Skip to main content

Advertisement

SpringerLink
Log in

Arsenic Root Sequestration by a Tropical Woody Legume as Affected by Arbuscular Mycorrhizal Fungi and Organic Matter: Implications for Land Reclamation

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

The potential use of the arsenic-tolerant woody leguminous species Anadenanthera peregrina (L) Spegazzini for rehabilitating arsenic (As)-contaminated areas was studied. In an As (539.33 mg/kg)-contaminated soil experiment, plants were able to accumulate arsenic in their roots with a low transfer index to the shoot. Inoculation with arbuscular mycorrhizal fungi (AMF) amplified this behavior and improved both biomass production and the phosphorus concentration in the shoot. AMF inoculation not only improved A. peregrina plant growth but also protected the shoot against As toxicity. Aside from the AMF inoculation, the addition of organic matter reduced the soil pH, thus improving the ability of the roots to accumulate arsenic. The majority (81 %) of the variations in As accumulation in A. peregrina roots were explained by the effects of the organic matter and soil pH as well as AMF treatments, as found by a principal component analysis. A. peregrina promoted phytostabilization through As root sequestration. Therefore, A. peregrina plants inoculated with AMF in the presence of organic matter are recommended to rehabilitate degraded areas of soil contaminated with arsenic.

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

Similar content being viewed by others

References

  • Ahmed, F. R. S., Alexander, I. J., Mwinyihija, M., & Killham, K. (2011). Effect of superphosphate and arbuscular mycorrhizal fungus Glomus mosseae on phosphorus and arsenic uptake in lentil (Lens culinaris L.). Water, Air, and Soil Pollution, 221, 169–182. doi:10.1007/s11270-011-078.

    Article  CAS  Google Scholar 

  • Ali, H., Khan, E., & Sajad, M. A. (2013). Phytoremediation of heavy metals—concepts and applications. Chemosphere, 91, 869–881. doi:10.1016/j.chemosphere.2013.01.075.

    Article  CAS  Google Scholar 

  • Bissen, M., & Frimmel, F. H. (2003). Arsenic—a review. Part I: Occurrence, toxicity, speciation, mobility. Acta Hydrochimica et Hydrobiologica, 31, 9–18. doi:10.1002/aheh.200390025.

    Article  CAS  Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry, 72, 248–254. doi:10.1016/0003-2697(76)90527-3.

    Article  CAS  Google Scholar 

  • Chen, B. D., Xiao, X. Y., Zhu, Y. G., Smith, F. A., Xie, Z. M., & Smith, S. E. (2007). The arbuscular mycorrhizal fungus Glomus mosseae gives contradictory effects on phosphorus and arsenic acquisition by Medicago sativa Linn. Science of the Total Environment, 147, 374–379. doi:10.1016/j.scitotenv.2006.07.038.

    CAS  Google Scholar 

  • Chopra, B. K., Bhat, S., Mikheenko, I. P., Xu, Z., Yang, Y., Luo, X., et al. (2007). The characteristics of rhizosphere microbes associated with plants in arsenic contaminated soils from cattle dip sites. Science of the Total Environment, 378, 331342. doi:10.1016/j.scitotenv.2007.02.036.

    Article  CAS  Google Scholar 

  • Christophersen, H. M., Smith, F. A., & Smith, S. E. (2012). Unraveling the influence of arbuscular mycorrhizal colonization on arsenic tolerance in Medicago: Glomus mosseae is more effective than G. intraradices, associated with lower expression of root epidermal Pi transporter genes. Frontiers in Physiology, 3, 1–13. doi:10.3389/fphys.2012.00091.

    Article  CAS  Google Scholar 

  • Cunningham, S. D., Berti, W. R., & Huang, J. W. (1995). Phytoremediation of contaminated soils. Trends in Biotechnology, 13, 393–397. doi:10.1016/S0167-799(00)88987-8.

    Article  CAS  Google Scholar 

  • David, T. S., Pinto, C. A., Nadezhdina, N., Kurz-Besson, C., Henriques, M. O., Quilhó, T., et al. (2013). Root functioning, tree water use and hydraulic redistribution in Quercus suber trees: A modeling approach based on root sap flow. Forest Ecology and Management, 307, 136–146.

    Article  Google Scholar 

  • Dickinson, N. M., Turner, A. P., Watmough, S. A., & Lepp, N. W. (1992). Acclimation of trees to pollution stress: Cellular metal tolerance traits. Annals of Botany, 70, 569–572.

    CAS  Google Scholar 

  • Dong, Y., Zhu, Y., Smith, A. F., Wang, Y., & Chen, B. (2008). Arbuscular mycorrhiza enhanced arsenic resistance of both white clover (Trifolium repens Linn.) and ryegrass (Lolium perenne L.) plants in an arsenic-contaminated soil. Environmental Pollution, 155, 174–181. doi:10.1016/j.envpol.2007.10.023.

    Article  CAS  Google Scholar 

  • EMBRAPA. (1997). Centro Nacional de Pesquisa de Solos (Rio de Janeiro, RJ). Sistema brasileiro de classificação de solos. Brasilia: CNPS.

    Google Scholar 

  • Fendorf, S., & Kocar, B. D. (2009). Biogeochemical processes controlling the fate and transport of arsenic: Implications for South and Southeast Asia. Advances in Agronomy, 104, 137–164. doi:10.1016/S0065-2113(09)04003-6.

    Article  CAS  Google Scholar 

  • Fließbach, A., Oberholzer, H., Ma, L., & der Gunst, P. (2007). Soil organic matter and biological soil quality indicators after 21 years of organic and conventional farming. Agriculture, Ecosystems & Environment, 118, 273–284. doi:10.1016/j.agee.2006.05.022.

    Article  Google Scholar 

  • Francesconi, K., Visoottiviseth, P., Sridokchan, W., & Goessler, W. (2002). Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: A potential phytoremediator of arsenic-contaminated soils. The Science of the Total Environment, 284, 27–35. doi:10.1016/S0048-9697(01)00854-3.

    Article  CAS  Google Scholar 

  • García-Salgado, S., García-Casillas, D., Quijano-Nieto, M. A., & Bonilla-Simón, M. M. (2012). Arsenic and heavy metal uptake and accumulation in native plant species from soils polluted by mining activities. Water, Air, and Soil Pollution, 223, 559–572. doi:10.1007/s11270-011-0882-x.

    Article  CAS  Google Scholar 

  • García-Sánchez, A., Alonso-Rojo, P., & Santos-Francés, F. (2010). Distribution and mobility of arsenic in soils of a mining area (Western Spain). The Science of the Total Environment, 408, 4194–4201. doi:10.1016/j.scitotenv.2010.05.032.

    Article  CAS  Google Scholar 

  • Garg, N., & Singla, P. (2012). The role of Glomus mosseae on key physiological and biochemical parameters of pea plants grown in arsenic contaminated soil. Scientia Horticulturae, 143, 92–101. doi:10.1016/j.scienta.2012.06.010.

    Article  CAS  Google Scholar 

  • Gerdemann, J., & Nicholson, T. (1963). Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society, 46, 235–244. doi:10.1016/S0007-1536(63)80079-0.

    Article  Google Scholar 

  • Gonzaga, M. I. S., Santos, J. A. G., & Ma, L. Q. (2008). Phytoextraction by arsenic hyperaccumulator Pteris vittata L. from six arsenic-contaminated soils: Repeated harvests and arsenic redistribution. Environmental Pollution, 154, 212–218. doi:10.1016/j.envpol.2007.10.011.

    Article  CAS  Google Scholar 

  • Gonzalez-Chavez, M. C., Carrillo-Gonzalez, R., Wright, S. F., & Nichols, K. A. (2004). The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environmental Pollution, 130, 317–323. doi:10.1016/j.envpol.2004.01.004.

    Article  CAS  Google Scholar 

  • González-Guerrero, M., Melville, L. H., Ferrol, N., Lott, J. N., Azcón-Aguilar, C., & Peterson, R. L. (2008). Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Canadian Journal of Microbiology, 54, 103–110. doi:10.1139/W07-119.

    Article  CAS  Google Scholar 

  • Gunes, A., Pilbeam, D., & Inal, A. (2009). Effect of arsenic–phosphorus interaction on arsenic-induced oxidative stressin chickpea plants. Plant & Soil, 314, 211–220. doi:10.1007/s11104-008-9719-9.

    Article  CAS  Google Scholar 

  • Hartley, W., Dickinson, N. M., Riby, P., Leese, E., Morton, J., & Lepp, N. W. (2010). Arsenic mobility and speciation in a contaminated urban soil are affected by different methods of green waste compost application. Environmental Pollution, 158, 3560–3570. doi:10.1016/j.envpol.2010.08.015.

    Article  CAS  Google Scholar 

  • Jackson, R. B., Sperry, J. S., & Dawson, T. E. (2000). Root water uptake and transport: using physiological processes in global predictions. Trends in Plant Science Perspectives, 5, 482–488.

    Article  CAS  Google Scholar 

  • Jankong, P., & Visoottiviseth, P. (2008). Effects of arbuscular mycorrhizal inoculation on plants growing on arsenic contaminated soil. Chemosphere, 72, 1092–1097. doi:10.1016/j.chemosphere.2008.03.040.

    Article  CAS  Google Scholar 

  • Kahle, H. (1993). Response of roots of trees to heavy metals. Environmental and Experimental Botany, 33, 99–119. doi:10.1016/0098-8472(93)90059-O.

    Article  Google Scholar 

  • King, E. G., & Hobbs, R. J. (2006). Identifying linkages among conceptual models of ecosystem degradation and restoration: Towards an integrative framework. Restoration Ecology, 14, 369–378. doi:10.1111/j.1526-100X.2006.00145.x.

    Article  Google Scholar 

  • Kumpiene, J., Lagerkvist, A., & Maurice, C. (2008). Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments: A review. Waste Management, 28, 215–222. doi:10.1016/j.wasman.2006.12.012.

    Article  CAS  Google Scholar 

  • Larner, B. L., Seen, A. J., & Townsend, A. T. (2006). Comparative study of optimized BCR sequential extraction scheme and acid leaching of elements in the certified reference material NIST 2711. Analytica Chimica Acta, 556, 444–449. doi:10.1016/j.aca.2005.09.058.

    Article  CAS  Google Scholar 

  • Lee, D. A., Chen, A., & Schroeder, J. I. (2003). ars1, an Arabidopsis mutant exhibiting increased tolerance to arsenate and increased phosphate uptake. Plant Journal, 35, 637–646. doi:10.1046/j-1365-313x200301835x.

    Article  CAS  Google Scholar 

  • Liu, Y. Y., Zhu, G., Chen, B. D., Christie, P., & Li, X. L. (2005). Influence of the arbuscular mycorrhizal fungus Glomus mosseae on uptake of arsenate by the As hyperaccumulator fern Pteris vittata L. Mycorrhiza, 15, 187–192. doi:10.1007/s00572-004-0320-7.

    Article  CAS  Google Scholar 

  • Lorenzi, H. (1992). Árvores brasileiras: Manual de identificação e cultivo de plantas nativas do Brasil. Nova Odessa: Plantarum.

    Google Scholar 

  • Ma, J. F., Yamaji, N., Mitani, N., Xu, X., Su, Y., McGrath, S. P., et al. (2008). Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proceedings of the National Academy of Science USA, 105, 9931–9935. doi:10.1073/pnas.0802361105.

    Article  Google Scholar 

  • Mattos, P. P. (1999). Identificação de anéis anuais de crescimento e estimativa de idade e incremento anual em diâmetro de espécies nativas do Pantanal. MS. Doctoral thesis, Federal University of Parana.

  • Mcgonigle, T. P., Millers, M. H., Evans, D. G., Fairchild, G. L., & Swan, J. A. (1990). A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytologist, 115, 495–501. doi:10.1111/j.1469-8137.1990.tb00476.x.

    Article  Google Scholar 

  • Meharg, A. A., & Hartley-Whitaker, J. (2002). Arsenic uptake and metabolism in arsenic resistant and non-resistant plant species. New Phytologist, 154, 29–43. doi:10.1111/j.1469-8137.2008.02716.x.

    Article  CAS  Google Scholar 

  • Moreno-Jiménez, E., Peñalosa, J. M., Carpena-Ruiz, R. O., & Esteban, E. (2008). Comparison of arsenic resistance in Mediterranean woody shrubs used in restoration activities. Chemosphere, 71, 466–473. doi:10.1016/j.chemosphere.2007.10.030.

    Article  CAS  Google Scholar 

  • Moreno-Jiménez, E., Manzano, R., Esteban, E., & Peñalosa, J. M. (2010). The fate of arsenic in soils adjacent to an old mine site (Bustarviejo, Spain): Mobility and transfer to native flora. Journal of Soils and Sediments, 10, 301–312. doi:10.1007/s11368-009-0099-4.

    Article  CAS  Google Scholar 

  • Morton, J. B. (1988). Taxonomy of VAM fungi: Classification, nomenclature, and identification. Mycotaxon, 32, 267–324.

    Google Scholar 

  • Oliveira, A. S. (1986). Método simplificado para determinação colorimétrica de nitrogênio em plantas. Ciência e Cultura, 38, 178–180.

    Google Scholar 

  • Phillips, J. M., & Hayman, D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment for infection. Transactions of the British Mycological Society, 55, 158–161. doi:10.1016/S0007-1536(70)801103.

    Article  Google Scholar 

  • Pilon-Smits, E. (2005). Phytoremediation. Annual Review of Plant Biology, 56, 15–39. doi:10.1146/annurev.arplant.56.032604.144214.

    Article  CAS  Google Scholar 

  • Pulford, I. D., & Watson, C. (2003). Phytoremediation of heavy metal-contaminated land by trees—a review. Environment International, 29, 529–540. doi:10.1016/S0160-4120(02)00152-6.

    Article  CAS  Google Scholar 

  • Raab, A., Feldmann, J., & Meharg, A. A. (2004). The nature of arsenic-phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiology, 134, 1113–1122. doi:10.1104/pp. 103.033506.

    Article  CAS  Google Scholar 

  • Rajkumar, M., Sandhya, S., Prasad, M. N. V., & Freitas, H. (2012). Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnology Advances, 30, 1562–1574. doi:10.1016/j.biotechadv.2012.04.011.

    Article  CAS  Google Scholar 

  • Rauf, M. A., Hakim, M. A., Hanafi, M. M., Islam, M. M., Rahman, M. G. K., & Panaullah, G. M. (2011). Bioaccumulation of arsenic (As) and phosphorous by transplanting Aman rice in arsenic-contaminated clay soils. Australian Journal of Crop Science, 5, 1678–1684.

    CAS  Google Scholar 

  • Redman, A., Macalady, D., & Ahmann, D. (2002). Natural organic matter affects arsenic speciation and sorption onto hematite. Environmental Science & Technology, 3, 2889–2896. doi:10.1021/es0112801.

    Article  CAS  Google Scholar 

  • Reubens, B., Poesen, J., Danjon, F., Geudens, G., & Muys, B. (2007). The role of fine and coarse roots in shallow slope stability and soil erosion control with a focus on root system architecture: A review. Trees: Structure and Function, 21, 385–402. doi:10.1007/s00468-007-0132-4.

    Article  Google Scholar 

  • Rezende, P. S., Moura, P. A. S., Durão, W. A., Jr., Nascentes, C. C., Windmöller, C. C., & Costa, L. M. (2011). Arsenic and mercury mobility in Brazilian sediments from the São Francisco River Basin. Journal of the Brazilian Chemical Society, 22, 910–918.

    Article  CAS  Google Scholar 

  • Rillig, M. C., Wright, S. F., Nichols, K. A., Schmidt, W. F., & Torn, M. S. (2001). Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant and Soil, 233, 167–177. doi:10.1023/A:1010364221169.

    Article  CAS  Google Scholar 

  • Sarruge, J. R., & Haag, H. P. (1974). Análises químicas em plantas. São Paulo: Escola Superior de Agricultura Luiz de Queiroz (ESALQ).

    Google Scholar 

  • Scotti, M. R., & Corrêa, E. J. A. (2004). Growth and litter decomposition of woody species inoculated with rhizobia and arbuscular mycorrhizal fungi in Semiarid Brazil. Annals of Forest Science, 61, 87–95. doi:10.1051/forest:2003088.

    Article  Google Scholar 

  • Smith, S. E., & Read, D. J. (1981). Mycorrhizal symbiosis. San Diego: Academic.

    Google Scholar 

  • Smith, E., Naidu, R., & Alston, A. M. (2002). Chemistry of inorganic arsenic in soils: II. Effect of phosphorus, sodium, and calcium on arsenic sorption. Journal of Environmental Quality, 31, 557–563. doi:10.2134/jeq2002.5570.

    Article  CAS  Google Scholar 

  • Smith, S. E., Christophersen, H. M., Pope, S., & Smith, F. A. (2010). Arsenic uptake and toxicity in plants: Integrating mycorrhizal influences. Plant & Soil, 327, 1–21. doi:10.1007/s11104-009-0089-8.

    Article  CAS  Google Scholar 

  • Somasegaran, P., & Hoben, H. J. (1985). Methods in legume–rhizobium technology. Hawaii: University of Hawaii, Niftal.

    Google Scholar 

  • Thanabalasingam, P., & Pickering, W. F. (1986). Arsenic adsorption by humic acids. Environmental Pollution, 12, 233–246. doi:10.1016/0143-148X(86)90012-1.

    CAS  Google Scholar 

  • Tu, C., & Ma, L. Q. (2002). Effects of arsenic concentrations and forms on arsenic uptake by the hyperaccumulator ladder brake. Journal of Environmental Quality, 31, 641–647.

    Article  CAS  Google Scholar 

  • Walker, C., Mize, W., & McNabb, H. S. (1982). Populations of endogonaceous fungi at two locations in central Iowa. Canadian Journal of Botany, 60, 2518–2529. doi:10.1139/b82-305.

    Article  Google Scholar 

  • Wang, H. B., Wong, M. H., Lan, C. Y., Baker, A. J. M., Qin, Y. R., Shu, W. S., et al. (2007). Uptake and accumulation of arsenic by 11 Pteris taxa from southern China. Environmental Pollution, 145, 225–233. doi:10.1016/j.envpol.2006.03.015.

    Article  CAS  Google Scholar 

  • Wenzel, W. W. (2009). Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant & Soil, 321, 385–408. doi:10.1007/s11104-008-9686-1.

    Article  CAS  Google Scholar 

  • Wright, S. F., & Upadhyaya, A. A. (1998). Survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant & Soil, 198, 97–107. doi:10.1023/A:1004347701584.

    Article  CAS  Google Scholar 

  • Xie, Q., Yan, X., Liao, X., & Li, X. (2009). The arsenic hyperaccumulator fern Pteris vittata L. Environmental Science & Technology, 43, 8488–8495. doi:10.1021/es9014647.

    Article  CAS  Google Scholar 

  • Xu, H., Allard, B., & Grimvall, A. (1988). Influence of pH and organic substance on the adsorption of As(V) on geological material. Water, Air, Soil Pollution, 40, 293–305. doi:10.1007/BF00163734.

    CAS  Google Scholar 

  • Xu, P., Christie, P., Liu, Y., & Junling, L. Z. X. (2008). The arbuscular mycorrhizal fungus Glomus mosseae can enhance arsenic tolerance in Medicago truncatula by increasing plant phosphorus status and restricting arsenate uptake. Environmental Pollution, 156, 215–220. doi:10.1016/j.envpol.2008.01.003.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Biological Science, Federal University of Minas Gerais, Avenida Antonio Carlos, 6627, Pampulha, Cep: 31.270-901, Belo Horizonte, Minas Gerais, Brazil

    Marcelo P Gomes & Marina Lages Andrade

  2. Department of Chemistry, Federal University of Minas Gerais, Avenida Antonio Carlos, 6627, Pampulha, Cep: 31.270-901, Belo Horizonte, Minas Gerais, Brazil

    Clésia C Nascentes

  3. Department of Botany, Institute of Biological Science, Federal University of Minas Gerais, Avenida Antonio Carlos, 6627, Pampulha, Cep: 31.270-901, Belo Horizonte, Minas Gerais, Brazil

    Maria Rita Scotti

Authors
  1. Marcelo P Gomes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marina Lages Andrade
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Clésia C Nascentes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Rita Scotti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Rita Scotti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gomes, M.P., Andrade, M.L., Nascentes, C.C. et al. Arsenic Root Sequestration by a Tropical Woody Legume as Affected by Arbuscular Mycorrhizal Fungi and Organic Matter: Implications for Land Reclamation. Water Air Soil Pollut 225, 1919 (2014). https://doi.org/10.1007/s11270-014-1919-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-014-1919-8

Keywords

Search

Navigation