2016) Indole-3-acetic acid production via the indole-3-pyruvate pathway by plant growth promoter Rhizobium tropici CIAT 899 is strongly inhibited by ammonium. Microbiol Res 168:283–292

    Google Scholar 

  • Islam MS, Ahmed MK, Raknuzzaman M, Habibullah-Al-Mamun M, Islam MK (2015) Heavy metal pollution in surface water and sediment: a preliminary assessment of an urban river in a developing country. Ecological Indicators 48:282–291

    Google Scholar 

  • Joshi FR (2016) Studies on siderophore mediated iron uptake system in rhizobacteria and expression of fegA gene from Bradyrhizobium japonicum 61A152 in commercial rhizobial inocula impact on competitive survival in rhizosphere. Curr Microbiol 53:141–147

    Article  CAS  Google Scholar 

  • Joshi SR, Kalita D, Kumar R, Nongkhlaw M, Swer PB (2014) Metal–microbe interaction and bioremediation. In: Radionuclide contamination and remediation through plants. Springer International, Cham, pp 235–251

    Google Scholar 

  • Kandziora-Ciupa M, Ciepał R, Nadgórska-Socha A, Barczyk G (2016) Accumulation of heavy metals and antioxidant responses in Pinus sylvestris L. needles in polluted and non-polluted sites. Ecotoxicology 25:970–981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang SM, Radhakrishnan R, You YH, Khan AL, Lee KE, Lee JD, Lee IJ (2015) Enterobacter asburiae KE17 association regulates physiological changes and mitigates the toxic effects of heavy metals in soybean. Plant Biol 17:1013–1022

    Article  CAS  PubMed  Google Scholar 

  • Karthik C, Oves M, Thangabalu R, Sharma R, Santhosh SB, Arulselvi PI (2016a) Cellulosimicrobium funkei-like enhances the growth of Phaseolus vulgaris by modulating oxidative damage under Chromium (VI) toxicity. J Adv Res 7:839–850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karthik C, Oves M, Sathya K, Sri Ramkumar V, Arulselvi PI (2016b). Isolation and characterization of multi-potential Rhizobium strain ND2 and its plant growth-promoting activities under Cr (VI) stress. Arch Agron Soil Sci 1–12

    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. J Ind Bot Soc 81:255–263

    Google Scholar 

  • Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19

    Article  CAS  Google Scholar 

  • Kinkle BK, Sadowsky MJ, Johnston K, Koskinen WC (1994) Tellurium and Selenium resistance in rhizobia and its potential use for direct isolation R. meliloti from soil. Appl Environ Microbiol 60:1674–1677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klimek B, Sitarz A, Choczyński M, Niklińska M (2016) The effects of heavy metals and total petroleum hydrocarbons on soil bacterial activity and functional diversity in the upper silesia industrial region (Poland). Water Air Soil Pollut 227:1–9

    Article  CAS  Google Scholar 

  • Kong Z, Glick BR, Duan J, Ding S, Tian J, McConkey BJ, Wei G (2015a) Effects of 1-aminocyclopropane-1-carboxylate (ACC) deaminase-overproducing Sinorhizobium meliloti on plant growth and copper tolerance of Medicago lupulina. Plant Soil 391:383–398

    Article  CAS  Google Scholar 

  • Kong Z, Mohamad OA, Deng Z, Liu X, Glick BR, Wei G (2015b) Rhizobial symbiosis effect on the growth, metal uptake, and antioxidant responses of Medicago lupulina under copper stress. Environ Sci Pollut Res 22:12479–12489

    Article  CAS  Google Scholar 

  • Kopittke PM, Dart PJ, Menzies NW (2007) Toxic effects of low concentrations of Cu on nodulation of cowpea (Vigna unguiculata). Environ Pollut 145:309–315

    Google Scholar 

  • Kraepiel AM, Bellenger JP, Wichard T, Morel FM (2009) Multiple roles of siderophores in free-living nitrogen-fixing bacteria. Biometals 22(4):573–581

    Article  CAS  PubMed  Google Scholar 

  • Lafuente A, Pajuelo E, Caviedes MA, Rodríguez-Llorente ID (2010) Reduced nodulation in alfalfa induced by arsenic correlates with altered expression of early nodulins. J Plant Physiol 167:286–291

    Article  CAS  PubMed  Google Scholar 

  • Lakzian A, Murphy P, Turner A, Beynon JL, Giller KE (2002) Rhizobium leguminosarum bv. viciae populations in soils with increasing heavy metal contamination: abundance, plasmid pro- files, diversity and metal tolerance. Soil Biol Biochem 34:519–529

    Article  CAS  Google Scholar 

  • Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils; a review. Environ Pollut 153:497–522

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Ma Z, Hao X, Rensing C, Wei G (2014) Genes conferring copper resistance in Sinorhizobium meliloti CCNWSX0020 also promote the growth of Medicago lupulina in copper-contaminated soil. Appl Environ Microbiol 80:1961–1971

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu M, Li Z, Liang J, Wei Y, Rensing C, Wei G (2016) Zinc resistance mechanisms of P1B-type ATPases in Sinorhizobium meliloti CCNWSX0020. Sci Rep 6:29355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo L, Shen Y, Liu J, Zeng Y (2016) Investigation of Pb species in soils, celery and duckweed by synchrotron radiation X-ray absorption near-edge structure spectrometry. Spectrochim Acta B At Spectrosc 122:40–45

    Article  CAS  Google Scholar 

  • Ma Y, Oliveira RS, Freitas H, Zhang C (2016) Biochemical and molecular mechanisms of plant-microbe-metal interactions: relevance for phytoremediation. Front Plant Sci 7:918

    PubMed  PubMed Central  Google Scholar 

  • Mamindy-Pajany Y, Sayen S, Mosselmans JFW, Guillon E (2014) Copper, nickel and zinc speciation in a biosolid-amended soil: pH adsorption edge, μ-XRF and μ-XANES investigations. Environ Sci Technol 48:7237–7244

    Article  CAS  PubMed  Google Scholar 

  • Manohari R, Yogalakshmi KN (2016) Optimization of Copper (II) removal by response surface methodology using root nodule endophytic bacteria isolated from Vigna unguiculata. Water Air Soil Pollut 227:285

    Article  CAS  Google Scholar 

  • Marino D, Damiani I, Gucciardo S, Mijangos I, Pauly N, Puppo A (2013) Inhibition of nitrogen fixation in symbiotic Medicago truncatula upon Cd exposure is a local process involving leghemoglobin. J Exp Bot 64:5651–5660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGrath SP, Brookes PC, Giller KE (1988) Effects of potentially toxic metals in soil derived from past applications of sewage sludge on nitrogen fixation by Trifolium repens L. Soil Biol Biochem 20:415–424

    Article  CAS  Google Scholar 

  • Miličić B, Delić D, Stajković O, Rasulić N, Kuzmanović Đ, Jošić D (2006) Effects of heavy metals on rhizobial growth. Roum Biotechnol Lett 11:2995–3003

    Google Scholar 

  • Miransari M (2011) Soil microbes and plant fertilization. Appl Microbiol Biotechnol 92:875–885

    Article  CAS  PubMed  Google Scholar 

  • Mishra S, Alfeld M, Sobotka R, Andresen E, Falkenberg G, Küpper H (2016) Analysis of sublethal arsenic toxicity to Ceratophyllum demersum: subcellular distribution of arsenic and inhibition of chlorophyll biosynthesis. J Exp Bot 67:4639–4646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohamad R, Maynaud G, Le Quéré A, Vidal C, Klonowska A, Yashiro E, Cleyet-Marel JC, Brunel B (2017) Ancient heavy metal contamination in soils as a driver of tolerant Anthyllis vulneraria rhizobial communities. Appl Environ Microbiol 83:1735–1716

    Article  Google Scholar 

  • Muneer S, Kim TH, Qureshi MI (2012) Fe modulates Cd-induced oxidative stress and the expression of stress responsive proteins in the nodules of Vigna radiata. Plant Growth Regul 68:421–433

    Article  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255

    Article  CAS  PubMed  Google Scholar 

  • Nascimento FX, Rossi MJ, Glick BR (2016) Role of ACC deaminase in stress control of leguminous plants. In: Plant growth promoting Actinobacteria. Springer, Singapore, pp 179–192

    Chapter  Google Scholar 

  • Nautiyal N, Sinha P (2012) Lead induced antioxidant defense system in pigeon pea and its impact on yield and quality of seeds. Acta Physiol Plant 34:977–983

    Article  CAS  Google Scholar 

  • Neumann H, Bode-Kirchhoff A, Madeheim A, Wetzel A (1998) Toxicity testing of heavy metals with the Rhizobium-legume symbiosis: high sensitivity to cadmium and arsenic compounds. Environ Sci Pollut Res 5:28–36

    Article  CAS  Google Scholar 

  • Nies DH (1995) The cobalt, zinc, and cadmium efflux system CzcABC from Alcaligenes eutrophus functions as a cation-proton antiporter in Escherichia coli. J Bacteriol 177:2707–2712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339

    Article  CAS  PubMed  Google Scholar 

  • Nocelli N, Bogino PC, Banchio E, Giordano W (2016) Roles of extracellular polysaccharides and biofilm formation in heavy metal resistance of rhizobia. Materials 9:418

    Article  PubMed Central  Google Scholar 

  • Nonnoi F, Chinnaswamy A, de la Torre VSG, de la Pena TC, 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 

  • Octive JC, Johnson AC, Wood M (1994) Effects of previous aluminium exposure on motility and nodulation by Rhizobium and Bradyrhizobium. Soil Biol Biochem 26:1477–1482

    Article  CAS  Google Scholar 

  • Oves M, Khan MS, Zaidi A (2013) Chromium reducing and plant growth promoting novel strain Pseudomonas aeruginosa OSG41 enhance chickpea growth in chromium amended soils. Eur J Soil Biol 56:72–83

    Article  CAS  Google Scholar 

  • Pajuelo E, Pérez-Palacios P, Romero-Aguilar A, Delgadillo J, Doukkali B, Rodríguez-Llorente ID, Caviedes MA (2016) Improving legume–rhizobium symbiosis for copper phytostabilization through genetic manipulation of both symbionts. In: Biological nitrogen fixation and beneficial plant-microbe interaction. Springer International, Cham, pp 183–193

    Chapter  Google Scholar 

  • Panigrahi DP, Sagar A, Dalal S, Randhawa GS (2013) Arsenic resistance and symbiotic efficiencies of alfalfa and cowpea rhizobial strains isolated from arsenic free agricultural fields. Eur J Exp Biol 3:322–333

    Google Scholar 

  • Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54:45

    Article  PubMed  PubMed Central  Google Scholar 

  • Paudyal SP, Aryal RR, Chauhan SVS, Maheshwari DK (2007) Effect of heavy metals on growth of rhizobium strains and symbiotic efficiency of two species of tropical legumes. Sci World 5:27–32

    Google Scholar 

  • Pérez-Palacios P, Agostini E, Ibáñez SG, Talano MA, Rodríguez-Llorente ID, Caviedes MA, Pajuelo E (2017) Removal of copper from aqueous solutions by rhizofiltration using genetically modified hairy roots expressing a bacterial Cu-binding protein. Environ Technol 1–12

    Google Scholar 

  • Petrova S, Yurukova L, Velcheva I (2013) Taraxacum officinale as a biomonitor of metals and toxic elements (Plovdiv, Bulgaria). Bulg J Agric Sci 19:241–247

    Google Scholar 

  • Pireh P, Yadavi A, Balouchi H (2017) Effect of cadmium chloride on soybean in presence of arbuscular mycorrhiza and vermicompost. Legum Res Int J 40:63–68

    Google Scholar 

  • Qing X, Yutong Z, Shenggao L (2015) Assessment of heavy metal pollution and human health risk in urban soils of steel industrial city (Anshan), Liaoning, Northeast China. Ecotoxicol Environ Saf 120:377–385

    Article  CAS  PubMed  Google Scholar 

  • Rai R, Agrawal M, Agrawal SB (2016) Impact of heavy metals on physiological processes of plants: with special reference to photosynthetic system. In: Plant responses to xenobiotics. Springer, Singapore, pp 127–140

    Chapter  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  PubMed  Google Scholar 

  • Rane MD, Shaikh EA, Malusare UG (2014) Effect of heavy metals on growth of Rhizobium. Int J Sci Eng Res 5:306–310

    Google Scholar 

  • Reichman SM (2007) The potential use of the legume–Rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol Biochem 39:2587–2593

    Article  CAS  Google Scholar 

  • Reis GS, de Almeida AA, de Almeida NM, de Castro AV, Mangabeira PA, Pirovani CP (2015) Molecular, biochemical and ultrastructural changes induced by Pb toxicity in seedlings of Theobroma cacao L. PLoS One 10:e0129696

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Romaniuk K, Dziewit L, Decewicz P, Mielnicki S, Radlinska M, Drewniak L (2017) Molecular characterization of the pSinB plasmid of the arsenite oxidizing, metallotolerant Sinorhizobium sp. M14–insight into the heavy metal resistome of sinorhizobial extrachromosomal replicons. FEMS Microbiol Ecol 93:fiw215

    Article  Google Scholar 

  • Rucińska-Sobkowiak R (2016) Water relations in plants subjected to heavy metal stresses. Acta Physiol Plant 38:257

    Article  CAS  Google Scholar 

  • Saadani O, FatnassiI C, Chiboub M, Abdelkrim S, Barhoumi F, Jebara M, Jebara SH (2016) In situ phytostabilisation capacity of three legumes and their associated plant growth promoting bacteria (PGPBs) in mine tailings of northern Tunisia. Ecotoxicol Environ Saf 130:263–269

    Article  CAS  PubMed  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    Article  CAS  PubMed  Google Scholar 

  • Sangwan P, Kumar V, Joshi UN (2014) Effect of chromium (VI) toxicity on enzymes of nitrogen metabolism in clusterbean (Cyamopsis tetragonoloba L.) Enzyme Res 2014:1–9

    Article  CAS  Google Scholar 

  • Sbabou L, Idir Y, Bruneel O, Le Quere A, Aurag J (2016) Characterization of root-nodule bacteria isolated from Hedysarum spinosissimum L, growing in mining sites of Northeastern region of Morocco. SOJ Microbiol Infect Dis 4:1–8

    Google Scholar 

  • Segura A, Ramos JL (2013) Plant–bacteria interactions in the removal of pollutants. Curr Opin Biotechnol 24:467–473

    Article  CAS  PubMed  Google Scholar 

  • Shvaleva A, de la Peña TC, Rincón A, Morcillo CN, de la Torre VSG, Lucas MM, Pueyo JJ (2010) Flavodoxin over expression reduces cadmium-induced damage in alfalfa root nodules. Plant Soil 326:109–121

    Article  CAS  Google Scholar 

  • Singh AK, Singh G (2015) A study of multiple heavy metal tolerance in root nodulating bacteria. Int J Res Dev Pharm Life Sci 4:1713–1721

    Google Scholar 

  • Singh Y, Ramteke PW, Shukla PK (2013) Characterization of Rhizobium isolates of pigeon pea rhizosphere from Allahabad soils and their potential PGPR characteristics. Int J Res Pure Appl Microbiol 3:4–7

    Google Scholar 

  • Singh RP, Shelke GM, Kumar A, Jha PN (2015) Biochemistry and genetics of ACC deaminase: a weapon to “stress ethylene” produced in plants. Front Microbiol 6:937

    PubMed  PubMed Central  Google Scholar 

  • Soni SK, Singh R, Singh M, Awasthi A, Wasnik K, Kalra A (2014) Pretreatment of Cr (VI)-amended soil with chromate-reducing rhizobacteria decreases plant toxicity and increases the yield of Pisum sativum. Arch Environ Contam Toxicol 66:616–627

    Article  CAS  PubMed  Google Scholar 

  • Stan V, Gament E, Cornea CP, Voaides C, Dusa M, Plopeanu G (2011) Effects of heavy metal from polluted soils on the Rhizobium diversity. Not Bot Hort Agrobot Cluj 39:88–95

    CAS  Google Scholar 

  • Talano MA, Cejas RB, González PS, Agostini E (2013) Arsenic effect on the model crop symbiosis Bradyrhizobium–soybean. Plant Physiol Biochem 63:8–14

    Article  CAS  PubMed  Google Scholar 

  • Tamas MJ, Sharma SK, Ibstedt S, Jacobson T, Christen P (2014) Heavy metals and metalloids as a cause for protein misfolding and aggregation. Biomol Ther 4:252–267

    Google Scholar 

  • Teng Y, Wang X, Li L, Li Z, Luo Y (2015) Rhizobia and their bio-partners as novel drivers for functional remediation in contaminated soils. Front Plant Sci 6:32

    Article  PubMed  PubMed Central  Google Scholar 

  • Tittabutr P, Awaya JD, Li QX, Borthakur D (2008) The cloned 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene from Sinorhizobium sp. strain BL3 in Rhizobium sp. strain TAL1145 promotes nodulation and growth of Leucaena leucocephala. Syst Appl Microbiol 31:141–150

    Article  CAS  PubMed  Google Scholar 

  • Ullah A, Heng S, Munis MFH, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40

    Article  CAS  Google Scholar 

  • Van Assche F, Clijsters H (1990) Effects of heavy metals on enzyme activity in plants. Plant Cell Environ 13:195–206

    Article  CAS  Google Scholar 

  • Velez PA, Talano MA, Paisio CE, Agostini E, González PS (2016) Synergistic effect of chickpea plants and Mesorhizobium as a natural system for chromium phytoremediation. Environ Technol 1–9

    Google Scholar 

  • Wakelin SA, Cavanagh JAE, Young S, Gray CW, van Ham RJC (2016) Cadmium in New Zealand pasture soils: toxicity to Rhizobia and white clover. N Z J Agric Res 59:65–78

    Article  CAS  Google Scholar 

  • Wang Y, Shi J, Wang H, Lin Q, Chen X, Chen Y (2007) The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicol Environ Saf 67:75–81

    Article  CAS  PubMed  Google Scholar 

  • Wani PA, Khan MS (2012) Bioremediaiton of lead by a plant growth promoting Rhizobium species RL9. J Bacteriol 2:66–78

    Google Scholar 

  • Wani PA, Khan MS (2013a) Isolation of multiple metal and antibiotic resistant mesorhizobium species and their plant growth promoting activity. Res J Microbiol 8:25–35

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS (2013b) Nickel detoxification and plant growth promotion by multi metal resistant plant growth promoting Rhizobium species RL9. Bull Environ Contam Toxicol 91:117–124

    Article  CAS  PubMed  Google Scholar 

  • Wani PA, Khan MS (2014) Screening of multiple metal and antibiotic resistant isolates and their plant growth promoting activity. Pak J Biol Sci 17:206–212

    Article  CAS  PubMed  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2008) Effects of heavy metal toxicity on growth, symbiosis, seed yield and metal uptake in pea grown in metal amended soil. Bull Environ Contam Toxicol 81:152–158

    Article  CAS  PubMed  Google Scholar 

  • Xie P, Hao X, Herzberg M, Luo Y, Nies DH, Wei G (2015) Genomic analyses of metal resistance genes in three plant growth promoting bacteria of legume plants in Northwest mine tailings, China. J Environ Sci 27:179–187

    Article  Google Scholar 

  • Xie Y, Fan J, Zhu W, Amombo E, Lou Y, Chen L, Fu J (2016) Effect of heavy metals pollution on soil microbial diversity and Bermudagrass genetic variation. Front Plant Sci 7:755

    PubMed  PubMed Central  Google Scholar 

  • Yu X, Li Y, Zhang C, Liu H, Liu J, Zheng W, Kang X, Leng X, Zhao K, Gu Y, Zhang X (2014) Culturable heavy metal-resistant and plant growth promoting bacteria in V-Ti magnetite mine tailing soil from Panzhihua, China. PLoS One 9:e106618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu X, Li Y, Cui Y, Liu R, Li Y, Chen Q, Gu Y, Zhao K, Xiang Q, Xu K, Zhang X (2016a) An indoleacetic acid producing Ochrobactrum sp. MGJ11 counteracts cadmium effect on soybean by promoting plant growth. J Appl Microbiol 122(4):987–996. doi:10.1111/jam.13379

    Article  CAS  Google Scholar 

  • Yu X, Li Y, Li Y, Xu C, Cui Y, Xiang Q, Gu Y, Zhao K, Zhang X, Penttinen P, Chen Q (2016b) Pongamia pinnata inoculated with Bradyrhizobium liaoningense PZHK1 shows potential for phytoremediation of mine tailings. Appl Microbiol Biotechnol 101:1739–1751

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Miró M, Kolev SD (2015) Hybrid flow system for automatic dynamic fractionation and speciation of inorganic arsenic in environmental solids. Environ Sci Technol 49:2733–2740

    Article  CAS  PubMed  Google Scholar 

  • Zribi K, Nouairi I, Slama I, Talbi-Zribi O, Mhadhbi H (2015) Medicago sativa-Sinorhizobium meliloti symbiosis promotes the bioaccumulation of zinc in nodulated roots. Int J Phytoremediation 17:49–55

    Article  CAS  PubMed  Google Scholar 

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Saif, S., Zaidi, A., Khan, M.S., Rizvi, A. (2017). Metal-Legume-Microbe Interactions: Toxicity and Remediation. In: Zaidi, A., Khan, M., Musarrat, J. (eds) Microbes for Legume Improvement. Springer, Cham. https://doi.org/10.1007/978-3-319-59174-2_15

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