Skip to main content
SpringerLink
Log in

Effects of arbuscular mycorrhizal fungi on Agrostis capillaris grown on amended mine tailing substrate at pot, lysimeter, and field plot scales

  • Using microbes for the regulation of heavy metal mobility at ecosystem and landscape scale
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Applied research programs in the remediation of contaminated areas can be used also for gaining insights in the physiological and ecological mechanisms supporting the resistance of plant communities in stress conditions due to toxic elements. The research hypothesis of this study was that in the heavily contaminated but nutrient-poor substrate of mine tailing dams, the beneficial effect of inoculation with arbuscular mychorrizal fungi (AMF) is due to an improvement of phosphorus nutrition rather than to a reduction of toxic element transfer to plants. A concept model assuming a causal chain from root colonization to element uptake, oxidative stress variables, and overall plant development was used. The methodological novelty lies in coupling in a single research program experiments conducted at three scales: pot, lysimeter, and field plot, with different ages of plants at the sampling moment (six subsets of samples in all). The inoculation with AMF in expanded clay carrier had a beneficial effect on the development of plants in the amended tailing substrate heavily contaminated with toxic elements. The effect of inoculation was stronger when the quantity of expanded carrier was smaller (1 % vs. 7 % inoculum), probably because of changes in substrate features. The improvement of plant growth was due mainly to an improvement in phosphorus nutrition leading to an increase of protein concentration and decrease of oxidative stress enzyme activity (superoxide dismutase and peroxidase). In a single data subset, an effect of inoculation on the uptake of several toxic elements could be proved (decrease of As concentration in plant roots correlated with a decrease of oxidative stress independent from the effect of P concentration increase). The multi-scale approach allowed us to find differences between the patterns characterising the data subsets. These subset-specific patterns point out the existence of physiological differences between plants in different development states (as a result of sampling at different plant ages). From an applied perspective, conclusions are drawn with respect to the use of plants in the monitoring programs of contaminated areas and the use of inoculation with AMF in the remediation of tailing dams.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adriano DC (2001) Trace elements in terrestrial environments. Biogeochemistry, bioavailability, and risk of metals (2nd edn). Springer, New York

    Book  Google Scholar 

  • Benhammou A, Yaacoubi A, Nibou L, Tanoutu B (2005) Adsorption of metal ions onto Moroccan stevensite: kinetic and isotherm studies. J Colloid Interf Sci 282:320–326

    Google Scholar 

  • Bernal MP, Clemente R, Walker DJ (2007) The role of organic amendments in the bioremediation polluted soil. In: Environmental research at the leading edge, Alfred G (ed). Nova Science Publishers Inc. Chapter 1, pp 1–57

  • Bes C, Mench M (2008) Remediation of copper-contaminated topsoils from a wood treatment facility using in situ stabilisation. Environ Pollut 156:1128–1138

    Article  CAS  Google Scholar 

  • Bucher M (2006) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173(1):11–26

    Article  Google Scholar 

  • Cao X, Dermatas D, Xu X, Shen G (2008) Immobilization of lead in shooting range soils by means of cement, quicklime, and phosphate amendments. Env Sci Pollut Res 15(2):120–12

    Article  CAS  Google Scholar 

  • Cárcamo V, Bustamante E, Trangolao E, de la Fuente LM, Mench M, Neaman A, Ginocchio R (2012) Simultaneous immobilization of metals and arsenic in acidic polluted soils near a copper smelter in central Chile. Environ Sci Pollut Res 19:1131–1143. doi:10.1007/s11356-011-0673-3

    Article  Google Scholar 

  • Carrasco L, Gattinger A, Flieβbach A, Roldán A, Schloter M, Caravaca F (2009) Estimation by PLFA of microbial community structure associated with the rhizosphere of Lygeum spartum and Piptatherum miliaceum growing in semiarid mine tailings. Microb Ecol 60:265–271

    Article  Google Scholar 

  • Carrasco L, Barata C, Garçia-Berthou E, Tobias A, Bayona JM, Diez S (2011) Patterns of mercury and methylmercury bioaccumulation in fish species downstream of a long-term mercury-contaminated site in the lower Ebro River (NE Spain). Chemosphere 84:1642–1649

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chen BD, Zhu YG, Duan J, Xiao XY, Smith SE (2007) Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environ Pollut 147:374–380

    Article  CAS  Google Scholar 

  • Chen B, Roos P, Zhu YG, Jakobsen I (2008) Arbuscular mycorrhizas contribute to phytostabilization of uranium in uranium mining tailings. Environ Radioactiv J 99:801–810

    Article  CAS  Google Scholar 

  • Chen MM, Yin HB, O’Connor P, Wang YS, Zhu YG (2010) C: N: P stoichiometry and specific growth rate of clover colonized by arbuscular mycorrhizal fungi. Plant Soil 326:21–29

    Article  CAS  Google Scholar 

  • Chen Q, Hu C, Tan Q, Sun X (2011) Effect of different phosphate sources on availability of cadmium in soil. Huanjing Kexue Xuebao/Acta Sci Circumstantiae 31(10):2254–2259

    CAS  Google Scholar 

  • Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2012) Arbuscular mycorrhizal fungi modulate the leaf transcriptome of a Populus alba L. clone grown on a zinc and copper-contaminated soil. Environ Experim Botany 75:25–35

    Article  CAS  Google Scholar 

  • Claassen VP, Zasoski RJ (2006) Enhancement of revegetation on construction fill by fertilizer and topsoil application: effect on mycorrhizal infection. Land Degrad Dev 4(1):45–57

    Article  Google Scholar 

  • Damian F, Damian G (2007) Detoxification of heavy metal contaminated soils. Am J Environ Sci 3:193–198

    Article  CAS  Google Scholar 

  • Dazy M, Béraud E, Cotelle S, Grévilliot F, Férard JF, Masfaraud JF (2009) Changes in plant communities along soil pollution gradients: responses of leaf antioxidant enzyme activities and phytochelatin contents. Chemosphere 77:376–383

    Article  CAS  Google Scholar 

  • de Souza LA, Lopez de Andrade SA, Ribeiro de Souza SC, Schiavinato MA (2012) Arbuscular mycorrhiza confers Pb tolerance in Calopogonium mucunoides. Acta Physiologiae Plantarum 34(2):523–531

    Article  Google Scholar 

  • de Souza LA, Lopez de Andrade SA, Ribeiro de Souza SC, Schiavinato MA (2013) Evaluation of mycorrhizal influence on the development and phytoremediation potential of Canavalia gladiata in Pb-contaminated soils. Int J Phytoremediat 15:465–476

    Article  CAS  Google Scholar 

  • DIN ISO 11260 1997–05 (1997) Soil quality—determination of effective cation exchange capacity and base saturation level using barium chloride solution. Deutsches Institut für Normung, Beuth Verlag GmbH, Berlin, D (in German)

  • Doula MK, Elaiopoulos K, Kavvadias VA, Mavraganis V (2012) Use of clinoptilolite to improve and protect soil quality from disposal of oil mills wastes. J Hazard Mater 207–208:103–110

    Article  Google Scholar 

  • Eapen S, Singh S, D’Souza SF (2007) Phytoremediation of metals and radionuclides, Chapter 8. In: Environmental bioremediation technologies. Springer, Heidelberg, pp 189–209

    Book  Google Scholar 

  • Farrag K, Senesi N, Nigro F, Petrozza A, Palma A, Shaarawi S, Brunetti G (2012) Growth responses of crop and weed species to heavy metals in pot and field experiments. Environ Sci Pollut Res 19:3636–3644

    Article  CAS  Google Scholar 

  • Fenglian F, Wan Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manage 92(3):407–418

    Article  Google Scholar 

  • Fenn ME, Perea-Estrada VM, De Bauer LI, Perez-Suarez M, Parker DR, Centina-Alcala VM (2006) Nutrient status and plant growth effects of forest soils in the basin of Mexico. Environ Pollut 140:187–199

    Article  CAS  Google Scholar 

  • Garau G, Castaldi P, Santona L, Deiana P, Melis P (2007) Influence of red mud, zeolite and lime on heavy metal immobilization, culturable heterotrophic microbial populations and enzyme activities in a contaminated soil. Geoderma 142:47–57

    Article  CAS  Google Scholar 

  • Garg N, Kaur H (2012) Influence of zinc on cadmium-induced toxicity in nodules of pigeonpea (Cajanus cajan L. Mill sp.) inoculated with arbuscular mycorrhizal (AM) fungi. Acta Physiol Plant 34:1363–1380

    Article  CAS  Google Scholar 

  • Ginocchio R, Baker AJM (2004) Metallophytes in Latin America: a remarkable biological and genetic resource scarcely known and studied in the region. Rev Chil Hist Nat 77:185–194

    Article  Google Scholar 

  • Gómez-Sagasti MT, Alkorta I, Becerril JM, Epelde L, Anza M, Garbisu C (2012) Microbial monitoring of the recovery of soil quality during heavy metal phytoremediation. Water Air Soil Pollut. doi:10.1007/s11270-012-1106-8

    Google Scholar 

  • González-Guerrero M, Oger E, Benabdellah K, Azcón-Aguilar C, Lanfranco L, Ferrol N (2010) Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices. Curr Genet 56:265–274

    Article  Google Scholar 

  • Hanauer T, Henningsen PF, Steffens D, Kalandadze B, Navrozashvili L, Urushadze T (2011) In situ stabilization of metals (Cu, Cd, and Zn) in contaminated soils in the region of Bolnisi, Georgia. Plant Soil 341:193–208

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146

    Article  CAS  Google Scholar 

  • Hoffmann G (1991) Methodenbuch, Band 1. In: Die Untersuchung von Böden (ed). VDLUFA-Verlag, Darmstadt

  • Hong CO, Lee DK, Kim PJ (2008) Feasibility of phosphate fertilizer to immobilize cadmium in a field. Chemosphere 70(11):2009–2015

    Article  CAS  Google Scholar 

  • Iordache V, Ion S, Pohoaţă A (2009a) Integrated modeling of metals biogeochemistry: potential and limits. Chem Erde-Geochem 69:125–169

    Article  CAS  Google Scholar 

  • Iordache V, Gherghel F, Kothe E (2009b) Assessing the effect of disturbances on ectomycorrhiza diversity, review. Int J Environ Res Public Health 6:414–432

    Article  Google Scholar 

  • IordacheV, Onete M, Paucă M, Oromulu L, Honciuc V, Purice D, Cobzaru I, Gomoiu I, Neagoe A (2010) Biological communities in mining areas: scale dependent patterns, organisms’ potential as bioindicators, and naive plants for remediation, Proceedings 7th European Conference on Ecological Restoration Avignon, France, 23-27/08/2010, http://ser.semico.be/ser-pdf/EA_SER2010_313.pdf

  • Iordache V, Lăcătusu R, Scrădeanu D, Onete M, Jianu D, Bodescu F, Neagoe A, Purice D, Cobzaru I (2012) Scale specific mechanisms of metals mobility in contaminated areas. In: Kothe E, Varma A (eds) Bio-geo-interactions in contaminated soils. Springer, Heidelberg, pp 385–416

    Chapter  Google Scholar 

  • Iverson SL, Maier RM (2009) Effects of compost on colonization of roots of plants grown in metalliferous mine tailings, as examined by fluorescence in situ hybridization. Appl Environ Microb 75:842–847

    Article  CAS  Google Scholar 

  • Javot H, Pumplin N, Harrison J (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322

    Article  CAS  Google Scholar 

  • Jianu D, Iordache V, Soare B, Petrescu L, Neagoe A, Iacob CR, Orza R (2012) The role of mineralogy and geochemistry in hazard potential assessment of mining areas. In: Kothe E, Varma A (eds) Bio-geo interactions in metal-contaminated soils. Springer, Heidelberg, pp 35–79

    Chapter  Google Scholar 

  • Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Khalvati M, Bartha B, Dupigny A, Schröder P (2010) Arbuscular mycorrhizal association is beneficial for growth and detoxification of xenobiotics of barley under drought stress. J Soils Sediments 10:54–64

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kumpiene J, Lagerkvist A, Maurice C (2008) Stabilization of As, Cr, Cu, Pb and Zn in soils using amendments. A review. Waste Manag 28:215–225

    Article  CAS  Google Scholar 

  • Lagrimini LM (1991) Wound induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol 96:577–583

    Article  CAS  Google Scholar 

  • Lasat MM (2000) Phytoextraction of metals from contaminated soil: a review of plant/soil/metal interaction and assessment of pertinent agronomic issues. J Hazard Subst Res 2:1–25

    Google Scholar 

  • Lefévre I, Marchal G, Corréal E, Zanuzzi A, Lutts S (2009) Variation in response to heavy metals during vegetative growth in Dorycnium pentaphyllum Scop. Plant Growth Regul 59:1–11

    Article  Google Scholar 

  • Liu LZ, Gong ZQ, Zhang YL, Li PJ (2011) Growth, cadmium accumulation and physiology of marigold (Tageteserecta L.) as affected by arbuscular mycorrhizal fungi. Pedosphere 21(3):319–327

    Article  CAS  Google Scholar 

  • Lopareva-Pohu A, Verdin A, Garçon G, Lounes-Hadj Sahraoui A, Pourrut B, Debiane D, Waterlot C, Laruelle F, Bidar G, Douay F, Shirali P (2011) Influence of fly ash aided phytostabilization of Pb, Cd and Zn highly contaminated soils on Lolium perenne and Trifolium repens metal transfer and physiological stress. Environ Pollut 159:1721–1729

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Luster J, Menon M, Hermle S, Schulin R, Günthard-Goerg MS, Nowack B (2008) Initial changes in refilled lysimeters built with metal polluted topsoil and acidic or calcareous subsoils as indicated by changes in drainage water composition. Water Air Soil Pollut Focus 8:163–176

    Article  CAS  Google Scholar 

  • Madejón E, Doronila AI, Madejón P, Baker AJM, Woodrow IE (2012) Biosolids, mycorrhizal fungi and eucalypts for phytostabilization of arsenical sulphidic mine tailings. Agroforest Syst 84:389–399

    Article  Google Scholar 

  • Madrid F, Diaz-Barrientos E, Florido MC (2008) Inorganic amendments to decrease metal availability in soil of recreational urban areas: limitations to their efficiency and possible drawbacks. Water Air Soil Pollut 192:117–125

    Article  CAS  Google Scholar 

  • Malizia D, Giuliano A, Ortaggi G, Masotti A (2012) Common plants as alternative analytical tools to monitor heavy metals in soil. Chem Cent J 6(Suppl 2):S6. doi:10.1186/1752-153X-6-S2-S6

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London

    Google Scholar 

  • Mascher R, Fischer S, Scheiding W, Neagoe A, Bergmann H (2005) Exogenous 2-aminoethanol can diminish paraquat induced oxidative stress in barley (Hordeum vulgare L.). Plant Growth Regul 45:103–112

    Article  CAS  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymatic function for erythrocuprein. J Biol Chem 244:6049–6055

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mench M, Vangroensveld J, Lepp NM, Edwards R (1998) Physico-chemical aspects and efficiency of trace element immobilization by soil amendments. In: Vangroensveld J, Cummingham SD (eds) Metal-contaminated soils. Springer, Berlin, pp 151–182

    Google Scholar 

  • Mench M, Lepp N, Bert V, Schwitzguebel JP, Gawronski SW, Schröder P, Vangronsveld J (2010) Successes and limitations of phytotechnologies at field scale: outcomes, assessment and outlook from COST Action 859. J Soils Sediments 10:1039–1070

    Article  CAS  Google Scholar 

  • Mendez MO, Maier RM (2008) Phytoremediation of mine tailings in temperate and arid environments. Rev Environ Sci Biotechnol 7:47–59

    Article  CAS  Google Scholar 

  • Moirou A, Xenidi A, Paspaliaris A (2001) Stabilization of Pb, Zn, and Cd-contaminated soils by means of natural zeolite. Soil Sediment Contam 10:251–267

    Article  CAS  Google Scholar 

  • Mozgawa W, Bajda T (2005) Spectroscopic study of heavy metals sorption on clinoptilolite. Phys Chem Minerals 31:709–713

    Article  Google Scholar 

  • Neagoe A, Ebenå G, Carlsson E (2005) The effects of soil amendments on plant performance in an area affected by acid mine drainage. Chem Erde-Geochem 65(S1):115–130

    Article  CAS  Google Scholar 

  • Neagoe A, Merten D, Iordache V, Buechel G (2009) The effect of bioremediation methods involving different degrees of soil disturbance on the export of metals by leaching and by plant uptake. Chem Erde-Geochem 69:57–73

    Article  CAS  Google Scholar 

  • Neagoe A, Iordache V, Fărcăşanu I (2011) Remediation of polluted areas. Bucharest University Press, Bucharest, p 95 (in Romanian)

    Google Scholar 

  • Neagoe A, Iordache V, Bergmann H, Kothe E (2013) Patterns of effects of arbuscular mycorrhizal fungi on plants grown in contaminated soil. J Plant Nutr Soil Sci. doi:10.1002/jpln.201200079

    Google Scholar 

  • Pansou M, Gautheyrou F (2006) Handbook of soil analysis: Mineralogical, organic and inorganic methods. Springer, Berlin

    Book  Google Scholar 

  • Petkovšek SAS (2013) Forest biomonitoring of the largest Slovene thermal power plant with respect to reduction of air pollution. Environ Monit Assess 185:1809–1823

    Article  Google Scholar 

  • Powell J, Klironomos J (2007) The ecology of plant-mutualisms. In: Eldor AP (ed) Soil microbiology, ecology, and biochemistry (third edn.). Elsevier, Amsterdam, pp 257–281

    Chapter  Google Scholar 

  • Prasad MNV, Freitas H (2003) Metal hyperaccumulation in plants - biodiversity prospecting for phytoremediation technology. Electronic J Biotechnol 6:275–321

    Article  Google Scholar 

  • Rydlova J, Vosatka M (2003) Effect of Glomus intraradices isolated from Pb-contaminated soil on Pb uptake by Agrostis capillaris is changed by its cultivation in a metal-free substrate. Folia Geobot 38:155–165

    Article  Google Scholar 

  • Salt DE, Blaylock M, Kumar NPBA, Dusenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnol 13:468–474

    Article  CAS  Google Scholar 

  • Sand W, Jozsa PG, Kovacs ZM, Săsăran N, Schippers A (2007) Long-term evaluation of acid rock drainage mitigation measures in large lysimeters. J Geochem Explor 92:205–211

    Article  CAS  Google Scholar 

  • Schöpfer P (1989) Experimentelle Pflanzenphysiologie-Einführung in die Anwendung, vol 2. Springer, Berlin

    Book  Google Scholar 

  • Schmitz O, Danneberg G, Hundeshagen B, Klinger A, Bothe H (1991) Quantification of vesicular-arbuscular mycorrhiza by biochemical parameters. J Plant Physiol 139:106–114

    Article  CAS  Google Scholar 

  • Soares CRFS, Siqueira JO (2008) Mycorrhiza and phosphate protection of tropical grass species against heavy metal toxicity in multi-contaminated soil. Biol Fertil Soils 44:833–841

    Article  CAS  Google Scholar 

  • Stancu P, Nicoară A, Neagoe A, Grawunder W, Iordache V (2011) The effect of amendments on geochemical characterisation of tailing substrate in a field experiment. Proceedings of the 11th international symposium on “Metal elements in environment, medicine and biology”, Cluj-Napoca, Romania

    Google Scholar 

  • Tordoff GM, Baker AJM, Willis AJ (2000) Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41:219–228

    Article  CAS  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Press, Paris, pp 217–221

    Google Scholar 

  • Turnau K, Orlowska E, Ryszka P, Zubek S, Anielska T, Gawronski S, Jurkiewicz A (2006) Role of mycorrhizal fungi in phytoremediation and toxicity monitoring of heavy metal rich industrial wastes in southern Poland. In: Twardowska I, Allen HE, Häggblom MH, Stefaniak S (eds) Soil and water pollution monitoring, protection and remediation. Springer, Berlin, pp 3–23

    Google Scholar 

  • Turnau K, Anielska T, Ryszka P, Gawroński S, Ostachowicz B, Jurkiewicz A (2008) Establishment of arbuscular mycorrhizal plants originating from xerothermic grasslands on heavy metal rich industrial wastes—new solution for waste revegetation. Plant Soil 305:267–280

    Article  CAS  Google Scholar 

  • Turnau K, Ryszka P, Wojtczak G (2010) Metal tolerant mycorrhizal plants: A review from the perspective on industrial waste in temperate region. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizal: Physiology and function. Springer, Dordrecht, pp 257–276

    Chapter  Google Scholar 

  • USEPA (2007) The use of soil amendments for remediation, revitalization, and reuse. EPA 542-R-07-013. Office of Superfund Remediation and Technology Innovation (OSRTI). EPA/ National Service Center for Environmental Publications, Cincinnati

  • Vangronsveld J, Herzig R, Weynes N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794

    Article  CAS  Google Scholar 

  • Von Alten H, Blal B, Dodd JC, Feldmann F, Vosatka M (2002) Quality control of arbuscular mycorrhizal fungi inoculum in Europe. In: Gianinazzi H, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture. Birkhäuser Verlag, Switzerland, pp 281–296

    Chapter  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Willscher S, Mirgorodsky D, Jablonski L, Ollivier D, Merten D, Büchel G, Wittig J, Werner P (2013) Field scale phytoremediation experiments on a heavy metal and uranium contaminated site, and further utilization of the plant residues. Hydrometallurgy 131–132:46–53

    Article  Google Scholar 

  • Wirtz S, Seeger M, Ries JB (2012) Field experiments for understanding and quantification of rill erosion processes. Catena 91:21–34

    Article  Google Scholar 

  • Wong MH (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50:775–780

    Article  CAS  Google Scholar 

  • Wu SC, Wong CC, Shu WS, Khan AG, Wong MH (2011) Mycorrhizo-remediation of lead/zinc mine tailings using vetiver: a field study. Int J Phytoremed 13:61–74

    Article  CAS  Google Scholar 

  • Xu W, Ly L, Grace JR (2010) Zinc removal from acid rock drainage by clinoptilolite in a slurry bubble column. Appl Clay Sci 50(1):158–163

    Article  CAS  Google Scholar 

  • Zaller JG, Saccani F, Frank T (2011) Effects of earthworms and mycorrhizal fungi on the growth of the medicinal herb Calendula officinalis (Asteraceae). Plant Soil Environ 57(11):499–504

    Google Scholar 

  • Zeien H, Brümmer GW (1989) Chemische Extraktionen zur Bestimmung von Schwermetall-bildungformen in Böden. Mitt Dtsch Bodenk Gesell 59:505–510

    Google Scholar 

  • Zhang HH, Tang M, Chen H, Zheng CL, Niu ZC (2010) Effect of inoculation with AM fungi on lead uptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasing lead concentrations. Eur J Soil Biol 46(5):306–311

    Article  Google Scholar 

Download references

Acknowledgments

This work was performed within the FP7 project UMBRELLA, grant agreement 226870/2009, and Partnership PN2 projects: 31-012/2007 FITORISC and 50/2012 ASPABIR funded by Executive Agency for Higher Education, Research, Development and Innovation Funding, Romania. The authors acknowledge Roxana Donciu, who was a technician in our lab. They also thank Prof. Dr. Katarzyna Turnau for the analysis of the mine tailing substrate with respect to mycorrhizal fungi content. They specially thank the anonymous reviewers for the constructive criticism that greatly improved the manuscript.

Author information

Authors and Affiliations

  1. Research Centre for Ecological Services (CESEC), Faculty of Biology, University of Bucharest, Spl. Independentei 91-95, Bucharest, Romania

    Aurora Neagoe, Paula Stancu, Andrei Nicoară, Florian Bodescu, Roxana Gheorghe & Virgil Iordache

  2. Bucharest Institute of Biology, Romanian Academy, Spl. Independentei 296, Bucharest, Romania

    Marilena Onete

Authors
  1. Aurora Neagoe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paula Stancu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrei Nicoară
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marilena Onete
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Florian Bodescu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Roxana Gheorghe
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Virgil Iordache
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aurora Neagoe.

Additional information

Responsible editor: Philippe Garrigues

Aurora Neagoe and Virgil Iordache had an equal contribution to the production of this article.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 1676 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Neagoe, A., Stancu, P., Nicoară, A. et al. Effects of arbuscular mycorrhizal fungi on Agrostis capillaris grown on amended mine tailing substrate at pot, lysimeter, and field plot scales. Environ Sci Pollut Res 21, 6859–6876 (2014). https://doi.org/10.1007/s11356-013-1908-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-1908-2

Keywords

Search

Navigation