Arbuscular mycorrhiza and plant chromium tolerance

Abstract

Arbuscular mycorrhizal (AM) fungi are ubiquitous soil fungi that readily form symbiotic associations with most terrestrial plants. The growth and functions of AM fungi depend on carbohydrates supplied by the plants, in return, they assist the plants acquire mineral nutrients (e.g., phosphorus) from soil. The AM symbiosis also improves plant survival in various environments of unfavorable growth conditions, such as metal (loid) contaminated soil. It has been well demonstrated that AM symbiosis improved plant adaptation to Cr contaminated soil, which would have a great potential in phytoremediation and ecological restoration of Cr contaminated soils. By using Cr as an example case, we have reviewed the role of AM fungi in alleviation of Cr phytotoxicity and associated factors influencing AM plant Cr tolerance. AM symbiosis improves plant Cr tolerance through its direct roles in Cr stabilization and transformation and indirect roles via AM symbiosis mediated nutrient acquisition and physiological regulation. Future research perspectives on physiological and molecular mechanisms underlying Cr behavior and detoxification in AM symbiosis, as well as potential usage of AM fungi in ecological restoration and agriculture production in Cr contaminated soils were also proposed.

Keywords

Arbuscular mycorrhizal fungi / Heavy metal / Chromium / Tolerance / Translocation and transformation / Bioremediation

References

[1] Al-Ghamdi, A.A.M., Jais, H.M., 2012. Interaction between arbuscular mycorrhiza and heavy metals in the rhizosphere and roots of Juniperus procera. International Journal of Agriculture and Biology 14, 69–74.

[2] Aldrich, M.V., Gardea-Torresdey, J.L., Peralta-Videa, J.R., Parsons, J.G., 2003. Uptake and reduction of Cr(VI) to Cr(III) by mesquite (Prosopis spp.): chromate-plant interaction in hydroponics and solid media studied using XAS. Environmental Science & Technology 37, 1859–1864

[3] Allen, J.W., Shachar-Hill, Y., 2009. Sulfur transfer through an arbuscular mycorrhiza. Plant Physiology 149, 549–560

[4] Aloui, A., Recorbet, G., Gollotte, A., Robert, F., Valot, B., Gianinazzi-Pearson, V., Aschi-Smiti, S., Dumas-Gaudot, E., 2009. On the mechanisms of cadmium stress alleviation in Medicago truncatula by arbuscular mycorrhizal symbiosis: a root proteomic study. Proteomics 9, 420–433

[5] Appenroth, K.J., Bischoff, M., Gabryś H., Stoeckel, J., Swartz, H.M., Walczak, T., Winnefeld, K., 2000. Kinetics of chromium(V) formation and reduction in fronds of the duckweed Spirodela polyrhiza--a low frequency EPR study. Journal of Inorganic Biochemistry 78, 235–242

[6] Arias, J.A., Peralta-Videa, J.R., Ellzey, J.T., Ren, M., Viveros, M.N., Gardea-Torresdey, J.L., 2010a. Effects of Glomus deserticola inoculation on Prosopis: Enhancing chromium and lead uptake and translocation as confirmed by X-ray mapping, ICP-OES and TEM techniques. Environmental and Experimental Botany 68, 139–148

[7] Arias, J.A., Peralta-Videa, J.R., Ellzey, J.T., Viveros, M.N., Ren, M., Mokgalaka-Matlala, N.S., Castillo-Michel, H., Gardea-Torresdey, J.L., 2010b. Plant growth and metal distribution in tissues of Prosopis juliflora-velutina grown on chromium contaminated soil in the presence of Glomus deserticola. Environmental Science & Technology 44, 7272–7279

[8] Arshad, M., Ali, S., Noman, A., Ali, Q., Rizwan, M., Farid, M., Irshad, M.K., 2016. Phosphorus amendment decreased cadmium (Cd) uptake and ameliorates chlorophyll contents, gas exchange attributes, antioxidants, and mineral nutrients in wheat (Triticum aestivum L.) under Cd stress. Archives of Agronomy and Soil Science 62, 533–546

[9] Audet, P., Charest, C., 2007. Dynamics of arbuscular mycorrhizal symbiosis in heavy metal phytoremediation: meta-analytical and conceptual perspectives. Environmental Pollution 147, 609–614

[10] Azcón, R., del Carmen Perálvarez, M., Biro, B., Roldán A., Ruíz-Lozano J. M., 2009. Antioxidant activities and metal acquisition in mycorrhizal plants growing in a heavy-metal multicontaminated soil amended with treated lignocellulosic agrowaste. Applied Soil Ecology 41, 168–177

[11] Biro, I., Nemeth, T., Takacs, T., 2009. Changes of parameters of infectivity and efficiency of different Glomus mosseae arbuscular mycorrhizal fungi strains in cadmium-loaded soils. Communications in Soil Science and Plant Analysis 40, 227–239

[12] Bothe, H., Regvar, M., Turnau, K., 2010. Arbuscular mycorrhiza, heavy metal, and salt tolerance. In: Sherameti I and Varma A (ed.) Soil Heavy Metals, Springer, Berlin Heidelberg, pp 87–111.

[13] Carbonnel, S., Gutjahr, C., 2014. Control of arbuscular mycorrhiza development by nutrient signals. Frontiers of Plant Science 5, 462

[14] Catarecha, P., Segura, M.D., Franco-Zorrilla, J.M., García-Ponce, B., Lanza, M., Solano, R., Paz-Ares, J., Leyva, A., 2007. A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19, 1123–1133

[15] 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 mX-ray fluorescence analysis. Microbes and Environments 33, 257–263

[16] Chen, B., Roos, P., Borggaard, O.K., Zhu, Y.G., Jakobsen, I., 2005b. Mycorrhiza and root hairs in barley enhance acquisition of phosphorus and uranium from phosphate rock but mycorrhiza decreases root to shoot uranium transfer. New Phytologist 165, 591–598

[17] Chen, B., Tang, X., Zhu, Y., Christie, P., 2005a. Metal concentrations and mycorrhizal status of plants colonizing copper mine tailings: potential for revegetation. Science in China Series C 48, 156–164

[18] Chen, B., Xiao, X., Zhu, Y.G., Smith, F.A., Xie, Z.M., Smith, S.E., 2007b. The arbuscular mycorrhizal fungus Glomus mosseae gives contradictory effects on phosphorus and arsenic acquisition by Medicago sativa Linn. Science of the Total Environment 379, 226–234

[19] Chen, B.D., Li, X.L., Tao, H.Q., Christie, P., Wong, M.H., 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, 839–846

[20] Chen, B.D., Zhu, Y.G., Duan, J., Xiao, X.Y., Smith, S.E., 2007a. Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environmental Pollution 147, 374–380

[21] Chen, X., Wu, C., Tang, J., Hu, S., 2005c. Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment. Chemosphere 60, 665–671

[22] Christie, P., Li, X., Chen, B., 2004. Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant and Soil 261, 209–217

[23] Chu, Q., Wang, X., Yang, Y., Chen, F., Zhang, F., Feng, G., 2013. Mycorrhizal responsiveness of maize (Zea mays L.) genotypes as related to releasing date and available P content in soil. Mycorrhiza 23, 497–505

[24] Citterio, S., Prato, N., Fumagalli, P., Aina, R., Massa, N., Santagostino, A., Sgorbati, S., Berta, G., 2005. The arbuscular mycorrhizal fungus Glomus mosseae induces growth and metal accumulation changes in Cannabis sativa L. Chemosphere 59, 21–29

[25] Cornejo, P., Meier, S., Borie, G., Rillig, M.C., Borie, F., 2008. Glomalin-related soil protein in a Mediterranean ecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration. Science of the Total Environment 406, 154–160

[26] Coughlan, A.P., Dalpe, Y., Lapointe, L., Piché Y., 2000. Soil pH-induced changes in root colonization, diversity, and reproduction of symbiotic arbuscular mycorrhizal fungi from healthy and declining maple forests. Canadian Journal of Forest Research 30, 1543–1554

[27] Davies, F.T. Jr, Puryear, J.D., Newton, R.J., Egilla, J.N., Saraiva Grossi, J.A., 2001. Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). Journal of Plant Physiology 158, 777–786

[28] Davies, F.T. Jr, Puryear, J.D., Newton, R.J., Egilla, J.N., Saraiva Grossi, J.A., 2002. Mycorrhizal fungi increase chromium uptake by sunflower plants: Influence on tissue mineral concentration, growth, and gas exchange. Journal of Plant Nutrition 25, 2389–2407

[29] de María Guillén-Jiménez, F., Morales-Barrera, L., Morales-Jiménez, J., Hernández-Rodríguez, C.H., Cristiani-Urbina, E., 2008. Modulation of tolerance to Cr(VI) and Cr(VI) reduction by sulfate ion in a Candida yeast strain isolated from tannery wastewater. Journal of Industrial Microbiology & Biotechnology 35, 1277–1287

[30] de Oliveira, L.M., Lessl, J.T., Gress, J., Tisarum, R., Guilherme, L.R.G., Ma, L.Q., 2015. Chromate and phosphate inhibited each other’s uptake and translocation in arsenic hyperaccumulator Pteris vittata L. Environmental Pollution 197, 240–246

[31] Dietterich, L.H., Gonneau, C., Casper, B.B., 2017. Arbuscular mycorrhizal colonization has little consequence for plant heavy metal uptake in contaminated field soils. Ecological Applications 27, 1862–1875

[32] Dong, Y., Zhu, Y.G., Smith, F.A., 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

[33] Du, J., Yan, C., Li, Z., 2014. Phosphorus and cadmium interactions in Kandelia obovata (S. L.) in relation to cadmium tolerance. Environmental Science and Pollution Research International 21, 355–365

[34] Estaun, V., Cortes, A., Velianos, K., Camprubí A., Calvet, C., 2010. Effect of chromium contaminated soil on arbuscular mycorrhizal colonisation of roots and metal uptake by Plantago lanceolata. Spanish Journal of Agricultural Research 8, S109–S115

[35] Ferrol, N., Tamayo, E., Vargas, P., 2016. The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications. Journal of Experimental Botany 67, 6253–6265

[36] Gardezi, A.K., Barceló-Quintal, I.D., Cetina-Alcalá V.M., , (2005) Phytoremediation by Leucaena leucocephala in association with arbuscular endomycorrhiza and rhizobium in soil polluted by Cr. In: Callaos et al (ed) The 9th World Multiconference on Systemics, Cybernetics and Informatics. Orlando, Florida, USA, pp 289–298.

[37] Garg, N., Chandel, S., 2012. Role of Arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis in Cajanus cajan (L.) Millsp under NaCl and Cd stresses. Journal of Plant Growth Regulation 31, 292–308

[38] Gil-Cardeza, M.L., Ferri, A., Cornejo, P., Gomez, E., 2014. Distribution of chromium species in a Cr-polluted soil: presence of Cr(III) in glomalin related protein fraction. Science of the Total Environment 493, 828–833

[39] González-Chávez, M.C., Carrillo-González, R., Gutiérrez-Castorena, M.C., 2009. Natural attenuation in a slag heap contaminated with cadmium: the role of plants and arbuscular mycorrhizal fungi. Journal of Hazardous Materials 161, 1288–1298

[40] González-Chávez, M.C., Carrillo-González, 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

[41] 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

[42] Govindarajulu, M., Pfeffer, P.E., Jin, H., Abubaker, J., Douds, D.D., Allen, J.W., Bücking, H., Lammers, P.J., Shachar-Hill, Y., 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819–823

[43] Holland, S.L., Avery, S.V., 2011. Chromate toxicity and the role of sulfur. Metallomics 3, 1119–1123

[44] Jiang, Y, Wang, W, Xie, QLiu, N., Liu, L., Wang, D., Zhang, X., Yang, C., Chen, X., Tang, D., Wang, E., 2017. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science: 356, 1172–1175.

[45] Johansson, J.F., Paul, L.R., Finlay, R.D., 2004. Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiology Ecology 48, 1–13

[46] Karandashov, V., Bucher, M., 2005. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends in Plant Science 10, 22–29

[47] Khan, A.G., 2001. Relationships between chromium biomagnification ratio, accumulation factor, and mycorrhizae in plants growing on tannery effluent-polluted soil. Environment International 26, 417–423

[48] Kováčik, J., Babula, P., Klejdus, B., Hedbavny, J., 2013. Chromium uptake and consequences for metabolism and oxidative stress in chamomile plants. Journal of Agricultural and Food Chemistry 61, 7864–7873

[49] Kuga, Y., Saito, K., Nayuki, K., Peterson, R.L., Saito, M., 2008. Ultrastructure of rapidly frozen and freeze-substituted germ tubes of an arbuscular mycorrhizal fungus and localization of polyphosphate. New Phytologist 178, 189–200

[50] Lenoir, I., Fontaine, J., Lounès-Hadj Sahraoui, A., 2016. Arbuscular mycorrhizal fungal responses to abiotic stresses: A review. Phytochemistry 123, 4–15

[51] Leyval, C., Singh, B.R., Joner, E.J., 1995. Occurrence and infectivity of arbuscular mycorrhizal fungi in some Norwegian soils influenced by heavy metals and soil properties. Water, Air, and Soil Pollution 84, 203–216

[52] Leyval, C., Turnau, K., Haselwandter, K., 1997. Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7, 139–153

[53] Long, L.K., Yao, Q., Guo, J., Yang, R.H., Huang, Y.H., Zhu, H.H., 2010. Molecular community analysis of arbuscular mycorrhizal fungi associated with five selected plant species from heavy metal polluted soils. European Journal of Soil Biology 46, 288–294

[54] Losi, M., Amrhein, C., Frankenberger, W. Jr, (1994) Environmental biochemistry of chromium. In: Ware GW (ed) Reviews of Environmental Contamination and Toxicology, Springer, New York, NY, USA, pp 91–121.

[55] Ma, Y., Dickinson, N.M., Wong, M.H., 2006. Beneficial effects of earthworms and arbuscular mycorrhizal fungi on establishment of leguminous trees on Pb/Zn mine tailings. Soil Biology & Biochemistry 38, 1403–1412

[56] Malcová R., Vosátka, M., Gryndler, M., 2003. Effects of inoculation with Glomus intraradices on lead uptake by Zea mays L. and Agrostis capillaris L. Applied Soil Ecology 23, 55–67

[57] Miransari, M., 2011. Interactions between arbuscular mycorrhizal fungi and soil bacteria. Applied Microbiology and Biotechnology 89, 917–930

[58] Nakatani, A.S., Mescolotti, D.L.C., Nogueira, M.A., Martines, A.M., Miyauchi, M.Y.H., Stürmer, S.L., Cardoso, E.J.B.N., 2011. Dosage-dependent shift in the spore community of arbuscular mycorrhizal fungi following application of tannery sludge. Mycorrhiza 21, 515–522

[59] Nayuki, K., Chen, B., Ohtomo, R., Kuga, Y., 2014. Cellular imaging of cadmium in resin sections of arbuscular mycorrhizas using synchrotron micro X-ray fluorescence. Microbes and Environments 29, 60–66

[60] Nichols, K., 2003. Characterization of glomalinda glycoprotein produced by arbuscular mycorrhizal fungi. PhD Dissertation, University of Maryland, College Park, Maryland.

[61] Orłowska, E., Przybyłowicz, W., Orlowski, D., Turnau, K., Mesjasz-Przybyłowicz, J., 2011. The effect of mycorrhiza on the growth and elemental composition of Ni-hyperaccumulating plant Berkheya coddii Roessler. Environmental Pollution 159, 3730–3738

[62] Pereira, Y., Lagniel, G., Godat, E., Baudouin-Cornu, P., Junot, C., Labarre, J., 2008. Chromate causes sulfur starvation in yeast. Toxicological Sciences 106, 400–412

[63] Rahmaty, R., Khara, J., 2011. Effects of vesicular arbuscular mycorrhiza Glomus intraradices on photosynthetic pigments, antioxidant enzymes, lipid peroxidation, and chromium accumulation in maize plants treated with chromium. Turkish Journal of Biology 35, 51–58.

[64] Repetto, O., Bestel-Corre, G., Dumas-Gaudot, E., Berta, G., Gianinazzi-Pearson, V., Gianinazzi, S., 2003. Targeted proteomics to identify cadmium-induced protein modifications in Glomus mosseae-inoculated pea roots. New Phytologist 157, 555–567

[65] Rufyikiri, G., Thiry, Y., Declerck, S., 2003. Contribution of hyphae and roots to uranium uptake and translocation by arbuscular mycorrhizal carrot roots under root-organ culture conditions. New Phytologist 158, 391–399

[66] Shanker, A.K., Cervantes, C., Loza-Tavera, H., Avudainayagam, S., 2005. Chromium toxicity in plants. Environment International 31, 739–753

[67] Shanker, A.K., Pathmanabhan, G., 2004. Speciation dependant antioxidative response in roots and leaves of sorghum (Sorghum bicolor (L.) Moench cv CO 27) under Cr(III) and Cr (VI) stress. Plant and Soil 265, 141–151

[68] Sharma, D.C., Sharma, C.P., Tripathi, R.D., 2003. Phytotoxic lesions of chromium in maize. Chemosphere 51, 63–68

[69] Singh, J., Kumar, M., Vyas, A., 2014. Healthy response from chromium survived pteridophytic plant-Ampelopteris prolifera with the interaction of mycorrhizal fungus-Glomus deserticola. International Journal of Phytoremediation 16, 524–535

[70] Singh, S., Parihar, P., Singh, R., Prasad, S.M., 2015. Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Frontiers of Plant Science, 6, 1143.

[71] Skeffington, R.A., Shewry, P.R., Peterson, P.J., 1976. Chromium uptake and transport in barley seedlings (Hordeum vulgare L.). Planta 132, 209–214

[72] Smith, S.E., Read, D., (2008) Mycorrhizal Symbiosis. Academic Press, San Diego.

[73] Subramanian, K.S., Tenshia, V., Jayalakshmi, K., Ramachandran, V., 2009. Biochemical changes and zinc fractions in arbuscular mycorrhizal fungus (Glomus intraradices) inoculated and uninoculated soils under differential zinc fertilization. Applied Soil Ecology 43, 32–39

[74] Sun, Y., Zhang, X., Wu, Z., Hu, Y., Wu, S., Chen, B., 2016. The molecular diversity of arbuscular mycorrhizal fungi in the arsenic mining impacted sites in Hunan Province of China. Journal of Environmental Sciences (China) 39, 110–118

[75] Vodnik, D., Grcman, H., Macek, I., van Elteren, J.T., Kovacevic, M., 2008. The contribution of glomalin-related soil protein to Pb and Zn sequestration in polluted soil. Science of the Total Environment 392, 130–136

[76] Wang, F., 2017. Occurrence of arbuscular mycorrhizal fungi in mining-impacted sites and their contribution to ecological restoration: Mechanisms and applications. Critical Reviews in Environmental Science and Technology 47, 1901–1957

[77] Weiersbye, I.M., Straker, C.J., Przybylowicz, W.J., 1999. Micro-PIXE mapping of elemental distribution in arbuscular mycorrhizal roots of the grass, Cynodon dactylon, from gold and uranium mine tailings. Nuclear Instruments and Methods in Physics Research Section B 158, 335–343

[78] Weissenhorn, I., Leyval, C., Berthelin, J., 1995. Bioavailability of heavy metals and abundance of arbuscular mycorrhiza in a soil polluted by atmospheric deposition from a smelter. Biology and Fertility of Soils 19, 22–28

[79] Wu, S., Vosátka, M., Vogel-Mikus, K., Kavčič A., Kelemen, M., Šepec, L., Pelicon, P., Skála, R., Valero Powter, A.R., Teodoro, M., Michálková Z., Komárek, M., 2018b. Nano zero-valent iron mediated metal (loid) uptake and translocation by arbuscular mycorrhizal symbioses. Environmental Science & Technology 52, 7640–7651

[80] Wu, S., Zhang, X., Sun, Y., Wu, Z., Li, T., Hu, Y., Lv, J., Li, G., Zhang, Z., Zhang, J., Zheng, L., Zhen, X., Chen, B., 2016b. Chromium immobilization by extra-and intraradical fungal structures of arbuscular mycorrhizal symbioses. Journal of Hazardous Materials 316, 34–42

[81] Wu, S., Zhang, X., Sun, Y., Wu, Z., Li, T., Hu, Y., Su, D., Lv, J., Li, G., Zhang, Z., Zheng, L., Zhang, J., Chen, B., 2015. Transformation and immobilization of chromium by arbuscular mycorrhizal fungi as revealed by SEM-EDS, TEM-EDS, and XAFS. Environmental Science & Technology 49, 14036–14047

[82] Wu, S.L., Chen, B.D., Sun, Y.Q., Ren, B.H., Zhang, X., Wang, Y.S., 2014. Chromium resistance of dandelion (Taraxacum platypecidum Diels.) and bermudagrass (Cynodon dactylon [Linn.] Pers.) is enhanced by arbuscular mycorrhiza in Cr(VI)-contaminated soils. Environmental Toxicology and Chemistry 33, 2105–2113

[83] Wu, S.L., Hu, Y.J., Zhang, X., Sun, Y., Wu, Z., Li, T., Lv, J., Li, J., Zhang, J., Zheng, L., Huang, L., Chen, B., 2018a. Chromium detoxification in arbuscular mycorrhizal symbiosis mediated by sulfur uptake and metabolism. Environmental and Experimental Botany 147, 43–52

[84] Wu, S.L., Zhang, X., Chen, B.D., 2013. Effects of Arbuscular mycorrhizal fungi on heavy metal translocation and transformation in the soil-plant continuum. Asian Journal of Ecotoxicology 8, 847–856 (in Chinese).

[85] Wu, S.L., Zhang, X., Chen, B.D., Wu, Z., Li, T., Hu, Y., Sun, Y., Wang, Y., 2016a. Chromium immobilization by extraradical mycelium of arbuscular mycorrhiza contributes to plant chromium tolerance. Environmental and Experimental Botany 122, 10–18

[86] Yang, Y., Han, X., Liang, Y., Ghosh, A., Chen, J., Tang, M., 2015. The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS One 10, e0145726

[87] Yu, Y., Zhang, S., Huang, H., Luo, L., Wen, B., 2009. Arsenic accumulation and speciation in maize as affected by inoculation with arbuscular mycorrhizal fungus Glomus mosseae. Journal of Agricultural and Food Chemistry 57, 3695–3701

[88] Yu, Y., Zhang, S.Z., Huang, H.L., Wu, N., 2010. Uptake of arsenic by maize inoculated with three different arbuscular mycorrhizal fungi. Communications in Soil Science and Plant Analysis 41, 735–743

[89] Yu, Y.G., Zhao, B., 2008. The interaction and effect of two species of arbuscular mycorrhizal fungi on the growth of Astragalus sinicus L at different pH level. Mycosystema 27, 209–216 (in Chinese).

[90] Zarei, M., Hempel, S., Wubet, T., Schäfer, T., Savaghebi, G., Jouzani, G.S., Nekouei, M.K., Buscot, F., 2010. Molecular diversity of arbuscular mycorrhizal fungi in relation to soil chemical properties and heavy metal contamination. Environmental Pollution 158, 2757–2765

[91] Zayed, A., Lytle, C.M., Qian, J.H., Terry, N., 1998. Chromium accumulation, translocation and chemical speciation in vegetable crops. Planta 206, 293–299

[92] Zhang, S., Feng, G., Li, X., 2005. The direct effect of cadmium in soil on growth of arbuscular mycorrhizal fungi Glomus mosseae. Mycosystema 24, 576–581 (in Chinese).

[93] Zhang, X., Ren, B.H., Wu, S.L., Sun, Y.Q., Lin, G., Chen, B.D., 2015. Arbuscular mycorrhizal symbiosis influences arsenic accumulation and speciation in Medicago truncatula L. in arsenic-contaminated soil. Chemosphere 119, 224–230

[94] Zhang, X.H., Lin, A.J., Zhang, X., Guo, L.P. 2012. The effects of arbuscular mycorrhizal fungi (AMF) on forms of Pb in the upland rice rhizosphere. Chinese Agricultural Science Bulletin 28, 24–29 (in Chinese).

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