Skip to main content
SpringerLink
Log in

A non-toxic polymer enhances sorghum-mycorrhiza symbiosis for bioremediation of Cd

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

In this study, the effect of a mycorrhizal symbiosis on the translocation of Cd from Cd-polluted soil to sorghum roots was investigated using rhizoboxes. A factorial experiment (two factors including fungus inoculation and Cd contamination) in a completely randomized design with three replicates was performed. In the rhizobox rhizosphere compartment, plants were cultivated in uncontaminated soil and mycorrhizal inoculation (inoculated with Claroideoglomus etunicatum or non-inoculated) was performed, and in the other compartment, the soil was contaminated with Cadmium (Cd) at one of three levels (0, 100 mg kg−1 using a non-toxic organic polymer (poly (N-vinyl succinate))–Cd, or 100 mg kg−1 using Cd-nitrate). Cd pollution resulted in a significant decrease in shoot dry weight (from 7.52 to 6.18 and 6.68 g pot−1, from control to polymer-Cd and nitrate-Cd respectively), root mycorrhizal colonization (from 32.33% to 8.16% and 8.33%), shoot phosphorus concentration (from 3.14 to 2.80 and 2.76 g kg−1), and soil carbohydrate (from 12.05 to 10.74 and 10.24 mg g−1), and also resulted in significant increases in soil glomalin (from 595.55 to 660.52 and 690.39 μg g−1). The use of mycorrhizal fungi increased the glomalin content of the soil and improved the studied parameters. The results revealed the key role of Claroideoglomus etunicatum in translocation of Cd in the rhizobox and also in precise control of Cd concentration of plant tissues (increase or decrease of them depending on Cd composition and Cd availability). Poly(N-vinyl succinate) increased Cd availability and Cd concentration of shoot tissue (5.19 mg kg−1) compared to nitrate-Cd (3.68 mg kg−1) and could be recommended for improving phytoremediation.

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
Fig. 7

Similar content being viewed by others

References

  • Adiloğlu S, Turgut Sağlam M, Adiloğlu A, Süme A (2016) Phytoremediation of nickel (Ni) from agricultural soils using canola (Brassica napus L.). Desalin Water Treat 57(6):2383–2388

    Article  CAS  Google Scholar 

  • Amin M, Flowers TH (2004) Evaluation of Kjeldahl digestion method. J Res Sci 15(2):159–179

    Google Scholar 

  • Awokunmi EE, Asaolu SS, Ajayi OO, Adebayo OA (2012) The role of EDTA on heavy metals phytoextraction by Jatropha gossypifolia grown on soil collected from dumpsites in Ekiti state Nigeria. Brit J Environ Climate Change 2(2):153–162

    Article  Google Scholar 

  • Barbosa B, Boléo S, Sidella S, Costa J, Duarte MP, Mendes B, Fernando AL (2015) Phytoremediation of heavy metal-contaminated soils using the perennial energy crops Miscanthus spp. and Arundo donax L. Bioenerg Res 8(4):1500–1511

    Article  CAS  Google Scholar 

  • Bouyoucos CJ (1962) Hydrometer method improved for making particle size analyses of soils 1. Agron J 54(5):464–465

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  CAS  PubMed  Google Scholar 

  • Bradley R, Burt AJ, Read DJ (1982) The biology of mycorrhiza in the Ericaceae. New Phytol 91(2):197–209

    Article  CAS  Google Scholar 

  • Cabral L, Soares CRFS, Giachini AJ, Siqueira JO (2015) Arbuscular mycorrhizal fungi in phytoremediation of contaminated areas by trace elements: mechanisms and major benefits of their applications. World J Microbiol Biotechnol 31:1655–1664

    Article  CAS  PubMed  Google Scholar 

  • Chang ZM, Wu XH (2005) Difference comparison of three alfalfa varieties resistant to cadmium pollution. Prata Cult Sci 22(12):20–23

    Google Scholar 

  • Chen B, Shen H, Li X, Feng G, Christie P (2004) Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc. Plant Soil 261(1–2):219–229

    Article  CAS  Google Scholar 

  • Chen X, Wu C, Tang J, Hu S (2005) Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment. Chemosphere 60(5):665–671

    Article  CAS  PubMed  Google Scholar 

  • Chen YM, Wang MK, Huang PM (2006) Catechin transformation as influenced by aluminum. J Agric Food Chem 54(1):212–218

    Article  CAS  PubMed  Google Scholar 

  • 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 μX-ray fluorescence analysis. Microbes Environ 33(3):257–263

    Article  PubMed  PubMed Central  Google Scholar 

  • Chibuike GU, Obiora SC (2014) Heavy metal polluted soils: effect on plants and bioremediation methods. Applied and Environmental Soil Science. Review Article (12 pages) Article ID 752708

  • 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 Soil 261(1–2):209–217

    Article  CAS  Google Scholar 

  • Cornejo P, Meier S, Borie G, Rillig MC, Borie F (2008) Glomalin-related soil protein in a Mediterranean ecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration. Sci Total Environ 406(1–2):154–160

    Article  CAS  PubMed  Google Scholar 

  • Cottenie A (1980) Soil and plant testing as a basis of fertilizer recommendations FAO. Soil’s Bulletin 38:64–65

  • De Andrade SA, da Silveira AP (2008) Mycorrhiza influence on maize development under Cd stress and P supply. Braz J Plant Physiol 20(1):39–50

    Article  Google Scholar 

  • de Fátima PD, Barbosa MV, dos Santos JV, Pinto FA, Siqueira JO, Carneiro MAC (2018) Arbuscular mycorrhizal fungi favor the initial growth of Acacia mangium, Sorghum bicolor, and Urochloa brizantha in soil contaminated with Zn, Cu, Pb, and Cd. Bull Environ Contam Toxicol 101(3):386–391

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PT, dSmith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356

    Article  CAS  Google Scholar 

  • Feddermann N, Finlay R, Boller T, Elfstrand M (2010) Functional diversity in arbuscular mycorrhiza–the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecol 3(1):1–8

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Current Science 528-534

  • Gonzalez-Chavez MC, Carrillo-Gonzalez R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130(3):317–323

    Article  CAS  PubMed  Google Scholar 

  • González-Guerrero M, Azcón-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42(2):130–140

    Article  CAS  PubMed  Google Scholar 

  • Grace C, Stribley DP (1991) A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol Res 95(10):1160–1162

    Article  Google Scholar 

  • Grant CA (2011) Influence of phosphate fertilizer on cadmium in agricultural soils and crops. Agric Agri Food Canada 54:143–155

    CAS  Google Scholar 

  • Gu HH, Zhou Z, Gao YQ, Yuan XT, Ai YJ, Zhang JY, Li FP (2017) The influences of arbuscular mycorrhizal fungus on phytostabilization of lead/zinc tailings using four plant species. Int J Phytoremediation 19(8):739–745

    Article  CAS  PubMed  Google Scholar 

  • Gupta PK (2007) Soil, plant, water and fertilizer analysis. 2thd ed. Agrobios (India), Jodhpur 36:3119–3121

  • Hallett PD, Feeney DS, Bengough AG, Rillig MC, Scrimgeour CM, Young IM (2009) Disentangling the impact of AM fungi versus roots on soil structure and water transport. Plant Soil 314(1–2):183–196

    Article  CAS  Google Scholar 

  • Hancock LM, Ernst CL, Charneskie R, Ruane LG (2012) Effects of cadmium and mycorrhizal fungi on growth, fitness, and cadmium accumulation in flax (Linum usitatissimum; Linaceae). Am J Bot 99:1445–1452

    Article  PubMed  Google Scholar 

  • Hooker JE, Piatti P, Cheshire MV, Watson CA (2007) Polysaccharides and monosaccharides in the hyphosphere of the arbuscular mycorrhizal fungi Glomus E3 and Glomus tenue. Soil Biol Biochem 39(2):680–683

    Article  CAS  Google Scholar 

  • Hu J, Wu F, Wu S, Lam CL, Lin X, Wong MH (2014) Biochar and Glomus caledonium influence Cd accumulation of upland kangkong (Ipomoea aquatica Forsk.) intercropped with Alfred stonecrop Sedum alfredii Hance. Sci Rep 4:46–71

    Google Scholar 

  • Huang W (1994) The syntheses and chelating ability of water-soluble polymer (master's thesis). School of Graduate Studies Laurentian University, Sudbury

    Google Scholar 

  • Jackson ML (1958) Soil chemical analysis. Prentice-Hall Inc, Englewood Cliffs, p 498

    Google Scholar 

  • Jansa J, Finlay R, Wallander H, Smith FA, Smith SE (2011) Role of mycorrhizal symbioses in phosphorus cycling. In: Bunemann EK, Oberson A, Frossard E (eds) Phosphorus in action. Biological processes in soil phosphorus cycling. Soil biology, vol 26. Springer, Heidelberg. https://doi.org/10.1007/978-3-642-15271-9_6

  • Jiang L, Yang Y, Xu WH, Wang CL, Chen R, Xiong SJ, Xie DT (2014) Effects of ryegrass and arbuscular mycorrhiza on activities of antioxidant enzymes, accumulation and chemical forms of cadmium in different varieties of tomato. Huan Jing Ke Xue 35(6):2349–2357

    CAS  PubMed  Google Scholar 

  • Joner E, Leyval C (2001) Time-course of heavy metal uptake in maize and clover as affected by root density and different mycorrhizal inoculation regimes. Biol Fertil Soils 33(5):351–357

    Article  CAS  Google Scholar 

  • Kabata-Pendias A (2010) Trace elements in soils and plants, 4th edn. CRC Press, Boca Raton, p 548

    Book  Google Scholar 

  • Kapoor A, Viraraghavan T (1995) Fungal biosorption—an alternative treatment option for heavy metal bearing wastewaters: a review. Bioresour Technol 53(3):195–206

    CAS  Google Scholar 

  • Kapoor R, Chaudhary V, Bhatnagar AK (2007) Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza 17(7):581–587

    Article  CAS  PubMed  Google Scholar 

  • Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41(1–2):197–207

    Article  CAS  PubMed  Google Scholar 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84(9):2292–2301

    Article  Google Scholar 

  • Liao JP, Lin XG, Cao ZH, Shi YQ, Wong MH (2003) Interactions between arbuscular mycorrhizae and heavy metals under sand culture experiment. Chemosphere 50(6):847–853

    Article  CAS  PubMed  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper 1. Soil Sci Soc Am J 42(3):421–428

    Article  CAS  Google Scholar 

  • Liu Z, He X, Chen W, Yuan F, Yan K, Tao D (2009) Accumulation and tolerance characteristics of cadmium in a potential hyperaccumulator—Lonicera japonica Thunb. J Hazard Mater 169(1–3):170–175

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Zhang Q, Hu L, Tang J, Xu L, Yang X, Chen X (2012) Legumes can increase cadmium contamination in neighboring crops. PLoS One 7(8):e42944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorenz N, Hintemann T, Kramarewa T, Katayama A, Yasuta T, Marschner P, Kandeler E (2006) Response of microbial activity and microbial community composition in soils to long-term arsenic and cadmium exposure. Soil Biol Biochem 386:1430–1437

    Article  CAS  Google Scholar 

  • Mechri B, Manga AG, Tekaya M, Attia F, Cheheb H, Meriem FB, Hammami M (2014) Changes in microbial communities and carbohydrate profiles induced by the mycorrhizal fungus (Glomus intraradices) in rhizosphere of olive trees (Olea europaea L.). Appl Soil Ecol 75:124–133

    Article  Google Scholar 

  • Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132(1):272–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molina M, Escudey M, Chang AC, Chen WP, Arancibia-Miranda N (2013) Trace element uptake dynamics for maize (Zea mays L.) grown under field;conditions. Plant Soil 370:471e483

    Article  CAS  Google Scholar 

  • Ogar A, Sobczyk Ł, Turnau K (2015) Effect of combined microbes on plant tolerance to Zn–Pb contaminations. Environ Sci Pollut Res 22(23):19142–19156

    Article  CAS  Google Scholar 

  • Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department of Agriculture, Washington

    Google Scholar 

  • Orłowska E, Godzik B, Turnau K (2012) Effect of different arbuscular mycorrhizal fungal isolates on growth and arsenic accumulation in Plantago lanceolate L. Environ Poll 168:121–130

    Article  CAS  Google Scholar 

  • Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52(3):199–223

    Article  CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55(1):158–161

    Article  Google Scholar 

  • Pietrini F, Iori V, Bianconi D, Mughini G, Massacci A, Zacchini M (2015) Assessment of physiological and biochemical responses, metal tolerance and accumulation in two eucalypt hybrid clones for phytoremediation of cadmium-contaminated waters. J Environ Manag 162:221–231

    Article  CAS  Google Scholar 

  • Pinel F, Leclerc-Cessac E, Staunton S (2003) Relative contributions of soil chemistry, plant physiology and rhizosphere induced changes in speciation on Ni accumulation in plant shoots. Plant Soil 255:619–629

    Article  CAS  Google Scholar 

  • Rajkumar M, Sandhya S, Prasad MN, Freitas H (2012) Perspectives of plant associated microbes in heavy metal phytoremediation. Biotechnol Adv 30(60):1562–1574

    Article  CAS  PubMed  Google Scholar 

  • Rillig MC, Wright SF, Torn MS (2001) Unusually large contribution of arbuscular mycorrhizal fungi to soil organic matter pools in tropical forest soils. Plant Soil 233:167–177

    Article  CAS  Google Scholar 

  • Rillig MC, Caldwell BA, Wösten HA, Sollins P (2007) Role of proteins in soil carbon and nitrogen storage: controls on persistence. Biogeochemistry 85(1):25–44

    Article  CAS  Google Scholar 

  • Rillig MC, Mardatin NF, Leifheit EF, Antunes PM (2010) Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates. Soil Biol Biochem 42(7):1189–1191

    Article  CAS  Google Scholar 

  • Rishcefid M, Aliasgharzad N, Neyshabouri M (2017) Effects of water deficit stress on glomalin secretion by glomerales in symbiosis with Zea mays plant. J Water Soil Sci 21(1):229–238

    Article  Google Scholar 

  • Rivera-Becerril F, Calantzis C, Turnau K, Caussanel JP, Belimov AA, Gianinazzi S, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53(371):1177–1185

    Article  CAS  PubMed  Google Scholar 

  • Sarsar V, Hardeep H, Selwal KK, Tanwar RS, Pankaj K, Tyagi PK, Anami Ahuja A (2012) Indian mustard Brassica juncea L. mediated phytoremediation of Lead. Int J Appl Biol Pharm Technol 3(4):1–5

    Google Scholar 

  • Shah K, Mankad AU, Reddy MN (2017) Cadmium accumulation and its effects on growth and biochemical parameters in Tagetes erecta L. J Pharmacogn Phytochem 6:111–115

    CAS  Google Scholar 

  • Shahabivand S, Maivan HZ, Goltapeh EM, Sharifi M, Aliloo AA (2012) The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Biochem 60:53–58

    Article  CAS  PubMed  Google Scholar 

  • Sharma S, Anand G, Singh N, Kapoor R (2017) Arbuscular mycorrhiza augments arsenic tolerance in wheat (Triticum aestivum L.) by strengthening antioxidant defense system and thiol metabolism. Frontiers in plant science 8, 906

  • Song H (2005) Effects of VAM on host plant in the condition of drought stress and its mechanisms. Electron J Biology 1(3):44–48

    Google Scholar 

  • Sparling GP, West AW, Whale KN (1985) Interference from plant roots in the estimation of soil microbial ATP, C, N and P. Soil Biol Biochem 17(3):275–278

    Article  CAS  Google Scholar 

  • Sposito GL, Lund J, Chang AC (1982) Trace metal chemistry in arid-zone field soils amended with sewage sludge: I. fractionation of Ni, Cu, Zn, Cd, and Pb in solid phases. Soil Sci Soc Am J 46:260–265

    Article  CAS  Google Scholar 

  • Sun YB, Zhou QX, Wang L, Liu W (2009) Cadmium tolerance and accumulation characteristics of Bidenspilosa L. as a potential Cd-hyperaccumulator. J Hazard Mater 161:808–814

    Article  CAS  PubMed  Google Scholar 

  • Taghavi M, Alizadeh R, Ghaemy M (2015) Preparation and properties of magnetic Fe3O4/poly (pyrimidine-amide) nanocomposites: selective polyamidation of a bis (amino-pyrimidine-diol) compound in an ionic liquid. RSC Adv 5(13):9581–9590

    Article  CAS  Google Scholar 

  • Thomas GW (1982) Exchangeable cations. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2, chemical and microbiological properties. ASA and SSSA, Madison, pp 159–165

    Google Scholar 

  • Waldrip HM, He Z, Erich MS (2011) Effects of poultry manure amendment on phosphorus uptake by ryegrass, soil phosphorus fractions and phosphatase activity. Biol Fertil Soils 47(4):407–418

    Article  Google Scholar 

  • Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37(1):29–38

    Article  CAS  Google Scholar 

  • Wang Z, Shan XQ, Zhang S (2002) Comparison between fractionation and bioavailability of trace elements in rhizosphere and bulk soils. Chemosphere 46(8):1163–1171

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Su MY, Chen YH, Lin FF, Luo D, Gao SF (2006) Transfer characteristics of cadmium and lead from soil to the edible parts of six vegetable species in southeastern China. Environ Pollut 144(1):127–135

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Yao J, Si Y, Chen H, Russel M, Chen K, Bramanti E (2010) Short-time effect of heavy metals upon microbial community activity. J Hazard Mater 173(1–3):510–516

    Article  CAS  PubMed  Google Scholar 

  • Wang FY, Shi ZY, Xu XF, Wang XG, Li YJ (2013) Contribution of AM inoculation and cattle manure to lead and cadmium phytoremediation by tobacco plants. Environ Sci Proc Impacts 15(4):794–801

    Article  CAS  Google Scholar 

  • Wang FY, Liu XQ, Shi ZY, Tong RJ, Adams CA, Shi XJ (2016) Arbuscular mycorrhizae alleviate negative effects of zinc oxide nanoparticle and zinc accumulation in maize plants-a soil microcosm experiment. Chemosphere 147:88–97

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Ji B, Hu Y, Liu R, Sun W (2017a) A review on in situ phytoremediation of mine tailings. Chemosphere 184:594–600

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Shi J, Xie Q, Jiang Y, Yu N, Wang E (2017b) Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol Plant 10(9):1147–1158

    Article  CAS  PubMed  Google Scholar 

  • Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci 161(9):575–586

    Article  CAS  Google Scholar 

  • Wu QT, Xu Z, Meng Q, Gerard E, Morel JL (2004) Characterization of cadmium desorption in soils and its relationship to plant uptake and cadmium leaching. Plant Soil 258(1):217–226

    Article  CAS  Google Scholar 

  • Wu QS, He XH, Zou YN, He KP, Sun YH, Cao MQ (2012) Spatial distribution of glomalin-related soil protein and its relationships with root mycorrhization, soil aggregates, carbohydrates, activity of protease and β-glucosidase in the rhizosphere of Citrus unshiu. Soil Biol Biochem 45:181–183

    Article  CAS  Google Scholar 

  • Wuana RA, Okieimen FE, Imborvungu JA (2010) Removal of heavy metals from a contaminated soil using organic chelating acids. Int J Environ Sci Tech 7(3):485–496

    Article  CAS  Google Scholar 

  • Xing BS, Liu JD, Liu XB, Han XZ (2005) Extraction and characterization of humic acids and humin fractions from a black soil of China. Pedosphere 15(1):1–8

    CAS  Google Scholar 

  • Xue ZC, Gao HY, Zhang LT (2013) Effects of cadmium on growth, photosynthetic rate and chlorophyll content in leaves of soybean seedlings. Biol Plant 57(3):587–590

    Article  CAS  Google Scholar 

  • 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(12):e0145726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, He C, Huang L, Ban Y, Tang M (2017) The effects of arbuscular mycorrhizal fungi on glomalin-related soil protein distribution, aggregate stability and their relationships with soil properties at different soil depths in lead-zinc contaminated area. PLoS One 12(8):e0182264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yi YJ, Yang ZF, Zhang SH (2011) Ecological risk assessment of heavy metals in sediment and human health risk assessment of heavy metals in fishes in the middle and lower reaches of the Yangtze River basin. Environ Pollut 159(10):2575–2585

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Wang LH, Yang JC, Liu H, Dai JL (2015) Health risk to residents and stimulation to inherent bacteria of various heavy metals in soil. Sci Total Environ 508:29–36

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Nie S, Liang J, Zeng G, Wu H, Hua S, Xiang H (2016) Effects of heavy metals and soil physicochemical properties on wetland soil microbial biomass and bacterial community structure. Sci Total Environ 557:785–790

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Liu M, Li Y, Che Y, Xiao Y (2018) Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa. Sci Total Environ 655:1150–1158

    Article  CAS  PubMed  Google Scholar 

  • Zhong WL, Li JT, Chen YT, Shu WS, Liao B (2012) A study on the effects of lead, cadmium and phosphorus on the lead and cadmium uptake efficacy of Viola baoshanensis inoculated with Arbuscular mycorrhizal fungi. J Environ Monit 14(9):2497–2504

    Article  CAS  PubMed  Google Scholar 

  • Zhou QX, Song YF (2004) Principles and methods of contaminated soil remediation. China Environmental Science Press, Beijing

    Google Scholar 

  • Zhuang P, Shu W, Li Z, Liao B, Li J, Shao J (2009) Removal of metals by sorghum plants from contaminated land. J Environ Sci 21(10):1432–1437

    Article  CAS  Google Scholar 

Download references

Funding

Shahid Chamran University of Ahvaz, Iran, funded this work (AG1397-Grant_Faculty of Agriculture).

Author information

Authors and Affiliations

  1. Department of Soil Science, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran

    Milad Babadi & Roya Zalaghi

  2. Department of Chemistry, Faculty of Science, Shahid Chamran University of Ahvaz, Ahvaz, Iran

    Mehdi Taghavi

Authors
  1. Milad Babadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roya Zalaghi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mehdi Taghavi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roya Zalaghi.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Babadi, M., Zalaghi, R. & Taghavi, M. A non-toxic polymer enhances sorghum-mycorrhiza symbiosis for bioremediation of Cd. Mycorrhiza 29, 375–387 (2019). https://doi.org/10.1007/s00572-019-00902-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-019-00902-5

Keywords

Search

Navigation