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Assessment of arbuscular mycorrhizal fungi status and heavy metal accumulation characteristics of tree species in a lead–zinc mine area: potential applications for phytoremediation

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Abstract

To select suitable tree species associated with arbuscular mycorrhizal fungi (AMF) for phytoremediation of heavy metal (HM) contaminated area, we measured the AMF status and heavy metal accumulation in plant tissues in a lead–zinc mine area, Northwest China. All 15 tree species were colonized by AM fungi in our investigation. The mycorrhizal frequency (F%), mycorrhizal colonization intensity (M%) and spore density (SP) reduced concomitantly with increasing Pb and Zn levels; however, positive correlations were found between arbuscule density (A%) and soil total/DTPA-extractable Pb concentrations. The average concentrations of Pb, Zn, Cu and Cd in plant samples were 168.21, 96.61, 41.06, and 0.79 mg/kg, respectively. Populus purdomii Rehd. accumulated the highest concentrations of Zn (432.08 mg/kg) and Cu (140.85 mg/kg) in its leaves. Considerable amount of Pb (712.37 mg/kg) and Cd (3.86 mg/kg) were concentrated in the roots of Robinia pseudoacacia Linn. and Populus simonii Carr., respectively. Plants developed different strategies to survive in HM stress environment: translocating more essential metals (Zn and Cu) into the aerial parts, while retaining more toxic heavy metals (Pb and Cd) in the roots to protect the above-ground parts from damage. According to the translocation factor (TF), bioconcentration factor (BCF), growth rate and biomass production, five tree species (Ailanthus altissima (Mill.) Swingle, Cotinus coggygria Scop., P. simonii, P. purdomii, and R. pseudoacacia) were considered to be the most suitable candidates for phytoextraction and/or phytostabilization purposes. Redundancy analysis (RDA) showed that the efficiency of phytoremediation was enhanced by AM symbioses, and soil pH, Pb, Zn, and Cd levels were the main factors influencing the HM accumulation characteristics of plants.

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References

  • Aggarwal A, Kadian N, Tanwar A, Yadav A, Gupta KK (2011) Role of arbuscular mycorrhizal fungi (AMF) in global sustainable development. J Applied Nat Sci 3(2):340–351

    Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91(7):869–881

    Article  CAS  Google Scholar 

  • Allen SE (1989) Chemical analysis of ecological materials, 2nd edn. Blackwell scientific publications, Oxford

    Google Scholar 

  • Alloway BJ (2013) Heavy metals in soils. Springer, Netherlands. doi:10.1007/978-94-007-4470-7

    Book  Google Scholar 

  • Atangana A, Khasa D, Chang S, Degrande A (2014) Phytoremediation in tropical agroforestry. In tropical agroforestry. Springer, Netherlands, pp 343–351

    Book  Google Scholar 

  • Bonanno G, Lo Giudice R (2010) Heavy metal bioaccumulation by the organs of Phragmites australis (common reed) and their potential use as contamination indicators. Ecol Indic 10(3):639–645

    Article  CAS  Google Scholar 

  • Bothe H, Regvar M, Turnau K (2010) Arbuscular mycorrhiza, heavy metal and salt tolerance. In: Sherameti I, Varma A (eds) Soil heavy metals. Springer, Heidelberg, pp 87–111

    Chapter  Google Scholar 

  • Bremner JM, Mulvaney CS (1982) Nitrogen-total. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part II. Chemical and microbiological properties. American Society of Agronomy, Madison, pp 595–641

    Google Scholar 

  • Carvalho LM, Caçador I, Martins-Loução MA (2006) Arbuscular mycorrhizal fungi enhance root cadmium and copper accumulation in the roots of the salt marsh plant Aster tripolium L. Plant Soil 285(1–2):161–169

    Article  CAS  Google Scholar 

  • Castagna A, Di Baccio D, Ranieri AM, Sebastiani L, Tognetti R (2014) Effects of combined ozone and cadmium stresses on leaf traits in two poplar clones. Environ Sci Poll Res 1–12

  • Chaney RL (1989) Toxic element accumulation in soils and crops: protecting soil fertility and agricultural food-chains. In inorganic contaminants in the vadose zone. Springer, Berlin, pp 140–158

    Google Scholar 

  • Chang P, Kim JY, Kim KW (2005) Concentrations of arsenic and heavy metals in vegetation at two abandoned mine tailings in South Korea. Environ Geochem Health 27(2):109–119

    Article  CAS  Google Scholar 

  • Chen B, Li X, Tao H, Christie P, Wong M (2003) The role of arbuscular mycorrhiza in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc. Chemosphere 50(6):839–846

    Article  CAS  Google Scholar 

  • Chen X, Wu C, Tang J, Hu S (2005) Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment. Chemosphere 60(5):665–671

    Article  CAS  Google Scholar 

  • Christophi CA, Axe L (2000) Competition of Cd, Cu, and Pb adsorption on goethite. J Environ Eng 126(1):66–74

    Article  CAS  Google Scholar 

  • Curaqueo G, Schoebitz M, Borie F, Caravaca F, Roldán A (2014) Inoculation with arbuscular mycorrhizal fungi and addition of composted olive-mill waste enhance plant establishment and soil properties in the regeneration of a heavy metal-polluted environment. Environ Sci Pollut Res 21(12):7403–7412

    Article  CAS  Google Scholar 

  • Dai J, Becquer T, Rouiller JH, Reversat G, Bernhard-Reversat F, Lavelle P (2004) Influence of heavy metals on C and N mineralisation and microbial biomass in Zn-, Pb-, Cu-, and Cd-contaminated soils. Appl Soil Ecol 25(2):99–109

    Article  Google Scholar 

  • De Moor S, De Fraeye M, Michels E, Van Nevel L, Tack F, Meers E (2013) Short rotation coppice in 6th growth year for phytoremediation on metal contaminated soil. In Knowledge for Growth 2013: New business models creating companies for the future

  • Del Val C, Barea JM, Azcon-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65(2):718–723

    CAS  Google Scholar 

  • Durães N, Bobos I, da Silva EF, Dekayir A (2014) Copper, zinc and lead biogeochemistry in aquatic and land plants from the Iberian Pyrite Belt (Portugal) and north of Morocco mining areas. Environ Sci Poll Res 1–19

  • Entry JA, Rygiewicz PT, Watrud LS, Donnelly PK (2002) Influence of adverse soil conditions on the formation and function of Arbuscular mycorrhizas. Adv Environ Res 7(1):123–138

    Article  CAS  Google Scholar 

  • Farrell M, Griffith GW, Hobbs PJ, Perkins WT, Jones DL (2010) Microbial diversity and activity are increased by compost amendment of metal-contaminated soil. FEMS Microbiol Ecol 71(1):94–105

    Article  CAS  Google Scholar 

  • García-Salgado S, García-Casillas D, Quijano-Nieto MA, Bonilla-Simón MM (2012) Arsenic and heavy metal uptake and accumulation in native plant species from soils polluted by mining activities. Water Air Soil Pollut 223(2):559–572

    Article  Google Scholar 

  • Gatti E (2008) Micropropagation of Ailanthus altissima and in vitro heavy metal tolerance. Biol Plant 52(1):146–148

    Article  CAS  Google Scholar 

  • Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogyne species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244

    Article  Google Scholar 

  • Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223(6):1115–1122

    Article  Google Scholar 

  • Gregson S, Alloway BJ (1984) Gel permeation chromatography studies on the speciation of lead in solutions of heavily polluted soils. J Soil Sci 35(1):55–61

    Article  CAS  Google Scholar 

  • Guo G, Wu F, Xie F, Zhang R (2012) Spatial distribution and pollution assessment of heavy metals in urban soils from southwest China. J Environ Sci 24(3):410–418

    Article  CAS  Google Scholar 

  • Hou E, Xue X, Liu G, Ma Z, Zhao K (2003) The mine environmental geology and conservation strategy of Fengxian County. Northwest Geology 36:26–30, in Chinese

    Google Scholar 

  • Hu Y, Nan Z, Su J, Wang N (2013) Heavy metal accumulation by poplar in calcareous soil with various degrees of multi-metal contamination: implications for phytoextraction and phytostabilization. Environ Sci Pollut Res 20(10):7194–7203

    Article  CAS  Google Scholar 

  • Jackson ML, Barak P (2005) Soil chemical analysis: advanced course. Libraries Parallel Press, Madison

    Google Scholar 

  • Joner E, Leyval C (2001) Time-course of heavy metal uptake in maize and clover as affected by root density and different mycorrhizal inoculation regimes. Biol Fertil Soils 33(5):351–357

    Article  CAS  Google Scholar 

  • Jung MC (2008) Heavy metal concentrations in soils and factors affecting metal uptake by plants in the vicinity of a Korean Cu-W mine. Sensors 8(4):2413–2423

    Article  Google Scholar 

  • Kabata-Pendias A (2010) Trace elements in soils and plants, 3rd edn. CRC press, Boca Raton

    Book  Google Scholar 

  • Kahiluoto H, Ketoja E, Vestberg M, Saarela I (2001) Promotion of AM utilization through reduced P fertilization 2. Field studies. Plant Soil 231(1):65–79

    Article  CAS  Google Scholar 

  • Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92(4):486–488

    Article  Google Scholar 

  • Kulakow PA, Schwab AP, Banks MK (2000) Screening plant species for growth on weathered, petroleum hydrocarbon-contaminated sediments. Int J Phytoremediation 2(4):297–317

    Article  CAS  Google Scholar 

  • Ladislas S, El-Mufleh A, Gérente C, Chazarenc F, Andrès Y, Béchet B (2012) Potential of aquatic macrophytes as bioindicators of heavy metal pollution in urban stormwater runoff. Water Air Soil Pollut 223(2):877–888

    Article  CAS  Google Scholar 

  • Li M, Luo Y, Su Z (2007) Heavy metal concentrations in soils and plant accumulation in a restored manganese mineland in Guangxi, South China. Environ Pollut 147(1):168–175

    Article  CAS  Google Scholar 

  • Li T, Liu M, Zhang X, Zhang H, Sha T, Zhao Z (2011) Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila. Sci Total Environ 409(6):1069–1074

    Article  CAS  Google Scholar 

  • Liu L, Chen H, Cai P, Liang W, Huang Q (2009) Immobilization and phytotoxicity of Cd in contaminated soil amended with chicken manure compost. J Hazard Mater 163(2):563–567

    Article  CAS  Google Scholar 

  • Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2001) Phytoremediation of heavy metal-contaminated soils. J Environ Qual 30(6):1919–1926

    Article  CAS  Google Scholar 

  • Mahamadi C, Nharingo T (2010) Competitive adsorption of Pb2+, Cd2+ and Zn2+ ions onto Eichhornia crassipes in binary and ternary systems. Bioresour Technol 101(3):859–864

    Article  CAS  Google Scholar 

  • Małecka A, Derba-Maceluch M, Kaczorowska K, Piechalak A, Tomaszewska B (2009) Reactive oxygen species production and antioxidative defense system in pea root tissues treated with lead ions: mitochondrial and peroxisomal level. Acta Physiol Plant 31(5):1065–1075

    Article  Google Scholar 

  • Malik RN, Husain SZ, Nazir I (2010) Heavy metal contamination and accumulation in soil and wild plant species from industrial area of Islamabad. Pak J Bot 42(1):291–301

    CAS  Google Scholar 

  • Marques AP, Oliveira RS, Samardjieva KA, Pissarra J, Rangel AO, Castro PM (2007) Solanum nigrum grown in contaminated soil: effect of arbuscular mycorrhizal fungi on zinc accumulation and histolocalisation. Environ Pollut 145(3):691–699

    Article  CAS  Google Scholar 

  • Mårtensson AM, Carlgren K (1994) Impact of phosphorus fertilization on VAM diaspores in two Swedish long-term field experiment. Agric Ecosyst Environ 47(4):327–334

    Article  Google Scholar 

  • Meier S, Borie F, Bolan N, Cornejo P (2012) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42(7):741–775

    Article  CAS  Google Scholar 

  • Mendez MO, Glenn EP, Maier RM (2007) Phytostabilization potential of quailbush for mine tailings. J Environ Qual 36(1):245–253

    Article  CAS  Google Scholar 

  • Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12(4):563–569

    CAS  Google Scholar 

  • Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol Adv 29(6):645–653

    Article  CAS  Google Scholar 

  • Miretzky P, Fernandez-Cirelli A (2008) Phosphates for Pb immobilization in soils: a review. Environ Chem Lett 6(3):121–133

    Article  CAS  Google Scholar 

  • Morgan JB, Connolly EL (2013) Plant-soil interactions: nutrient uptake. Nat Educ Knowl 4(8):2

    Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. Methods of soil analysis. Part 2, Second Edition American Society of Agronomy, Inc, Wisconsin, pp 574–578

    Google Scholar 

  • Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyper-accumulation metals in plants. Water Air Soil Pollut 184(1–4):105–126

    Article  CAS  Google Scholar 

  • Påhlsson AMB (1989) Toxicity of heavy metals (Zn, Cu, Cd, Pb) to vascular plants. Water Air Soil Pollut 47(3–4):287–319

    Article  Google Scholar 

  • Peng K, Li X, Luo C, Shen Z (2006) Vegetation composition and heavy metal uptake by wild plants at three contaminated sites in Xiangxi area, China. J Environ Sci Health 41(1):65–76

    Article  CAS  Google Scholar 

  • Peuke AD, Rennenberg H (2005) Phytoremediation. EMBO Rep 6(6):497–501

    Article  CAS  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    Article  CAS  Google Scholar 

  • Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29(4):529–540

    Article  CAS  Google Scholar 

  • Qian K, Wang L, Yin N (2012) Effects of AMF on soil enzyme activity and carbon sequestration capacity in reclaimed mine soil. Int J Mining Sci Tech 22(4):553–557

    Article  CAS  Google Scholar 

  • Qin F, Wen B, Shan X, Xie Y, Liu T, Zhang S, Khan SU (2006) Mechanisms of competitive adsorption of Pb, Cu, and Cd on peat. Environ Pollut 144(2):669–680

    Article  CAS  Google Scholar 

  • Rees F, Simonnot MO, Morel JL (2014) Short‐term effects of biochar on soil heavy metal mobility are controlled by intra‐particle diffusion and soil pH increase. Eur J Soil Sci 65(1):149–161

    Article  CAS  Google Scholar 

  • Regvar M, Vogel-Mikuš K (2008) Recent advances in understanding of plant responses to excess metals: exposure, accumulation, and tolerance. Springer, Berlin, pp 227–251

    Google Scholar 

  • Ren W, Geng Y, Ma Z, Sun L, Xue B, Fujita T (2014) Reconsidering brownfield redevelopment strategy in China’s old industrial zone: a health risk assessment of heavy metal contamination. Environ Sci Poll Res 1–11

  • Robinson BH, Mills TM, Petit D, Fung LE, Green SR, Clothier BE (2000) Natural and induced cadmium-accumulation in poplar and willow: implications for phytoremediation. Plant Soil 227(1–2):301–306

    Article  CAS  Google Scholar 

  • Rodriguez E, da Conceição SM, Azevedo R, Correia C, Moutinho-Pereira J, de Oliveira JMPF, Dias MC (2015) Photosynthesis light-independent reactions are sensitive biomarkers to monitor lead phytotoxicity in a Pb-tolerant Pisum sativum cultivar. Environ Sci Pollut Res 22(1):574–585

    Article  CAS  Google Scholar 

  • Sauve S, McBride M, Hendershot W (1998) Soil solution speciation of lead (II): effects of organic matter and pH. Soil Sci Soc Am J 62(3):618–621

    Article  CAS  Google Scholar 

  • Seo KW, Son Y, Rhoades CC, Noh NJ, Koo JW, Kim JG (2008) Seedling growth and heavy metal accumulation of candidate woody species for revegetating Korean mine spoils. Restor Ecol 16(4):702–712

    Article  Google Scholar 

  • Serbula SM, Miljkovic DD, Kovacevic RM, Ilic AA (2012) Assessment of airborne heavy metal pollution using plant parts and topsoil. Ecotoxicol Environ Saf 76:209–214

    Article  CAS  Google Scholar 

  • Sheoran V, Sheoran AS, Poonia P (2010) Soil reclamation of abandoned mine land by revegetation: a review. Int J Soil, Sediment Water 3(2):13

    Google Scholar 

  • Shu W, Ye Z, Zhang Z, Lan C, Wong M (2005) Natural colonization of plants on five lead/zinc mine tailings in Southern China. Restor Ecol 13(1):49–60

    Article  Google Scholar 

  • Singh PK (2012) Role of glomalin related soil protein produced by arbuscular mycorrhizal fungi: a review. Agric Sci Res J 2(3):119–125

    Google Scholar 

  • Smith SE, Read DJ (1996) Mycorrhizal symbiosis. Academic press

  • Sudová R, Vosátka M (2007) Differences in the effects of three arbuscular mycorrhizal fungal strains on P and Pb accumulation by maize plants. Plant Soil 296(1–2):77–83

    Article  Google Scholar 

  • Trouvelot AK, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d'un système radiculaire. Recherche des méthodes d'estimation ayant une signification fonctionnelle. Mycorrhizae: Physiol Genetics, 217–221

  • Vangronsveld J, Van Assche F, Clijsters H (1995) Reclamation of a bare industrial area contaminated by non-ferrous metals: In situ metal immobilization and revegetation. Environ Pollut 87(1):51–59

    Article  CAS  Google Scholar 

  • Vivas A, Vörös I, Biró B, Campos E, Barea JM, Azcón R (2003) Symbiotic efficiency of autochthonous arbuscular mycorrhizal fungus (G. mosseae) and Brevibacillus sp. isolated from cadmium polluted soil under increasing cadmium levels. Environ Pollut 126(2):179–189

    Article  CAS  Google Scholar 

  • Wang AS, Angle JS, Chaney RL, Delorme TA, Reeves RD (2006) Soil pH effects on uptake of Cd and Zn by Thlaspi caerulescens. Plant Soil 281(1–2):325–337

    Article  CAS  Google Scholar 

  • Wang X, He M, Xie J, Xi J, Lu X (2010) Heavy metal pollution of the world largest antimony mine-affected agricultural soils in Hunan province (China). J Soils Sediments 10(5):827–837

    Article  CAS  Google Scholar 

  • Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321(1–2):385–408

    Article  CAS  Google Scholar 

  • Wójcik M, Sugier P, Siebielec G (2014) Metal accumulation strategies in plants spontaneously inhabiting Zn-Pb waste deposits. Sci Total Environ 487:313–322

    Article  Google Scholar 

  • Wu Q, Wang S, Thangavel P, Li Q, Zheng H, Bai J, Qiu R (2011) Phytostabilization potential of Jatropha curcas L. in polymetallic acid mine tailings. Int J Phytoremediation 13(8):788–804

    Article  Google Scholar 

  • Xu Z, Tang M, Chen H, Ban Y, Zhang H (2012) Microbial community structure in the rhizosphere of Sophora viciifolia grown at a lead and zinc mine of northwest China. Sci Total Environ 435:453–464

    Article  Google Scholar 

  • Xue L, Liu J, Shi S, Wei Y, Chang E, Gao M, Chen L, Jiang Z (2014) Uptake of heavy metals by native herbaceous plants in an antimony mine (Hunan, China). Clean-Soil, Air, Water 42(1):81–87

    Article  CAS  Google Scholar 

  • Yang J, Ye Z (2014) Antioxidant enzymes and proteins of wetland plants: their relation to Pb tolerance and accumulation. Environ Sci Poll Res 1–9

  • Yang S, Liang S, Yi L, Xu B, Cao J, Guo Y, Zhou Y (2014) Heavy metal accumulation and phytostabilization potential of dominant plant species growing on manganese mine tailings. Front Environ Sci Eng 8(3):394–404

    Article  CAS  Google Scholar 

  • Yao Y, Tian M, Wu S (2004) Mineral resources exploitation and sustainable development of Fengxian County in Shanxi province. Miner Resour Geol 18:470–475

    Google Scholar 

  • Yao Z, Li J, Xie H, Yu C (2012) Review on remediation technologies of soil contaminated by heavy metals. Procedia Environ Sci 16:722–729

    Article  CAS  Google Scholar 

  • Yoon J, Cao X, Zhou Q, Ma L (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368(2):456–464

    Article  CAS  Google Scholar 

  • Zarei M, Hempel S, Wubet T, Schäfer T, Savaghebi G, Jouzani GS, Nekouei MK, Buscot F (2010) Molecular diversity of arbuscular mycorrhizal fungi in relation to soil chemical properties and heavy metal contamination. Environ Pollut 158(8):2757–2765

    Article  CAS  Google Scholar 

  • Zeng F, Ali S, Zhang H, Ouyang Y, Qiu B, Wu F, Zhang G (2011) The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environ Pollut 159(1):84–91

    Article  CAS  Google Scholar 

  • Zhang C, Song N, Zeng G, Jiang M, Zhang J, Hu X, Chen A, Zhen J (2014) Bioaccumulation of zinc, lead, copper, and cadmium from contaminated sediments by native plant species and Acrida cinerea in South China. Environ Monit Assess 186(3):1735–1745

    Article  CAS  Google Scholar 

  • Zu Y, Li Y, Chen J, Chen H, Qin L, Christian S (2005) Hyperaccumulation of Pb, Zn and Cd in herbaceous grown on lead-zinc mining area in Yunnan, China. Environ Int 31(5):755–762

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was financially supported by the National Natural Science Foundation of China (31270639, 31170607, and 31170567), Program for Changjiang Scholars and Innovative Research Team in University of China (IRT1035). We thank Dr. Jingxia Li (College of Forestry, Northwest A&F University, Yangling, Shaanxi 712100, China) for tree species identification.

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Yang, Y., Liang, Y., Ghosh, A. et al. Assessment of arbuscular mycorrhizal fungi status and heavy metal accumulation characteristics of tree species in a lead–zinc mine area: potential applications for phytoremediation. Environ Sci Pollut Res 22, 13179–13193 (2015). https://doi.org/10.1007/s11356-015-4521-8

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