Effect of arbuscular mycorrhizal fungi on nutrients and heavy metals uptake by Pennisetum purpureum cv Mott in phytoremediation of gold mine tailings


  • Bela Putra Department of Animal Science, Faculty of Agriculture, Universitas Muara Bungo. Jl. Pendidikan, Muara Bungo, Bungo 37215, Jambi, Indonesia.
  • Lili Warly Department of Animal Science, Faculty of Animal Husbandry, Universitas Andalas. Jl. Unand, Limau Manis, Pauh, Padang 25175, West Sumatra, Indonesia.
  • Evitayani Evitayani Department of Animal Science, Faculty of Animal Husbandry, Universitas Andalas. Jl. Unand, Limau Manis, Pauh, Padang 25175, West Sumatra, Indonesia.
  • Bopalion Pedi Utama Department of Animal Science, Faculty of Agriculture, Universitas Muara Bungo. Jl. Pendidikan, Muara Bungo, Bungo 37215, Jambi, Indonesia.




bioconcentration factor, mercury amalgamation, translocation factor, removal efficiency


Mercury composite and cyanidation are gold mining methods that are frequently used. The mercury composite method produces tailings containing heavy metals that can harm living organisms. Utilisation of tailings for the development of forage may be enhanced through arbuscular mycorrhizal fungi (AMF) inoculation to increase plant resistance, absorption of macro and micronutrients, and reduce levels of metal contaminants in the tailings. This study aimed to investigate the effect of arbuscular mycorrhizal fungi on nutrients and heavy metals uptake by Pennisetum purpureum cv Mott in phytoremediation of gold mine tailings. Treatments consisted of four levels of AMF inoculation (0, 5, 10 and 15 g pot-1) were arranged in a completely randomised design with five replications. Each pot contained 3 kg of tailings. The results showed that the best crude protein, crude fiber, crude fat, Ca, and P contents in the plant shoots was obtained by providing AMF inoculation of 15 g pot-1. However, the treatment had no significant effect on dry weight, dry matter, and nitrogen-free extract. AMF significantly increased the uptake of heavy metals by the plant roots. The treatments did not significantly affect Pb uptake by plant roots and shoots and Hg uptake by plant shoots. AMF treatments significantly reduced the translocation factor (TF) value for Hg, bioconcentration factor (BCF) values for Cd and Pb, and removal efficiency (RE) values for Cd and Pb. AMF could effectively increase nutrient absorption in the plant shoots, reduce Cd, Hg, and Pb translocation in plant shoots, and reduce Cd, Hg, and Pb in the tailings.


Alford, É.R., Pilon-Smits, E.A.H. and Paschke, M.W. 2010. Metallophytes-a view from the rhizosphere. Plant and Soil 337(1):33-50, doi:10.1007/s11104-010-0482-3

Alotaibi, M.O., Saleh, A.M., Sobrinho, R.L., Sheteiwy, M.S., Elâ€sawah, A.M., Mohammed, A.E. and Abdelgawad, H. 2021. Arbuscular mycorrhizae mitigate aluminum toxicity and regulate proline metabolism in plants grown in acidic soil. Journal of Fungi 7(7):531, doi:10.3390/jof7070531.

Arnot, J.A. and Gobas, F.A.P.C. 2006. A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environmental Reviews 14(4:257-297, doi:10.1139/A06-005.

Atteya, A.K.G., Sami, R., Al-Mushhin, A.A.M., Ismail, K.A. and Genaidy, E.A.E. 2021. Response of seeds, oil yield and fatty acids percentage of Jojoba shrub strain EAI to mycorrhizal fungi and moringa leaves extract. Horticulturae 7(10):395, doi:10.3390/ horticulturae7100395.

Bae, Y.Y., Choi, Y.M., Kim, M.J., Kim, K.H., Kim, B.C. and Rhee, M.S. 2011. Application of supercritical carbon dioxide for microorganism reductions in fresh pork. Journal of Food Safety 31(4):511-517, doi:10.1111/j.1745-4565.2011.00328.x.

Basyal, B. and Emery, S.M. 2021. An arbuscular mycorrhizal fungus alters switchgrass growth, root architecture, and cell wall chemistry across a soil moisture gradient. Mycorrhiza 31(2):251-258, doi:10.1007/s00572-020-00992-6.

Bhantana, P., Rana, M.S., Sun, X.C., Moussa, M.G., Saleem, M.H., Syaifudin, M., Shah, A., Poudel, A., Pun, A.B., Bhat, M.A., Mandal, D.L., Shah, S., Zhihao, D., Tan, Q. and Hu, C.X. 2021. Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and phytoremediation. Symbiosis 84(12), doi:10.1007/s13199-021-00756-6.

Bonfante, P. and Genre, A. 2010. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Communications 1(4), Article number: 48 (2010), doi:10.1038/ncomms1046.

Boonmeerati, U. and Sampanpanish, P. 2021. Enhancing arsenic phytoextraction of dwarf Napier grass (Pennisetum purpureum cv. Mott) from gold mine tailings by electrokinetics remediation with phosphate and EDTA. Journal of Hazardous, Toxic, and Radioactive Waste 25(4), doi:10.1061/(asce)hz.2153-5515.0000633.

Brundrett, M.C. and Tedersoo, L. 2020. Resolving the mycorrhizal status of important northern hemisphere trees. Plant and Soil 454(1-2):3-34, doi:10.1007/s11104-020-04627-9.

Bundschuh, J., Maity, J.P., Nath, B., Baba, A., Gunduz, O., Kulp, T.R., Jean, J.S., Kar, S., Yang, H.J., Tseng, Y.J., Bhattacharya, P. and Chen, C.Y. 2013. Naturally occurring arsenic in terrestrial geothermal systems of western Anatolia, Turkey: Potential role in contamination of freshwater resources. Journal of Hazardous Materials 262:951-959, doi:10.1016/j.jhazmat.2013.01.039.

Chen, M., Arato, M., Borghi, L., Nouri, E. and Reinhardt, D. 2018. Beneficial services of arbuscular mycorrhizal fungi from ecology to application. Frontiers in Plant Science 9, doi:10.3389/fpls.2018.01270.

Chen, S., Zhang, S., Yan, Z., Peng, Y. and Chen, Q. 2019. Differences in main processes to transform phosphorus influenced by ammonium nitrogen in flooded intensive agricultural and steppe soils. Chemosphere 22(6), doi:10.1016/j.chemosphere.2019.03.123.

Christie, P., Li, X. and Chen, B. 2004. Arbuscular mycorrhiza can depress the translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant and Soil 261(1-2):209-217, doi:10.1023/B:PLSO.0000035542.79345.1b.

Colpaert, J.V., Wevers, J.H.L., Krznaric, E. and Adriaensen, K. 2011. How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution. Annals of Forest Science 68(1):17-24, doi:10.1007/s13595-010-0003-9.

Danh, L.T., Truong, P., Mammucari, R. and Foster, N. 2014. A critical review of the arsenic uptake mechanisms and phytoremediation potential of Pteris vittata. International Journal of Phytoremediation 16(5):429-453, doi:10.1080/15226514.2013.798613.

Dhalaria, R., Kumar, D., Kumar, H., Nepovimova, E., Kuca, K., Islam, M.T. and Verma, R. 2020. Arbuscular mycorrhizal fungi as potential agents in ameliorating heavy metal stress in plants. Agronomy 10(6), doi:10.3390/agronomy10060815.

Fashola, M.O., Ngole-Jeme, V.M. and Babalola, O.O. 2016. Heavy metal pollution from gold mines: Environmental effects and bacterial strategies for resistance. International Journal of Environmental Research and Public Health 13(11), doi:10.3390/ijerph13111047.

Fiorilli, V., Catoni, M., Miozzi, L., Novero, M., Accotto, G.P. and Lanfranco, L. 2009. Global and cell-type gene expression profiles in tomato plants colonised by an arbuscular mycorrhizal fungus. New Phytologist 184(4), doi:10.1111/j.1469-8137.2009.03031.x.

Gupta, M.M. and Abbott, L.K. 2021. Exploring economic assessment of the arbuscular mycorrhizal symbiosis. Symbiosis 83(2), doi:10.1007/s13199-020-00738-0.

Holford, I.C.R. 1997. Soil phosphorus: Its measurement and its uptake by plants. Australian Journal of Soil Research 35(2), doi:10.1071/S96047.

Husna, Tuheteru, F.D. and Arif, A. 2021a. Arbuscular mycorrhizal fungi to enhance the growth of tropical endangered species Pterocarpus indicus and Pericopsis mooniana in post gold mine field in southeast Sulawesi, Indonesia. Biodiversitas 22(9):3844-3853, doi:10.13057/biodiv/d220930.

Husna, Tuheteru, F.D. and Arif, A. 2021b. The potential of arbuscular mycorrhizal fungi to conserve Kalappia celebica, an endangered endemic legume on gold mine tailings in Sulawesi, Indonesia. Journal of Forestry Research 32(2), doi:10.1007/s11676-020-01097-8.

Jaelani, L.M., Nurgiantoro, and Putri, R.A. 2018. Analysis of land cover change due to gold mining in Bombana using Sentinel 1A radar data. International Journal of Geoinformatics 14(2):1-7.

Joner, E.J., Roos, P., Jansa, J., Frossard, E., Leyval, C. and Jakobsen, I. 2004. No significant contribution of arbuscular mycorrhizal fungi to the transfer of radiocesium from soil to plants. Applied and Environmental Microbiology 70(11):6512-6517, doi:10.1128/AEM.70.11.6512-6517.2004.

Kim, S., Lim, H. and Lee, I. 2010. Enhanced heavy metal phytoextraction by Echinochloa crus-galli using root exudates. Journal of Bioscience and Bioengineering 109(1):47-50, doi:10.1016/j.jbiosc.2009.06.018.

Kord, B., Mataji, A. and Babaie, S. 2010. Pine (Pinus eldarica Medw.) needles as an indicator of heavy metals pollution. International Journal of Environmental Science and Technology 7(1):79-84, doi:10.1007/BF03326119.

Kullu, B., Patra, D.K., Acharya, S., Pradhan, C. and Patra, H.K. 2020. AM fungi mediated bioaccumulation of hexavalent chromium in Brachiaria mutica-a mycorrhizal phytoremediation approach. Chemosphere 258, doi:10.1016/j.chemosphere.2020.127337.

Kumar, V., Kumar, P., Kumar, P. and Singh, J. 2020. Anaerobic digestion of Azolla pinnata biomass grown in integrated industrial effluent for enhanced biogas production and COD reduction: Optimisation and kinetics studies. Environmental Technology and Innovation 17, doi:10.1016/j.eti.2020.100627.

Leung, H.M., Wu, F.Y., Cheung, K.C., Ye, Z.H. and Wong, M.H. 2010. The effect of arbuscular mycorrhizal fungi and phosphate amendment on arsenic uptake, accumulation and growth of Pteris vittata in As-contaminated soil. International Journal of Phytoremediation 12(4):384-403, doi:10.1080/15226510903051740.

Leyval, C., Turnau, K. and Haselwandter, K. 1997. Effect of heavy metal pollution on mycorrhizal colonisation and function: Physiological, ecological and applied aspects. Mycorrhiza 7(3):139-153, doi:10.1007/s005720050174.

Liu, M., Zhao, Z., Chen, L., Wang, L., Ji, L. and Xiao, Y. 2020. Influences of arbuscular mycorrhizae, phosphorus fertiliser and biochar on alfalfa growth, nutrient status and cadmium uptake. Ecotoxicology and Environmental Safety 196, doi:10.1016/j.ecoenv.2020.110537.

Lone, M.I., He, Z.L., Stoffella, P. and Yang, X.E. 2008. Phytoremediation of heavy metal polluted soils and water: Progress and perspectives. Journal of Zhejiang University: Science 9(3):210-220, doi:10.1631/jzus.B0710633.

Ma, Y., Rajkumar, M., Oliveira, R.S., Zhang, C. and Freitas, H. 2019. Potential of plant beneficial bacteria and arbuscular mycorrhizal fungi in phytoremediation of metal-contaminated saline soils. Journal of Hazardous Materials 379, doi:10.1016/j.jhazmat.2019.120813.

Mellem, J.J. 2012. Bioaccumulation of Cr, Hg, As, Pb, Cu and Ni with the ability for hyperaccumulation by Amaranthus dubius. African Journal of Agricultural Research 7(4):591-596, doi:10.5897/ajar11.1486.

Morgan, J.A.W., Bending, G.D. and White, P.J. 2005. Biological costs and benefits to plant-microbe interactions in the rhizosphere. Journal of Experimental Botany 56(417):1729-1739, doi:10.1093/jxb/eri205.

Ndimele, P.E. and Jimoh, A.A. 2011. Water hyacinth (Eichhornia crassipes (Mart.) Solms.) in phytoremediation of heavy metal polluted water of Ologe Lagoon, Lagos, Nigeria. Research Journal of Environmental Sciences 5(5):424-433, doi:10.3923/rjes.2011.424.433.

Patra, D.K., Pradhan, C., Kumar, J. and Patra, H.K. 2020. Assessment of chromium phytotoxicity, phytoremediation and tolerance potential of Sesbania sesban and Brachiaria mutica grown on chromite mine overburden dumps and garden soil. Chemosphere 252, doi:10.1016/j.chemosphere.2020.126553.

Putra, B., Warly, L., Evitayani, and Utama, B.P. 2022. The role of arbuscular mycorrhizal fungi in phytoremediation of heavy metals and their effect on the growth of Pennisetum purpureum cv. Mott on gold mine tailings in Muara Bungo, Jambi, Indonesia. Biodiversitas 23(1):478-485, doi:10.13057/biodiv/d230151.

Rezaeian, M., Moghadam, M.T, Kiaei, M.M. and Zadeh, H.M. 2020. The effect of heavy metals on the nutritional value of Alfalfa: comparison of nutrients and heavy metals of Alfalfa (Medicago sativa) in industrial and non-industrial areas. Toxicological Research 36(2):183-193, doi:10.1007/s43188-019-00012-6.

Sharma, V., Parmar, P. and Kumari, N. 2016. Differential cadmium stress tolerance in wheat genotypes under mycorrhizal association. Journal of Plant Nutrition 39(14):2025-2036, doi:10.1080/01904167.2016. 1170851.

Sheoran, V., Sheoran, A.S. and Poonia, P. 2011. Role of hyperaccumulators in phytoextraction of metals from contaminated mining sites: A review. Critical Reviews in Environmental Science and Technology 41(2):168-214, doi:10.1080/10643380902718418.

Tian, W., Zhang, C.Q., Qiao, P. and Milne, R. 2011. Diversity of culturable ericoid mycorrhizal fungi of Rhododendron decorum in Yunnan, China. Mycologia 103(4):703-709, doi:10.3852/10-296.

Vamerali, T., Bandiera, M. and Mosca, G. 2010. Field crops for phytoremediation of metal-contaminated land. A review. Environmental Chemistry Letters 8(1):1-17, doi:10.1007/s10311-009-0268-0.

Wahl, M., Shahnaz, L., Dobretsov, S., Saha, M., Symanowski, F., David, K., Lachnit, T., Vasel, M. and Weinberger, F. 2010. Ecology of antifouling resistance in the bladder wrack Fucus vesiculosus: Patterns of microfouling and antimicrobial protection. Marine Ecology Progress Series 411:33-48, doi:10.3354/meps08644.

Wang, Y. and Greger, M. 2004. Clonal differences in mercury tolerance, accumulation, and distribution in Willow. Journal of Environmental Quality 33(5):1779-1785, doi:10.2134/jeq2004.1779.

Wei, Z., Van Le, Q., Peng, W., Yang, Y., Yang, H., Gu, H., Lam, S.S. and Sonne, C. 2021. A review on phytoremediation of contaminants in air, water and soil. Journal of Hazardous Materials 403, doi:10.1016/j.jhazmat.2020.123658.

Wu, Q., Wang, S., Thangavel, P., Li, Q., Zheng, H., Bai, J. and Qiu, R. 2011. Phytostabilisation potential of Jatropha curcas in polymetallic acid mine tailings. International Journal of Phytoremediation 13(8):788-804, doi:10.1080/15226514.2010.525562.

Wu, S., Zhang, X., Huang, L. and Chen, B. 2019. Arbuscular mycorrhiza and plant chromium tolerance. Soil Ecology Letters 1( 3-4):94-104, doi:10.1007/s42832-019-0015-9.

Zhang, F., Liu, M., Li, Y., Che, Y. and Xiao, Y. 2019. Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa. Science of The Total Environment 655:1150-1158, doi:10.1016/j.scitotenv.2018.11.317.








How to Cite

Putra, B., Warly, L., Evitayani, E., & Utama, B. P. (2022). Effect of arbuscular mycorrhizal fungi on nutrients and heavy metals uptake by Pennisetum purpureum cv Mott in phytoremediation of gold mine tailings. Journal of Degraded and Mining Lands Management, 10(1), 3795–3802. https://doi.org/10.15243/jdmlm.2022.101.3795



Research Article