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

##plugins.themes.bootstrap3.article.main##

BELA PUTRA
LILI WARLY
EVITAYANI
BOPALION PEDI UTAMA

Abstract

Abstract. Putra B, Warly L, Evitayani, Utama BP. 2021. 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: 478-485. The increase of heavy metal pollution in the soil results from human activities such as gold mining, which impacts human and environmental health problems. Phytoremediation is an environmentally friendly, inexpensive, and efficient solution to overcome environmental damage caused by heavy metal contamination. Inoculation of AMF in dwarf Napier grass can reduce the level of metal contaminants in soil and subsequently its absorption in plant tissue. This study investigates the effect of arbuscular mycorrhizal fungi (AMF) on dwarf Napier grass (Pennisetum purpureum cv. Mott) plant growth and heavy metal remediation rates. The experiment was a completely randomized design with 4 levels of AMF inoculation (0, 5, 10, and 15 g/pot) with 5 repetitions. After eight weeks of potting experiments, shoot and root biomass, plant growth, heavy metal content in potting media were assessed. The results revealed that AMF inoculation of 10 g/pot exhibited a higher growth yield of dwarf Napier grass compared to other treatments (plant height (p<0.01), leaf length (P<0.01), leaf width (P<0.01), stem diameter (P<0.01) and plant fresh weight (P<0.01)), but had no significant effect on the number of leaves and number of shoots (P>0.05). AMF (10 g/pot) significantly affected root growth of dwarf Napier grass (root length (P<0.01), number of roots (P<0.05), and root fresh weight (P<0.01)). The results also showed that AMF increased the uptake of Al, Co, Cr, and Fe significantly in the growing media (Al (P<0.01), Co (P<0.05), Cr (P<0.01), Fe (P<0.05) but no significant effect on Pb (P>0.05). This study concluded that AMF effectively increased the growth of dwarf Napier grass and reduced heavy metal contaminants on gold mines tailings.

##plugins.themes.bootstrap3.article.details##

References
Adeyemi, N. O., Atayese, M. O., Sakariyawo, O. S., Azeez, J. O., Olubode, A. A., Ridwan, M., Adebiyi, A., Oni, O., & Ibrahim, I. (2021). Influence of different arbuscular mycorrhizal fungi isolates in enhancing growth, phosphorus uptake and grain yield of soybean in a phosphorus deficient soil under field conditions. Communications in Soil Science and Plant Analysis, 52(10). https://doi.org/10.1080/00103624.2021.1879117
Aguilera, P., Larsen, J., Borie, F., Berríos, D., Tapia, C., & Cornejo, P. (2018). New evidences on the contribution of arbuscular mycorrhizal fungi inducing Al tolerance in wheat. Rhizosphere, 5. https://doi.org/10.1016/j.rhisph.2017.11.002
Ali, H., Khan, E., & Ilahi, I. (2019). Environmental chemistry and ecotoxicology of hazardous heavy metals: Environmental persistence, toxicity, and bioaccumulation. In Journal of Chemistry (Vol. 2019). https://doi.org/10.1155/2019/6730305
Ashofie, I., & Prasetya, B. (2019). Pengaruh Aplikasi Kompos Dan Mikoriza Arbuskuar Pada Tailing Tambang Emas Terhadap Pertumbuhan Dan Serapan Fosfor Tanaman Bunga Matahari. Jurnal Tanah Dan Sumberdaya Lahan, 6(1).
Basyal, B., & 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). https://doi.org/10.1007/s00572-020-00992-6
Begum, N., Qin, C., Ahanger, M. A., Raza, S., Khan, M. I., Ashraf, M., Ahmed, N., & Zhang, L. (2019). Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance. In Frontiers in Plant Science (Vol. 10). https://doi.org/10.3389/fpls.2019.01068
Boonmeerati, U., & 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). https://doi.org/10.1061/(asce)hz.2153-5515.0000633
Chen, B., Nayuki, K., Kuga, Y., Zhang, X., Wu, S., & Ohtomo, R. (2018). Uptake and intraradical immobilization of cadmium by arbuscular mycorrhizal fungi as revealed by a stable isotope tracer and synchrotron radiation ?x-ray fluorescence analysis. Microbes and Environments, 33(3). https://doi.org/10.1264/jsme2.ME18010
Chen, M., Arato, M., Borghi, L., Nouri, E., & Reinhardt, D. (2018). Beneficial services of arbuscular mycorrhizal fungi – from ecology to application. In Frontiers in Plant Science (Vol. 9). https://doi.org/10.3389/fpls.2018.01270
Chen, W., Koide, R. T., & Eissenstat, D. M. (2018). Root morphology and mycorrhizal type strongly influence root production in nutrient hot spots of mixed forests. Journal of Ecology, 106(1). https://doi.org/10.1111/1365-2745.12800
Chu, Q., Sha, Z., Osaki, M., & Watanabe, T. (2017). Contrasting Effects of Cattle Manure Applications and Root-Induced Changes on Heavy Metal Dynamics in the Rhizosphere of Soybean in an Acidic Haplic Fluvisol: A Chronological Pot Experiment. Journal of Agricultural and Food Chemistry, 65(15). https://doi.org/10.1021/acs.jafc.6b05813
Conversa, G., Miedico, O., Chiaravalle, A. E., & Elia, A. (2019). Heavy metal contents in green spears of asparagus (Asparagus officinalis L.) grown in Southern Italy: Variability among farms, genotypes and effect of soil mycorrhizal inoculation. Scientia Horticulturae, 256. https://doi.org/10.1016/j.scienta.2019.108559
Crossay, T., Cavaloc, Y., Majorel, C., Redecker, D., Medevielle, V., & Amir, H. (2020). Combinations of different arbuscular mycorrhizal fungi improve fitness and metal tolerance of sorghum in ultramafic soil. Rhizosphere, 14. https://doi.org/10.1016/j.rhisph.2020.100204
Danh, L. T., Truong, P., Mammucari, R., & Foster, N. (2014). A Critical Review of the Arsenic Uptake Mechanisms and Phytoremediation Potential of Pteris vittata. In International Journal of Phytoremediation (Vol. 16, Issue 5). https://doi.org/10.1080/15226514.2013.798613
Entwistle, J. A., Hursthouse, A. S., Marinho Reis, P. A., & Stewart, A. G. (2019). Metalliferous Mine Dust: Human Health Impacts and the Potential Determinants of Disease in Mining Communities. In Current Pollution Reports (Vol. 5, Issue 3). https://doi.org/10.1007/s40726-019-00108-5
Fashola, M. O., Ngole-Jeme, V. M., & Babalola, O. O. (2016). Heavy metal pollution from gold mines: Environmental effects and bacterial strategies for resistance. In International Journal of Environmental Research and Public Health (Vol. 13, Issue 11). https://doi.org/10.3390/ijerph13111047
Favas, P. J. C., Sarkar, S. K., Rakshit, D., Venkatachalam, P., & Prasad, M. N. V. (2016). Acid Mine Drainages From Abandoned Mines: Hydrochemistry, Environmental Impact, Resource Recovery, and Prevention of Pollution. In Environmental Materials and Waste: Resource Recovery and Pollution Prevention. https://doi.org/10.1016/B978-0-12-803837-6.00017-2
Ghasemi Siani, N., Fallah, S., Pokhrel, L. R., & Rostamnejadi, A. (2017). Natural amelioration of Zinc oxide nanoparticle toxicity in fenugreek (Trigonella foenum-gracum) by arbuscular mycorrhizal (Glomus intraradices) secretion of glomalin. Plant Physiology and Biochemistry, 112. https://doi.org/10.1016/j.plaphy.2017.01.001
Haselwandter, K. (2008). Structure and function of siderophores produced by mycorrhizal fungi. Mineralogical Magazine, 72(1). https://doi.org/10.1180/minmag.2008.072.1.61
Hu, S., Hu, B., Chen, Z., Vosátka, M., & Vymazal, J. (2021). Arbuscular mycorrhizal fungi modulate the chromium distribution and bioavailability in semi-aquatic habitats. Chemical Engineering Journal, 420. https://doi.org/10.1016/j.cej.2021.129925
Husna, Tuheteru, F. D., & Arif, A. (2021). 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). https://doi.org/10.1007/s11676-020-01097-8
Joner, E. J., Roos, P., Jansa, J., Frossard, E., Leyval, C., & Jakobsen, I. (2004). No significant contribution of arbuscular mycorrhizal fungi to transfer of radiocesium from soil to plants. Applied and Environmental Microbiology, 70(11). https://doi.org/10.1128/AEM.70.11.6512-6517.2004
Khan, M. A., Mahmood-ur-Rahman, Ramzani, P. M. A., Zubair, M., Rasool, B., Khan, M. K., Ahmed, A., Khan, S. A., Turan, V., & Iqbal, M. (2020). Associative effects of lignin-derived biochar and arbuscular mycorrhizal fungi applied to soil polluted from Pb-acid batteries effluents on barley grain safety. Science of the Total Environment, 710. https://doi.org/10.1016/j.scitotenv.2019.136294
Kim, R. Y., Yoon, J. K., Kim, T. S., Yang, J. E., Owens, G., & Kim, K. R. (2015). Bioavailability of heavy metals in soils: definitions and practical implementation—a critical review. Environmental Geochemistry and Health, 37(6). https://doi.org/10.1007/s10653-015-9695-y
Krewski, D., Yokel, R. A., Nieboer, E., Borchelt, D., Cohen, J., Harry, J., Kacew, S., Lindsay, J., Mahfouz, A. M., & Rondeau, V. (2007). Human health risk assessment for aluminium, aluminium oxide, and aluminium hydroxide. In Journal of Toxicology and Environmental Health - Part B: Critical Reviews (Vol. 10, Issue SUPPL. 1). https://doi.org/10.1080/10937400701597766
Kullu, B., Patra, D. K., Acharya, S., Pradhan, C., & Patra, H. K. (2020). AM fungi mediated bioaccumulation of hexavalent chromium in Brachiaria mutica-a mycorrhizal phytoremediation approach. Chemosphere, 258. https://doi.org/10.1016/j.chemosphere.2020.127337
Lubis, J., A., Fikrinda, F., & Hifnalisa, H. (2021). Pengaruh Fungi Mikoriza Arbuskula dan Pupuk Kandang Terhadap Serapan Hara Kacang Hijau (Phaseolus radiatus L.) pada Ultisol. Jurnal Ilmiah Mahasiswa Pertanian, 6(2), 110–116.
Ma, Y., Rajkumar, M., Oliveira, R. S., Zhang, C., & Freitas, H. (2019). Potential of plant beneficial bacteria and arbuscular mycorrhizal fungi in phytoremediation of metal-contaminated saline soils. Journal of Hazardous Materials, 379. https://doi.org/10.1016/j.jhazmat.2019.120813
Mallick, I., Bhattacharyya, C., Mukherji, S., Dey, D., Sarkar, S. C., Mukhopadhyay, U. K., & Ghosh, A. (2018). Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: A step towards arsenic rhizoremediation. Science of the Total Environment, 610–611. https://doi.org/10.1016/j.scitotenv.2017.07.234
Manoharan, S., Ramalakshmi, O. I., & Ramasamy, S. (2021). Fungal Siderophores: Prospects and Applications. https://doi.org/10.1007/978-3-030-53077-8_9
Mishra, V., Gupta, A., Kaur, P., Singh, S., Singh, N., Gehlot, P., & Singh, J. (2016). Synergistic effects of Arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria in bioremediation of iron contaminated soils. International Journal of Phytoremediation, 18(7). https://doi.org/10.1080/15226514.2015.1131231
Ng, J. C., Ciminelli, V., Gasparon, M., & Caldeira, C. (2019). Health risk apportionment of arsenic from multiple exposure pathways in Paracatu, a gold mining town in Brazil. Science of the Total Environment, 673. https://doi.org/10.1016/j.scitotenv.2019.04.048
Ngole-Jeme, V. M., & Fantke, P. (2017). Ecological and human health risks associated with abandoned gold mine tailings contaminated soil. PLoS ONE, 12(2). https://doi.org/10.1371/journal.pone.0172517
Okereafor, U., Makhatha, M., Mekuto, L., Uche-Okereafor, N., Sebola, T., & Mavumengwana, V. (2020). Toxic metal implications on agricultural soils, plants, animals, aquatic life and human health. In International Journal of Environmental Research and Public Health (Vol. 17, Issue 7). https://doi.org/10.3390/ijerph17072204
Olobatoke, R. Y., & Mathuthu, M. (2016). Heavy metal concentration in soil in the tailing dam vicinity of an old gold mine in Johannesburg, South Africa. Canadian Journal of Soil Science, 96(3). https://doi.org/10.1139/cjss-2015-0081
Oyewo, O. A., Agboola, O., Onyango, M. S., Popoola, P., & Bobape, M. F. (2018). Current Methods for the Remediation of Acid Mine Drainage Including Continuous Removal of Metals From Wastewater and Mine Dump. In Bio-Geotechnologies for Mine Site Rehabilitation. https://doi.org/10.1016/B978-0-12-812986-9.00006-3
Prasad, M. N. V. (2003). Phytoremediation of Metal-Polluted Ecosystems: Hype for Commercialization. In Russian Journal of Plant Physiology (Vol. 50, Issue 5). https://doi.org/10.1023/A:1025604627496
Püschel, D., Bitterlich, M., Rydlová, J., & Jansa, J. (2020). Facilitation of plant water uptake by an arbuscular mycorrhizal fungus: a Gordian knot of roots and hyphae. Mycorrhiza, 30(2–3). https://doi.org/10.1007/s00572-020-00949-9
Raffo, A., Mozzanini, E., Ferrari Nicoli, S., Lupotto, E., & Cervelli, C. (2020). Effect of light intensity and water availability on plant growth, essential oil production and composition in Rosmarinus officinalis L. European Food Research and Technology, 246(1). https://doi.org/10.1007/s00217-019-03396-9
Riaz, M., Kamran, M., Fang, Y., Wang, Q., Cao, H., Yang, G., Deng, L., Wang, Y., Zhou, Y., Anastopoulos, I., & Wang, X. (2021). Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review. In Journal of Hazardous Materials (Vol. 402). https://doi.org/10.1016/j.jhazmat.2020.123919
Roychoudhury, A., & Chakraborty, S. (2021). Cobalt and molybdenum transport in plants. In Metal and Nutrient Transporters in Abiotic Stress. https://doi.org/10.1016/b978-0-12-817955-0.00010-7
Seguel, A., Cumming, J. R., Klugh-Stewart, K., Cornejo, P., & Borie, F. (2013). The role of arbuscular mycorrhizas in decreasing aluminium phytotoxicity in acidic soils: A review. Mycorrhiza, 23(3), 167–183. https://doi.org/10.1007/s00572-013-0479-x
Sharma, V., Parmar, P., & Kumari, N. (2016). Differential cadmium stress tolerance in wheat genotypes under mycorrhizal association. Journal of Plant Nutrition, 39(14). https://doi.org/10.1080/01904167.2016.1170851
Sheoran, V., Sheoran, A. S., & 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). https://doi.org/10.1080/10643380902718418
Singh, P., Nel, A., & Durand, J. F. (2017). The use of bioassays to assess the toxicity of sediment in an acid mine drainage impacted river in gauteng (South Africa). Water SA, 43(4). https://doi.org/10.4314/wsa.v43i4.15
Singh, S., & Fulzele, D. P. (2021). Phytoextraction of arsenic using a weed plant Calotropis procera from contaminated water and soil: growth and biochemical response. International Journal of Phytoremediation, 23(12). https://doi.org/10.1080/15226514.2021.1895717
Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., & Sutton, D. J. (2012). Heavy metal toxicity and the environment. In EXS (Vol. 101). https://doi.org/10.1007/978-3-7643-8340-4_6
Tisarum, R., Theerawitaya, C., Samphumphuang, T., Polispitak, K., Thongpoem, P., Singh, H. P., & Cha-um, S. (2020). Alleviation of Salt Stress in Upland Rice (Oryza sativa L. ssp. indica cv. Leum Pua) Using Arbuscular Mycorrhizal Fungi Inoculation. Frontiers in Plant Science, 11. https://doi.org/10.3389/fpls.2020.00348
Turan, V. (2021). Arbuscular mycorrhizal fungi and pistachio husk biochar combination reduces Ni distribution in mungbean plant and improves plant antioxidants and soil enzymes. Physiologia Plantarum, 173(1). https://doi.org/10.1111/ppl.13490
Vallejos-Torres, G., Espinoza, E., Marín-Díaz, J., Solis, R., & Arévalo, L. A. (2021). The Role of Arbuscular Mycorrhizal Fungi Against Root-Knot Nematode Infections in Coffee Plants. Journal of Soil Science and Plant Nutrition, 21(1). https://doi.org/10.1007/s42729-020-00366-z
Vymazal, J., Švehla, J., Kröpfelová, L., N?mcová, J., & Suchý, V. (2010). Heavy metals in sediments from constructed wetlands treating municipal wastewater. Biogeochemistry, 101(1). https://doi.org/10.1007/s10533-010-9504-8
Wang, Q., Mei, D., Chen, J., Lin, Y., Liu, J., Lu, H., & Yan, C. (2019). Sequestration of heavy metal by glomalin-related soil protein: Implication for water quality improvement in mangrove wetlands. Water Research, 148. https://doi.org/10.1016/j.watres.2018.10.043
Wei, Z., Van Le, Q., Peng, W., Yang, Y., Yang, H., Gu, H., Lam, S. S., & Sonne, C. (2021). A review on phytoremediation of contaminants in air, water and soil. Journal of Hazardous Materials, 403. https://doi.org/10.1016/j.jhazmat.2020.123658
Wu, S. C., Wong, C. C., Shu, W. S., Khan, A. G., & Wong, M. H. (2011). Mycorrhizo-remediation of lead/zinc mine tailings using vetiver: A field study. International Journal of Phytoremediation, 13(1). https://doi.org/10.1080/15226511003671353
Wu, S., Zhang, X., Chen, B., Wu, Z., Li, T., Hu, Y., Sun, Y., & Wang, Y. (2016). Chromium immobilization by extraradical mycelium of arbuscular mycorrhiza contributes to plant chromium tolerance. Environmental and Experimental Botany, 122. https://doi.org/10.1016/j.envexpbot.2015.08.006
Wu, S., Zhang, X., Huang, L., & Chen, B. (2019). Arbuscular mycorrhiza and plant chromium tolerance. In Soil Ecology Letters (Vol. 1, Issues 3–4). https://doi.org/10.1007/s42832-019-0015-9
Wu, Y., Chen, C., Li, J., & Wang, G. (2021). Effects of arbuscular mycorrhizal fungi on maize nitrogen uptake strategy under different soil water conditions. Plant and Soil, 464(1–2). https://doi.org/10.1007/s11104-021-04972-3
Xiao, Y., Liu, M., Chen, L., Ji, L., Zhao, Z., Wang, L., Wei, L., & Zhang, Y. (2020). Growth and elemental uptake of Trifolium repens in response to biochar addition, arbuscular mycorrhizal fungi and phosphorus fertilizer applications in low-Cd-polluted soils. Environmental Pollution, 260. https://doi.org/10.1016/j.envpol.2019.113761
Zhang, F., Liu, M., Li, Y., Che, Y., & 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. https://doi.org/10.1016/j.scitotenv.2018.11.317
Zhuo, F., Zhang, X. F., Lei, L. L., Yan, T. X., Lu, R. R., Hu, Z. H., & Jing, Y. X. (2020). The effect of arbuscular mycorrhizal fungi and biochar on the growth and Cd/Pb accumulation in Zea mays. International Journal of Phytoremediation, 22(10). https://doi.org/10.1080/15226514.2020.1725867