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Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils

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Abstract

Heavy metal pollution of soil is a significant environmental problem and has its negative impact on human health and agriculture. Rhizosphere, as an important interface of soil and plant, plays a significant role in phytoremediation of contaminated soil by heavy metals, in which, microbial populations are known to affect heavy metal mobility and availability to the plant through release of chelating agents, acidification, phosphate solubilization and redox changes, and therefore, have potential to enhance phytoremediation processes. Phytoremediation strategies with appropriate heavy metal-adapted rhizobacteria have received more and more attention. This article paper reviews some recent advances in effect and significance of rhizobacteria in phytoremediation of heavy metal contaminated soils. There is also a need to improve our understanding of the mechanisms involved in the transfer and mobilization of heavy metals by rhizobacteria and to conduct research on the selection of microbial isolates from rhizosphere of plants growing on heavy metal contaminated soils for specific restoration programmes.

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References

  • Abou-Shanab, R.A., Angle, J.S., Delorme, T.A., Chaney, R.L., van Berkum, P., Moawad, H., Ghanem, K., Ghozlan, H.A., 2003a. Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. N. Phytol., 158(1):219–224. [doi:10.1046/j.1469-8137.2003.00721.x]

    Article  CAS  Google Scholar 

  • Abou-Shanab, R.A., Delorme, T.A., Angle, J.S., Chaney, R.L., Ghanem, K., Moawad, H., Ghozlan, H.A., 2003b. Phenotypic characterization of microbes in the rhizosphere of Alyssum murale. Int. J. Phytoremediation, 5(4):367–379. [doi:10.1080/16226510390268766]

    Article  PubMed  CAS  Google Scholar 

  • Abou-Shanab, R.A., Ghozlan, H., Ghanem, K., Moawad, H., 2005. Behaviour of bacterial populations isolated from rhizosphere of Diplachne fusca dominant in industrial sites. World J. Microbiol. Biotechnol., 21(6–7):1095–1101. [doi:10.1007/s11274-004-0005-6]

    Article  CAS  Google Scholar 

  • Aleem, A., Isar, J., Malik, A., 2003. Impact of long-term application of industrial wastewater on the emergence of resistance traits in Azotobacter chroococcum isolated from rhizospheric soil. Bioresour. Technol., 86(1):7–13. [doi:10.1016/S0960-8524(02)00134-7]

    Article  PubMed  CAS  Google Scholar 

  • Alkorta, I., Garbisu, C., 2001. Phytoremediation of organic contaminants. Bioresour. Technol., 79(3):273–276. [doi:10.1016/S0960-8524(01)00016-5]

    Article  PubMed  CAS  Google Scholar 

  • Alstrom, S., 1991. Induction of disease resistance in common bean susceptible to halo blight bacterial pathogen after seed bacterization with rhizosphere pseudomonads. J. Gen. Appl. Microbiol., 37(6):495–501.

    Google Scholar 

  • Anderson, T.A., Guthrie, E.A., Walton, B.T., 1993. Bioremediation in the rhizosphere: plant roots and associated microbes clean contaminated soil. Environ. Sci. Technol., 27(13):2630–2636. [doi:10.1021/es00049a001]

    Article  CAS  Google Scholar 

  • Barber, S.A., Lee, R.B., 1974. The effect of microorganisms on the absorption of manganese by plants. N. Phytol., 73(1):97–106. [doi:10.1111/j.1469-8137.1974.tb04610.x]

    Article  CAS  Google Scholar 

  • Bar-Ness, E., Chen, Y., Hadar, Y., Marchner, H., Romheld, V., 1991. Siderophores of Pseudomonas putida as an iron source for dicot and monocot plants. Plant Soil, 130(1–2):231–241. [doi:10.1007/BF00011878]

    Article  CAS  Google Scholar 

  • Bar-Ness, E., Hadar, Y., Chen, Y., Shanzer, A., Libman, J., 1992. Iron uptake by plant from microbial siderophores. Plant Physiol., 99(4):1329–1335.

    PubMed  CAS  Google Scholar 

  • Belimov, A.A., Kunakova, A.M., Gruzdeva, E.V., 1998. Influence of soil pH on the interaction of associative bacteria with barley. Microbiology (Moscow), 67(4):463–469.

    CAS  Google Scholar 

  • Belimov, A.A., Safronova, V.I., Sergeyeva, T.A., Egorova, T.N., Matveyeva, V.A., Tsyganov, V.E., Borisov, A.Y., Tikhonovich, I.A., Kluge, C., Preisfeld, A., et al., 2001. Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can. J. Microbiol., 47(7):642–652. [doi:10.1139/cjm-47-7-642]

    Article  PubMed  CAS  Google Scholar 

  • Belimov, A.A., Safronova, V.I., Mimura, T., 2002. Response of spring rape to inoculation with plant growth-promoting rhizobacteria containing 1-aminocyclopropane-1-car-boxylate deaminase depends on nutrient status of the plant. Can. J. Microbiol., 48(3):189–199. [doi:10.1139/w02-007]

    Article  PubMed  CAS  Google Scholar 

  • Belimov, A.A., Kunakova, A.M., Safronova, V.I., Stepanok, V.V., Yudkin, L.Y., Alekseev, Y.V., Kozhemyakov, A.P., 2004. Employment of rhizobacteria for the inoculation of barley plants cultivated in soil contaminated with lead and cadmium. Microbiology (Moscow), 73(1):99–106.

    CAS  Google Scholar 

  • Belimov, A.A., Hontzeas, N., Safronova, V.I., Demchinskaya, S.V., Piluzza, G., Bullitta, S., Glick, B.R., 2005. Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol. Biochem., 37(2):241–250. [doi:10.1016/j.soilbio.2004.07.033]

    Article  CAS  Google Scholar 

  • Bewley, J.D., Black, M., 1985. Dormaney and the Control of Germination, Seeds: Physiology of Development and Germination. Plenum Press, New York, p.175–235.

    Google Scholar 

  • Bingham, F.T., Pereyea, F.J., Jarrell, W.M., 1986. Metal toxicity to agricultural crops. Metal Ions Biol. Syst., 20:119–156.

    CAS  Google Scholar 

  • Blake, R.C., Choate, D.M., Bardhan, S., Revis, N., Barton, L.L., Zocco, T.G., 1993. Chemical transformation of toxic metals by a Pseudomonas strain from a toxic waste site. Environ. Toxicol. Chem., 12(5):1365–1376.

    CAS  Google Scholar 

  • Bogardt, A.H., Hemmingsen, B.B., 1992. Enumeration of phenanthracene-degrading bacteria by an overlayer technique and its use in the evaluation of petroleum-contaminated sites. Appl. Environ. Microbiol., 58(7):2579–2582.

    PubMed  CAS  Google Scholar 

  • Bollard, E.G., 1983. Involvement of Unusual Elements in Plant Growth and Nutrition. In: Lauchli, A., Bielsky, R.L. (Eds.), Inorganic Plant Nutrition. Encyclopedia of Plant Physiology, Vol. 15B. Springer-Verlag KG, Berlin, Germany, p.695–744.

    Google Scholar 

  • Borowitz, J.J., Stankie-Diez, M., Lewicka, T., Zukowska, Z., 1992. Inhibition of fungal cellulase, pectinase and xylanase activity of plant growth promoting fluorescent pseudomonads. Bull. OILB/SROP, 15(4):103–106.

    Google Scholar 

  • Bradley, R., Burt, A.J., Read, D.J., 1982. The biology of mycorrhyza in the Ericaceae. VIII. The role of mycorrhyzal infection in heavy metal resistance. N. Phytol., 91(2):197–202. [doi:10.1111/j.1469-8137.1982.tb03306.x]

    Article  CAS  Google Scholar 

  • Brookes, P.C., McGrath, S.P., 1984. Effects of metal toxicity on the size of the soil microbial biomass. Eur. J. Soil Sci., 35(2):341–346. [doi:10.1111/j.1365-2389.1984.tb00288.x]

    Article  CAS  Google Scholar 

  • Brown, M.T., Wilkins, D.A., 1985. Zinc tolerance of mycorrhyial Betula. N. Phytol., 99(1):101–106. [doi:10.1111/j.1469-8137.1985.tb03640.x]

    Article  CAS  Google Scholar 

  • Budzikiewicz, H., 1997. Siderophores of fluorescent Pseudomonas L. Nat. Foresche, 52C:413–420.

    Google Scholar 

  • Burd, G.I., Dixon, D.G., Glick, B.R., 1998. A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl. Environ. Microbiol., 64(3):3663–3668.

    PubMed  CAS  Google Scholar 

  • Burd, G.I., Dixon, D.G., Glick, B.R., 2000. Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can. J. Microbiol., 46(3):237–245. [doi:10.1139/cjm-46-3-237]

    Article  PubMed  CAS  Google Scholar 

  • Chander, K., Brookes, P.C., 1991. Effects of heavy metals from past applications of sewage sluge on microbial biomass and organic matter accumulaiton in a sandy loam soil and silty loam UK soil. Soil Biol. Biochem., 23(10):927–932. [doi:10.1016/0038-0717(91)90172-G]

    Article  Google Scholar 

  • Chaney, R.L., Brown, S.L., Li, Y.M., Angle, J.S., Stuczynski, T.I., Daniel, W.L., Henry, C.L., Siebelec, G., Malik, M., Ryan, J.A., et al., 2000. Progress in Risk Assessment for Soil Metals, and In-situ Remediation and Phytoextraction of Metals from Hazardous Contaminated Soils. US-EPA “Phytoremediation: State of Science”, 2000 May 1–2, Boston, MA.

  • Chaudri, A.M., McGrath, S.P., Giller, K.E., 1992. Survival of the indigenous population of Rhizobium leguminosarum biovar trifolii in soil spiked with Cd, Zn, Cu and Ni salts. Soil Biol. Biochem., 24(7):625–632. [doi:10.1016/0038-0717(92)90040-5]

    Article  CAS  Google Scholar 

  • Cheng, S., Grosse, W., Karrenbrock, F., Thoennessen, M., 2002. Efficiency of constructed wetlands in decontamination of water polluted by heavy metals. Ecol. Eng., 18(3):317–325. [doi:10.1016/S0925-8574(01)00091-X]

    Article  Google Scholar 

  • Claverys, J.P., 2001. A new family of high-affinity ABC manganese and zinc permeases. Res. Microbiol., 152(3–4):231–243. [doi:10.1016/S0923-2508(01)01195-0]

    Article  PubMed  CAS  Google Scholar 

  • Crowley, D.E., Wang, Y.C., Reid, C.P.P., Szansiszlo, P.J., 1991. Mechanism of iron acquisition from siderophores by microorganisms and plants. Plant Soil, 130(1–2):179–198. [doi:10.1007/BF00011873]

    Article  CAS  Google Scholar 

  • Cunningham, S.D., Berti, W.R., 1993. Remediation of contaminated soils with green plants: an overview. In Vitro Cell Dev. Biol., 29(4):207–212.

    Google Scholar 

  • Cunningham, S.D., Ow, D.W., 1996. Promises and prospects of phytoremediation. Plant. Physiol., 110(5):715–719.

    PubMed  CAS  Google Scholar 

  • Cunningham, S.D., Berti, W.R., Huang, J.W., 1995. Phytoremediation of contaminated soils. Trends Biotechnol., 13(9):393–397. [doi:10.1016/S0167-7799(00)88987-8]

    Article  CAS  Google Scholar 

  • Davies, F.T.Jr, Puryear, J.D., Newton, R.J., 2001. Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). J. Plant Physiol., 158(6):777–786. [doi:10.1078/0176-1617-00311]

    Article  CAS  Google Scholar 

  • de Souza, M.P., Chu, D., Zhao, M., Zayed, A.M., Ruzin, S.E., Schichnes, D., Terry, N., 1999a. Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard. Plant Physiol., 119(2):565–573. [doi:10.1104/pp.119.2.565]

    Article  PubMed  Google Scholar 

  • de Souza, M.P., Huang, C.P., Chee, N., Terry, N., 1999b. Rhizosphere bacteria enhance the accumulation of selenium and mercury in wetland plants. Planta, 209(2):259–263. [doi:10.1007/s004250050630]

    Article  PubMed  Google Scholar 

  • Défago, G., Berling, C.H., Burger, U., Hass, D., Kahr, G., Keel, C., Voisard, C., Wirthner, P., Wuthrich, B., 1990. Suppression of Black Root Rot of Tobacco and Other Root Diseases by Strains of Pseudomonas fluorescens: Potential Applications and Mechanisms. In: Hornby, D. (Ed.), Biological Control of Soilborne Plant Pathogens. CAB International, Wellingford, Oxon, UK, p.93–108.

    Google Scholar 

  • Dell’Amico, 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(2):153–162. [doi:10.1016/j.femsec.2004.11.005]

    Article  PubMed  CAS  Google Scholar 

  • Delorme, T.A., Gagliardi, J.V., Angle, J.S., Chaney, R.L., 2001. Influence of the zinc hyperaccumulator Thalaspi caerulescens J. and C. Presl and the nonmetal accumulator Trifolium pratense L. on soil microbial populations. Can. J. Microbiol., 47(8):773–776. [doi:10.1139/cjm-47-8-773]

    Article  PubMed  CAS  Google Scholar 

  • Dueck, T.A., Visser, P., Ernest, W.H.O., Schat, H., 1986. Vesiculararbuscular mycorrhyzae decrease zinc toxicity to grasses in zinc polluted soil. Soil Biol. Biochem., 18(3):331–333. [doi:10.1016/0038-0717(86)90070-2]

    Article  Google Scholar 

  • Duffy, B.K., Défago, G., 1997. Zine improves biocontrol of Fusarium crown and root rot of tomato by Pseudomonas fluorescens and represses the production of pathogen metabolites inhibitory to bacterial antibiotic biosynthesis. Phytopathology, 87(12):1250–1257.

    CAS  PubMed  Google Scholar 

  • Duffy, B.K., Défago, G., 1999. Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol., 65(6):2429–2438.

    PubMed  CAS  Google Scholar 

  • Egamberdiyeva, D., Höflich, G., 2004. Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. J Arid Environ., 56(2):293–301. [doi:10.1016/S0140-1963(03)00050-8]

    Article  Google Scholar 

  • Elad, Y., Baker, R., 1985. The role of competition for iron and carbon in suppression of chlamydospore germination of Fusarium oxysporum. Phytopathology, 75:190–195.

    Google Scholar 

  • Elad, Y., Chet, I., 1987. Possible role of competition for nutrition in biocontrol of Pythium damping-off by bacteria. Phytopathology, 77:190–195.

    Google Scholar 

  • Ellis, R.J., Timms-Wilson, T.M., Bailey, M.J., 2000. Identification of conserved traits in fluorescent pseudomonads with antifungal activity. Environ. Microbiol., 2(3):274–284. [doi:10.1046/j.1462-2920.2000.00102.x]

    Article  PubMed  CAS  Google Scholar 

  • Elsgaard, L., Petersen, S.O., Debosz, K., 2001. Effects and risk assessment of linear alkylbenzene sulfonates in agricultural soil. 1. Short-term effects on soil microbiology. Environ. Toxicol Chem., 20(8):1656–1663. [doi:10.1897/1551-5028(2001)020〈1656:EARAOL〉2.0.CO;2]

    Article  PubMed  CAS  Google Scholar 

  • Ernst, W.H.O., 1996. Bioavailability of heavy metals and decontamination of soils by plants. Appl. Geochem., 11(1–2):163–167. [doi:10.1016/0883-2927(95)00040-2]

    Article  CAS  Google Scholar 

  • Filip, Z., 2002. International approach to assessing soil quality by ecologically-related biological parameters. Agric. Ecosyst. Environ., 88(2):689–712.

    Google Scholar 

  • Foy, C.D., Chaney, R.L., White, M.C., 1978. The physiology of metal toxicity in plants. Annu. Rev. Plant Physiol., 29(1):511–566. [doi:10.1146/annurev.pp.29.060178.002455]

    Article  CAS  Google Scholar 

  • Fridlender, M., Inbar, J., Chet, I., 1993. Biological control of soilborne plant pathogens by a β-1,3-glucanase-producing Pseudomonas cepacia. Soil Biol. Biochem., 25(9):1211–1221. [doi:10.1016/0038-0717(93)90217-Y]

    Article  CAS  Google Scholar 

  • Gadd, G.M., 1990. Heavy metal accumulation by bacteria and other microorganisms. Experientia, 46(8):834–840. [doi:10.1007/BF01935534]

    Article  CAS  Google Scholar 

  • Garbisu, C., Alkorta, I., 2001. Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresour. Technol., 77(3):229–236. [doi:10.1016/S0960-8524(00)00108-5]

    Article  PubMed  CAS  Google Scholar 

  • Garbisu, C., Hernandez-Allica, J., Barrutia, O., Alkorta, I., Becerril, J.M., 2002. Phytoremediation: a technology using green plants to remove contaminants from polluted areas. Rev. Environ. Health, 17(3):173–188.

    PubMed  CAS  Google Scholar 

  • Giller, K.E., Witter, E., McGrath, S.P., 1998. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils. Soil Biol. Biochem., 30(10–11):1389–1414. [doi:10.1016/S0038-0717(97)00270-8]

    Article  CAS  Google Scholar 

  • Glick, B.R., 1995. The enhancement of plant growth by free-living bacteria. Can. J. Microbiol., 41:109–117.

    CAS  Google Scholar 

  • Glick, B.R., 2003. Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol. Adv., 21(5):383–393. [doi:10.1016/S0734-9750(03)00055-7]

    Article  PubMed  CAS  Google Scholar 

  • Glick, B.R., Jacobson, C.B., Schwarze, M.M.K., Pasternak, J.J., 1994. 1-aminocyclopropane-1-carboxylic acid deaminase mutants of the plant growth promoting rhyzobacterium Pseudomonas putida GR 12-2 do not stimulate canola root elongation. Can. J. Microbiol., 40(2):911–915.

    CAS  Google Scholar 

  • Glick, B.R., Karaturovic, D.M., Newell, P.C., 1995. A novel procedure for rapid isolation of plant growth promoting pseudomonads. Can. J. Microbiol., 41(6):533–536.

    Article  CAS  Google Scholar 

  • Glick, B.R., Penrose, D.M., Li, J.P., 1998. A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J. Theor. Biol., 190(1):63–68. [doi:10.1006/jtbi.1997.0532]

    Article  PubMed  CAS  Google Scholar 

  • Glick, B.R., Patten, C.L., Holguin, G., Penrose, D.M., 1999. Biochemical and Genetic Mechanisms Used by Plant Growth-Promoting Bacteria. Imperial College Press, London.

    Google Scholar 

  • Gray, C.W., McLaren, R.G., Roberts, A.H.C., Condron, L.M., 1998. Sorption and desorption of cadmium from some New Zealand soils: effect of pH and contact time. Aust. J. Soil Res., 36(2):199–216. [doi:10.1071/S97085]

    Article  CAS  Google Scholar 

  • Gremion, F., Chatzinotas, A., Kaufmann, K., von Sigler, W., Harms, H., 2004. Impacts of heavy metal contamination and phytoremediation on a microbial community during a twelve-month microcosm experiment. FEMS Microbiol. Ecol., 48(2):273–283. [doi:10.1016/j.femsec.2004.02.004]

    Article  CAS  PubMed  Google Scholar 

  • Grichko, V.P., Glick, B.R., 2001. Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiol. Biochem., 39(1):11–17. [doi:10.1016/S0981-9428(00)01212-2]

    Article  CAS  Google Scholar 

  • Hall, J.A., Peirson, D., Ghosh, S., Glick, B.R., 1996. Root elongation in various agronomic crops by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Isr. J. Plant Sci., 44(2):37–42.

    Google Scholar 

  • Han, J.G., Sun, L., Dong, X.Z., Cai, Z.Q., Sun, X.L., Yang, H.L., Wang, Y.S., 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(1):66–76. [doi:10.1016/j.syapm.2004.09.003]

    Article  PubMed  CAS  Google Scholar 

  • Hasnain, S., Sabri, A.N., 1996. Growth Stimulation of Triticum Aestivum Seedlings under Cr-Stresses by Non Rhizospheric Pseudomonad Strains. Abstracts of the 7th International Symposium on Biological Nitrogen Fixation with Non-Legumes. Kluwer Academic Publishers, the Netherlands, p.36.

    Google Scholar 

  • Heggo, A., Angle, J.S., Chaney, R.L., 1990. Effect of vesicular-arbuscular mycorrhyzae fungi on heavy metal uptake by soybeans. Soil Biol. Biochem., 22(6):865–869. [doi:10.1016/0038-0717(90)90169-Z]

    Article  CAS  Google Scholar 

  • Hinsinger, P., 2001. Bioavailability of soil inorganic P in the rhizospere as affected by root-induced chemical changes: a review. Plant Soil, 237(2):173–195. [doi:10.1023/A:1013351617532]

    Article  CAS  Google Scholar 

  • Huang, Y., Tao, S., Chen, Y.J., 2005. The role of arbuscular mycorrhiza on change of heavy metal speciation in rhizosphere of maize in wastewater irrigated agriculture soil. J. Environ. Sci., 17(2):276–280 (in Chinese).

    CAS  Google Scholar 

  • Imsande, J., 1998. Iron, sulfur, and chlorophy II deficiencies: a need for an integrative approach in plant physiology. Physiologia Plantarum, 103(1):139–144. [doi:10.1034/j.1399-3054.1998.1030117.x]

    Article  CAS  Google Scholar 

  • Jacobson, C.B., Pasternak, J.J., Glick, B.R., 1994. Partial purification and characterization of the enzyme ACC deaminase from the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Can. J. Microbiol., 40(2):1019–1025.

    CAS  Google Scholar 

  • Jordan, M.J., LeChevalier, M.P., 1975. Effects of zinc-smelter emissions on forest soil microflora. Can. J. Microbiol., 21:1855–1865.

    Article  PubMed  CAS  Google Scholar 

  • Kabata-Pendias, A., Pendias, H., 1989. Trace Elements in the Soil and Plants. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Kamnev, A.A., 2003. Phytoremediation of Heavy Metals: An Overview. In: Fingerman, M., Nagabhushanam, R. (Eds.), Recent Advances in Marine Biotechnology, Vol. 8: Bioremediation. Science Publishers Inc., Enfield (NH), USA, p.269–317.

    Google Scholar 

  • Kamnev, A.A., Tugarova, A.V., Antonyuk, L.P., Tarantilis, P.A., Polissiou, M.G., Gardiner, P.H., 2005. Effects of heavy metals on plant-associated rhizobacteria: comparison of endophytic and non-endophytic strains of Azospirillum brasilense. J. Trace Elem. Med. Biol., 19(1): 91–95. [doi:10.1016/j.jtemb.2005.03.002]

    Article  PubMed  CAS  Google Scholar 

  • Kanazawa, K., Higuchi, K., Nishizawa, N.K., Fushiya, S., Chino, M., Mori, S., 1994. Nicotianamine aminotransferase activities are correlated to the phytosiderophore secretion under Fe-deficient conditions, in Gramineae. J. Exp. Bot., 45(12):1903–1906. [doi:10.1093/jxb/45.12.1903]

    Article  CAS  Google Scholar 

  • Kärenlampi, S., Schat, H., Vangronsveld, J., Verkleij, J.A.C., van der Lelie, D., Mergeay, M., Tervahauta, A.I., 2000. Genetic engineering in the improvement of plants for phytoremediation of metal polluted soils. Environ. Pollut., 107(2):225–231. [doi:10.1016/S0269-7491(99)00141-4]

    Article  PubMed  Google Scholar 

  • Killham, K., Firestone, M.K., 1983. Vesicular arbuscular mycorrhyzal mediation of grass response to acidic and heavy metal deposition. Plant Soil, 72(1):39–48. [doi:10.1007/BF02185092]

    Article  CAS  Google Scholar 

  • Kloepper, J.W., Schroth, M.N., Miller, T.D., 1980. Effects of rhizosphere colonization by plant growth promoting rhizobacteria on potato plant development and yield. Phytopathology, 70:1078–1082.

    Google Scholar 

  • Kloepper, J.W., Lifshitz, R., Zablotowicz, R.M., 1989. Free-living bacterial inocula for enhancing crop productivity. Trends. Biotechnol., 7(2):39–44. [doi:10.1016/0167-7799(89)90057-7]

    Article  Google Scholar 

  • Konopka, A., Zakharova, T., Bischoff, M., Oliver, L., Nakatsu, C., Turco, R.F., 1999. Microbial biomass and activity in lead-contaminated soil. Appl. Environ. Microbiol., 65(5):2256–2259.

    PubMed  CAS  Google Scholar 

  • Kumar, P.B.A., Dushenkov, V., Motto, H., Raskin, I., 1995. Phytoextraction: the use of plants to remove heavy metals from soils. Environ. Sci. Technol., 29(5):1232–1238. [doi:10.1021/es00005a014]

    Article  CAS  Google Scholar 

  • Lambrecht, M., Okon, Y., Vande Broek, A., Vanderleyden, J., 2000. Indole-3-acetic acid: a reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol., 8(7):298–300. [doi:10.1016/S0966-842X(00)01732-7]

    Article  PubMed  CAS  Google Scholar 

  • Lasat, H.A., 2002. Phytoextraction of toxic metals: a review of biological mechanisms. J. Environ. Qual., 31(1):109–120.

    PubMed  CAS  Google Scholar 

  • Leggett, J.E., Epstein, E., 1956. Kinetics of sulfate adsorption by barley roots. Plant Physiol., 31:222–226.

    PubMed  CAS  Google Scholar 

  • Lemanceau, P., Bakker, P.A.H.M., Dekogel, W.J., Alabouvette, C., Schippers, B., 1992. Effect of pseudobactin 358 produced by Pseudomonas putida WSC358 on suppression of Fusarium wilt of carnations by non pathogenic Fusarium oxysporum. Appl. Environ. Microbiol., 58(3):2978–2980.

    PubMed  CAS  Google Scholar 

  • Leong, J., 1986. Siderophores: their biochemistry and possible role in control of plant pathogens. Annu. Rev. Phytopathol., 24(1):187–209. [doi:10.1146/annurev.py.24.090186.001155]

    Article  CAS  Google Scholar 

  • Lim, H., Kim, Y., Kim, S., 1991. Pseudomonas stutzeri YLP-1 genetic transformation and antifungal mechanism against Fusarium solani, an agent of plant root rot. Appl. Environ. Microbiol., 57(2):510–516.

    PubMed  CAS  Google Scholar 

  • Liu, A., Hamel, C., Hamilton, R.I., Ma, B.L., Smith, D.L., 2000. Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza, 9(6):331–336. [doi:10.1007/s005720050277]

    Article  CAS  Google Scholar 

  • Lonergan, D.J., Jenter, H., Coates, J.D., Phillips, E.J.P., Schmidt, T., Lovley, D.R., 1996. Phylogenetic analysis of dissimilatory Fe(lll)-reducing bacteria. J. Bacterial., 176(3):2402–2408.

    Google Scholar 

  • Loper, J.E., Henkels, M.D., 1999. Utilization of heterologous siderophore enhances levels of iron available to Pseudomonas putida in rhizosphere. Appl. Environ. Microbiol., 65(12):5357–5363.

    PubMed  CAS  Google Scholar 

  • Lovley, D.R., 1993. Dissimilatory metal reduction. Annu. Rev. Microbial., 47(1):263–290. [doi:10.1146/annurev.mi.47.100193.001403]

    Article  CAS  Google Scholar 

  • Lovley, D.R., 1995. Bioremediation of organic and metal contaminants with dissimilatory metal reduction. J. Ind. Microbiol., 14(2):85–93. [doi:10.1007/BF01569889]

    Article  PubMed  CAS  Google Scholar 

  • Lovley, D.R., Coates, J.D., Saffarini, D.A., Lonergan, D.J., 1997. Dissimilatory Iron Reduction. In: Winkelman, G., Carrano, C.J. (Eds.), Iron and Related Transition Metals in Microbial Metabolism. Harwood Academic Publishers, New York.

    Google Scholar 

  • Ma, J.F., Nomoto, K., 1993. Inhibition of mugineic acid-ferric complex in barley by copper, zinc and cobalt. Physiologia Plantarum, 89(2):331–334. [doi:10.1034/j.1399-3054.1993.890213.x]

    Article  CAS  Google Scholar 

  • Marschner, H., 1995. Mineral Nutrition of Higher Plants. Academic Press, London, p.889.

    Google Scholar 

  • Masalha, J., Kosegarten, H., Elmaci, O., Mengal, K., 2000. The central role of microbial activity for iron acquisition in maize and sunflower. Biol. Fertil. Soils, 30(5–6):433–439. [doi:10.1007/s003740050021]

    Article  CAS  Google Scholar 

  • Mason, R.P., Reinfelder, J.R., Morel, F.M.M., 1996. Uptake, toxicity, and trophic transfer of mercury in a coastal diatom. Environ. Sci. Technol., 30(6):1835–1845. [doi:10.1021/es950373d]

    Article  CAS  Google Scholar 

  • Maurhofer, M., Reimmann, C., Sacherer, S.P., Heeb, S., Haas, D., Defago, G., 1998. Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology, 88(2):678–684.

    CAS  PubMed  Google Scholar 

  • Mayak, S., Tirosh, T., Glick, B.R., 1999. Effect of wild-type and mutant plant growth promoting rhizobacteria on the rooting of mung bean cuttings. J. Plant Growth Regul., 18(2):49–53. [doi:10.1007/PL00007047]

    Article  PubMed  CAS  Google Scholar 

  • Mayak, S., Tirosh, T., Glick, B.R., 2004a. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci., 166(2):525–530. [doi:10.1016/j.plantsci.2003.10.025]

    Article  CAS  Google Scholar 

  • Mayak, S., Tirosh, T., Glick, B.R., 2004b. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem., 42(6):565–572. [doi:10.1016/j.plaphy.2004.05.009]

    Article  PubMed  CAS  Google Scholar 

  • Mayer, A.M., Poljakoff-Mayber, A., 1989. The Germination of Seeds. Pergamon Press, Oxford.

    Google Scholar 

  • McGrath, S.P., 1994. Effects of Heavy Metals from Sewage Sludge on Soil Microbes in Agricultural Ecosystems. In: Ross, S.M. (Ed.), Toxic Metals in Soil-Plant Systems. Wiley, New York, p.247–273.

    Google Scholar 

  • McGrath, S.P., Chaudri, A.M., Giller, K.E., 1995. Long-term effects of metals in sewage sluge on soils, microorganisms and plants. J. Ind. Microbiol., 14(2):94–104. [doi:10.1007/BF01569890]

    Article  PubMed  CAS  Google Scholar 

  • McGrath, S.P., Zhao, F.J., Lombi, E., 2001. Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil, 232(1–2):207–214. [doi:10.1023/A:1010358708525]

    Article  CAS  Google Scholar 

  • Mengoni, A., Barzanti, R., Gonnelli, C., Gabbrielli, R., Bazzicalupo, M., 2001. Characterization of nickel-resistant bacteria isolated from serpentine soil. Environ.Microbiol., 3(11):691–698. [doi:10.1046/j.1462-2920.2001.00243.x]

    Article  PubMed  CAS  Google Scholar 

  • Meyer, J.M., 2000. Pyoverdines: pigments siderophores and potential taxonomic markers of fluorescent Pseudomonas species. Arch. Microbiol., 174(3):135–142. [doi:10.1007/s002030000188]

    Article  PubMed  CAS  Google Scholar 

  • Mishra, D., Kar, M., 1974. Nickel in plant growth and metabolism. Bot. Rev., 40:395–452.

    CAS  Google Scholar 

  • Nie, L., Shan, S., Rashid, A., Burd, G.I., George, D.D., Glich, B.R., 2002. Phytoremediation of arsenate contaminated soil by transgenic canola and the plant growth-promoting bacterium Enterobacter cloacae CAL2. Plant Physiol. Biochem., 40(4):355–361. [doi:10.1016/S0981-9428(02)01375-X]

    Article  CAS  Google Scholar 

  • Oostendorp, M., Sikora, R.A., 1989. Seed-treatment with antagonistic rhizobacteria for the suppression of Heterodera schachtii early root infection of sugar beet. Rev. Nematol., 12(1):77–83.

    Google Scholar 

  • Oostendorp, M., Sikora, R.A., 1990. In vitro interrelationship between rhizosphere bacteria and Heterodera schachtii. Rev. Nematol., 13(3):269–274.

    Google Scholar 

  • Pan, B., Bai, Y.M., Leibovitch, S., Smith, D.L., 1999. Plant-growth-promoting rhizobacteria and kinetin as ways to promote corn growth and yield in a short-growing-season area. Eur. J. Agron., 11(3–4):179–186. [doi:10.1016/S1161-0301(99)00029-5]

    Article  CAS  Google Scholar 

  • Park, C.H., Keyhan, M., Matin, A., 1999. Purification and characterization of chromate reductase in Pseudomonas putida. Abs. Gen. Meet. American Soc. Microbial., 99(4):536–548.

    Google Scholar 

  • Patten, C.I., Glick, B.R., 1996. Bacterial biosynthesis of indole-3-acetic acid. Can. J. Microbiol., 42(3):207–220.

    Article  PubMed  CAS  Google Scholar 

  • Patten, C.L., Glick, B.R., 2002. The role of bacterial indoleacetic acid in the development of the host plant root system. Appl. Environ. Microbiol., 68(8):3795–3801. [doi:10.1128/AEM.68.8.3795-3801.2002]

    Article  PubMed  CAS  Google Scholar 

  • Penrose, D.M., Glick, B.R., 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(4):368–372. [doi:10.1139/cjm-47-4-368]

    Article  PubMed  CAS  Google Scholar 

  • Pierson, L.S., Thomashow, L.S., 1992. Cloning and heterologous expression of the phenazine biosynthetic locus from Pseudomonas aureofaciens. Mol. Plant-Microb. Interact., 5(4):330–339.

    CAS  Google Scholar 

  • Potgieter, H., Alexander, M., 1996. Susceptibility and resistance of several fungi to microbial lysis. J. Bacteriol., 91(4):1526–1532.

    Google Scholar 

  • Probanza, A., Lucas García, J.A., Ruiz Palomino, M., Ramos, B., Gutiérrez Mañero, F.J., 2002. Pinus pinea L. seedling growth and bacterial rhizosphere structure after inoculation with PGPR Bacillus (B. licheniformis CECT 5106 and B. pumilus CECT 5105). Appl. Soil. Ecol., 20(2):75–84.

    Google Scholar 

  • Ramos, B., Lucas García, J.A., Probanza, A., Barrientos, M.L., Gutiérrez Mañero, F.J., 2003. Alterations in the rhizobacterial community associated with European alder growth when inoculated with PGPR strain Bacillus licheniformis. Environ. Exp. Bot., 49(1):61–68. [doi:10.1016/S0098-8472(02)/00059-X]

    Article  Google Scholar 

  • Reid, C.P., Szaniszlo, P.J., Crowley, D.E., 1986. Siderophore Involvement in Plant Iron Nutrition. In: Swinburne, T.R. (Ed.), Iron Siderophores and Plant Diseases. Plenum Press, New York, p.29–42.

    Google Scholar 

  • Römheld, V., Marschner, H., 1986. Mobilization of iron in the rhizosphere of different plant species. Adv. Plant Nutr., 2:155–204.

    Google Scholar 

  • Sabry, S.A., Ghozlan, H.A., Abou-Zeid, D.M., 1997. Metal tolerance and antobiotic resistance patterns of a bacterial population isolated from sea water. J. Appl. Microbiol., 82(2):245–252.

    PubMed  CAS  Google Scholar 

  • Salt, D.E., Blaylock, M., Kumar, N.P.B.A., Dushenkov, V., Ensley, B.D., Chet, I., Raskin, I., 1995. Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biol. Technol., 13(5):468–474.

    CAS  Google Scholar 

  • Sandaa, R.A., Torsvik, V., Enger, O., Daae, L.F., Castberg, T., Hahn, D., 1999. Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. FEMS Microbiol. Ecol., 30(3):237–251. [doi:10.1111/j.1574-6941.1999.tb00652.x]

    Article  PubMed  CAS  Google Scholar 

  • Sanità di Toppi, L., Gabrielli, R., 1999. Response to cadmium in higher plants. Environ. Exp. Bot., 41(2):105–130. [doi: 10.1016/S0098-8472(98)00058-6]

    Article  Google Scholar 

  • Saxena, P.K., Krishnaraj, S., Dan, T., Perras, M.R., Vettaakkorumakankav, N.N., 1999. Phytoremediation of Heavy Metal Contaminated and Polluted Soils. In: Prasad, M.N.V., Hagemeyer, J. (Eds.), Heavy Metal Stress in Plants: from Molecules to Ecosystems. Springer, Berlin, p.305–329.

    Google Scholar 

  • Sharma, A., Johri, B.N., Sharma, A.K., Glick, B.R., 2003. Plant growth-promoting bacterium Pseudomonas sp. strain GRP3 influences iron acquisition in mung bean (Vigna radiata L. Wilzeck). Soil Biol. Biochem., 35(7):887–894. [doi:10.1016/S0038-0717(03)00119-6]

    Article  CAS  Google Scholar 

  • Sikora, R.A., 1992. Management of the antagonistic potential in agricultural ecosystems for the biological control of plant parasitic nematodes. Annu. Rev. Phytopathol., 30(1):245–270. [doi:10.1146/annurev.py.30.090192.001333]

    Article  Google Scholar 

  • Sikora, R.A., Hoffmann-Hergarten, S., 1992. Importance of plant health-promoting rhizobacteria for the control of soil-borne fungal diseases and plant parasitic nematodes. Arab. J. Plant Prot., 10(4):53–58.

    Google Scholar 

  • Sitaula, B.K., Almas, A., Bakken, L.R., Singh, B.R., 1999. Assessment of heavy metals associated with bacteria in soil. Soil Biol. Biochem., 31(2):315–316. [doi:10.1016/S0038-0717(98)00104-7]

    Article  CAS  Google Scholar 

  • Smalle, J., van der Straeten, J.D., 1997. Ethylene and vegetative development. Physiologia Plantarum, 100(3):593–605. [doi:10.1034/j.1399-3054.1997.1000322.x]

    Article  CAS  Google Scholar 

  • Smith, S.E., Read, D.J., 1997. Mycorrhizal Symbiosis. Academic Press Inc., San Diego.

    Google Scholar 

  • Steenhoudt, O., Vanderleyden, J., 2000. Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol. Rev., 24(4):487–506. [doi:10.1111/j.1574-6976.2000.tb00552.x]

    Article  PubMed  CAS  Google Scholar 

  • Tam, P.C.F., 1995. Heavy metal tolerance by ectomycorrhyzal fungi and metal amelioration by Pisolithus tinctorium. Mycorrhiza, 5(3):181–187. [doi:10.1007/s005720050057]

    Article  CAS  Google Scholar 

  • van Loon, L.C., 1984. Regulation of Pathogenesis and Symptom Expression in Diseased Plants by Ethylene. In: Fuchs, Y., Chalutz, E. (Eds.), Ethylene: Biochemical, Physiological and Applied Aspects. Martinus Nijhoff/Dr. W. Junk, the Hague, the Netherlands, p.171–180.

    Google Scholar 

  • Velazhahan, R., Samiyappan, R., Vidhyasekaran, P., 1999. Relationship between antagonistic activities of Pseudomonas fluorescens isolates against Rhizoctonia solani and their production of lytic enzyme. J. Plant Dis. Prot., 106(3):244–250.

    CAS  Google Scholar 

  • Vidhyasekaran, P., Muthamilan, M., 1999. Evaluation of powder formulation of Pseudomonas fluorescens Pf1 for control of rice sheath blight. Biocontrol Sci. Technol., 9(1):67–74. [doi:10.1080/09583159929910]

    Article  Google Scholar 

  • Viswanathan, R., Samiyappan, R., 1999. Induction of Systemic Resistance by Plant Growth Promoting Rhizobacteria against Red Rot Disease Caused by Collectotrichum falcatum Went in Sugarcane. In: Proceedings of the Sugar Technology Association of India, Vol. 61. Sugar Technology Association, New Delhi, India, p.24–39.

    Google Scholar 

  • Wallace, A., Wallace, G.A., Cha, J.W., 1992. Some modifications in trace elements toxicities and deficiencies in plants resulting from interactions with other elements and chelating agents. The special case of iron. J. Plant. Nutr., 15(2):1589–1598.

    Article  CAS  Google Scholar 

  • Wang, Y.T., Shen, H., 1995. Bacterial reduction of hexavalent chromium. J. Ind. Microbiol., 14(2):159–163. [doi:10.1007/BF01569898]

    Article  PubMed  CAS  Google Scholar 

  • Wang, Y., Brown, H.N., Crowley, D.E., Szaniszlo, P.J., 1993. Evidence for direct utilization of a siderophore, ferroxamine B, in axenically grown cucumber. Plant Cell Environ., 16(5):579–585. [doi:10.1111/j.1365-3040.1993.tb00906.x]

    Article  CAS  Google Scholar 

  • Weber, O., Scholz, R.W., Bvhlmann, R., Grasmuck, D., 2001. Risk perception of heavy metal soil contamination and attitudes toward decontamination strategies. Risk Anal., 21(5):967–977. [doi:10.1111/0272-4332.215165]

    Article  PubMed  CAS  Google Scholar 

  • Wei, L., Kloepper, J.W., Tuzun, S., 1991. Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth promoting rhizobacteria. Phytopathology, 81(11):1508–1512.

    Google Scholar 

  • Wei, L., Kloepper, J.W., Tuzun, S., 1996. Induced systemic resistance to cucumber diseases and increased plant growth by plant growth promoting rhizobacteria under field conditions. Phytopathology, 86(2):221–224. [doi:10.1094/Phyto-86-221]

    Article  Google Scholar 

  • Wenzel, W.W., Lombi, E., Adriano, D.C., 1999. Biochemical Processes in the Rhizosphere: Role in Phytoremediation of Metal-Polluted Soils. In: Prasad, M.N.V., Hagemeyer, J. (Eds.), Heavy Metal Stress in Plants: from Molecules to Ecosystems. Springer, Berlin, p.273–303.

    Google Scholar 

  • Whiting, S.N., de Souza, M.P., Terry, N., 2001. Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environ. Sci. Technol., 35(15):3144–3150. [doi:10.1021/es001938v]

    Article  PubMed  CAS  Google Scholar 

  • Xie, H., Pastemak, J.J., Glick, B.R., 1996. Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2 that overproduce indoleacetic acid. Curr. Microbiol., 32(2):67–71. [doi:10.1007/s002849900012]

    Article  CAS  Google Scholar 

  • Yang, X., Baligar, V.C., Martens, D.C., Clark, P.B., 1996. Plant tolerance to nickel toxicity. II. Nickel effect on influx and transport of mineral nutrients in four plant species. J. Plant Nutr., 19(2):265–279.

    CAS  Google Scholar 

  • Zayed, A.M., Lytle, C.M., Terry, N., 1998. Accumulation and volatilization of different chemical species of selenium by plants. Planta, 206(2):284–292. [doi:10.1007/s004250050402]

    Article  CAS  Google Scholar 

  • Zehnder, G., Kloepper, J., Yao, C., Wei, G., 1997. Induction of systemic resistance in cucumber against cucumber beetles (Coleoptera: Chrysomelidae) by plant growth promoting rhizobacteria. J. Econ. Entomol., 90(2):391–396.

    Google Scholar 

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Correspondence to He Zhen-li.

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Project supported by the National Natural Science Foundation of China (No. 20577044), the National Basic Research Program (973) of China (No. 2002CB410804), and the Program for Changjiang Scholars and Innovative Research Team in University (No. IRT0536), China

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Jing, Yd., He, Zl. & Yang, Xe. Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J. Zhejiang Univ. - Sci. B 8, 192–207 (2007). https://doi.org/10.1631/jzus.2007.B0192

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