Skip to main content
Log in

Heavy metal domestication enhances beneficial effects of arbuscular mycorrhizal fungi on lead (Pb) phytoremediation efficiency of Bidens parviflora through improving plant growth and root Pb accumulation

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Native arbuscular mycorrhizal fungi (AMF) generally provide more effective assistance for phytoremediation to remove heavy metal (HM) from polluted soils than non-native AMF. Nevertheless, it is a time-consuming work to isolate, identify, and propagate AMF inoculum for practical application. This study aims to explore an alternative method to improve the phytoremediation efficiency of Bidens parviflora using domesticated AMF under HM stress condition for a certain period of time. Our results showed that Funneliformis mosseae inoculation alleviated oxidative damage to plant membranes by enhancing activities of superoxide dismutase, catalase, ascorbate peroxidase, and glutathione reductase. Furthermore, mycorrhizal plants had higher chlorophyll concentration, photosynthesis efficiency, and root Pb content to protect the aerial parts from damage. These protective mechanisms were found to be more efficient in domesticated AMF inoculation compared with non-domesticated AMF inoculation. Overall, this study suggests that F. mosseae domesticated for 12 months could greatly enhance plant root Pb accumulation and plant growth mainly through strengthening antioxidant defenses as well as the photosynthesis efficiency under Pb stress conditions. Plants inoculated with pre-domesticated AMF provided a promising new strategy to enhance phytoremediation of Pb-contaminated soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Adeyemi NO, Atayese MO, Sakariyawo OS, Azeez JO, Ridwan M (2021) Arbuscular mycorrhizal fungi species differentially regulate plant growth, phosphorus uptake and stress tolerance of soybean in lead contaminated soil. J Plant Nutr 44:1633–1648

    CAS  Google Scholar 

  • Aebi H (1984) Catalase in Vitro. Method Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Baker AJ (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Baker AJ, Brooks R (1989) Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery 1(2):81–126

    CAS  Google Scholar 

  • Bhantana P, Rana MS, Sun XC, Moussa MG, Saleem MH, Syaifudin M, Shah A, Poudel A, Pun AB, Bhat MA, Mandal DL (2021) Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and phytoremediation. Symbiosis 84:19–37

    Article  CAS  Google Scholar 

  • Biermann B, Linderman RG (1981) Quantifying vesicular-arbuscular mycorrhizae: a proposed method towards standardization. New Phytol 87:63–67

    Article  Google Scholar 

  • Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6:e04691

    Article  Google Scholar 

  • Chandrasekaran M, Chanratana M, Kim K, Seshadri S, Sa T (2019) Impact of arbuscular mycorrhizal fungi on photosynthesis, water status, and gas exchange of plants under salt stress-a meta-analysis. Front Plant Sci 10:457

    Article  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Env Sci-Switz 2:53

    Google Scholar 

  • Deng H, Ye ZH, Wong MH (2004) Accumulation of lead, zinc, copper and cadmium by 12 wetland plant species thriving in metal-contaminated sites in China. Environ Pollut 132:29–40

    Article  CAS  Google Scholar 

  • Deng Q, Deng Q, Wang Y, Li L, Long X, Ren S, Fan Y, Lin L, Xia H, Liang D, Wang J (2019) Effects of intercropping with Bidens species plants on the growth and cadmium accumulation of Ziziphus acidojujuba seedlings. Environ Monit Assess 191:1–8

    Article  CAS  Google Scholar 

  • Ezawa T, Smith SE, Smith FA (2002) P metabolism and transport in AM fungi. Plant Soil 244:221–230

    Article  CAS  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  CAS  Google Scholar 

  • Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244

    Article  Google Scholar 

  • Global No. 1 Business Data Platform. Available online: https://www.statista.com/statistics/273652/global-lead-reserves-by-selected-countries (Accessed on 24 November 2021)

  • Hansen MH, Li H, Svarverud R (2018) Ecological civilization: interpreting the Chinese past, projecting the global future. Global Environ Chang 53:195–203

    Article  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Huang L, Chen D, Zhang H, Song Y, Chen H, Tang M (2019) Funneliformis mosseae enhances root development and Pb phytostabilization in Robinia pseudoacacia in Pb-contaminated soil. Front Microbiol 10:2591

    Article  Google Scholar 

  • Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 124:61–68

    Google Scholar 

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

    Article  Google Scholar 

  • Lajayer BA, Moghadam NK, Maghsoodi MR, Ghorbanpour M, Kariman K (2019) Phytoextraction of heavy metals from contaminated soil, water and atmosphere using ornamental plants: mechanisms and efficiency improvement strategies. Environ Sci Pollut Res 26:8468–8484

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids-measurement and characterisation by UV-VIS. Current Protocols in Food Analytical Chemistry (CPFA), (Supplement 1), F4.3.1-F4.3.8. John Wiley, New York

  • López-Maury L, Marguerat S, Bähler J (2008) Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 9(8):583–593

    Article  CAS  Google Scholar 

  • Mahama GY, Prasad PV, Roozeboom KL, Nippert JB, Rice CW (2016) Response of maize to cover crops, fertilizer nitrogen rates, and economic return. AGRON J 108:17–31

    Article  CAS  Google Scholar 

  • Malekzadeh E, Aliasgharzad N, Majidi J, Abdolalizadeh J, Aghebati-Maleki L (2016) Contribution of glomalin to Pb sequestration by arbuscular mycorrhizal fungus in a sand culture system with clover plant. Eur J Soil Biol 74:45–51

    Article  CAS  Google Scholar 

  • Marques AP, Rangel AO, Castro PM (2009) Remediation of heavy metal contaminated soils: phytoremediation as a potentially promising clean-up technology. Crit Rev Environ Sci Technol 39:622–654

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Orłowska E, Ryszka P, Jurkiewicz A, Turnau K (2005) Effectiveness of arbuscular mycorrhizal fungal (AMF) strains in colonisation of plants involved in phytostabilisation of zinc wastes. Geoderma 129(1–2):92–98

    Article  CAS  Google Scholar 

  • Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492

    Article  CAS  Google Scholar 

  • Pellegrino E, Bedini S, Avio L, Bonari E, Giovannetti M (2011) Field inoculation effectiveness of native and exotic arbuscular mycorrhizal fungi in a Mediterranean agricultural soil. Soil Biol Biochem 43:367–376

    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. T Brit Mycol Soc 55:158–161

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Raskin I, Smith RD, Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8:221–226

    Article  CAS  Google Scholar 

  • Riaz M, Kamran M, Fang Y, Wang Q, Cao H, Yang G, Deng Lu, Wang Y, Zhou Y, Anastopoulos I, Wang X (2020) Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: a critical review. J Hazard Mater 402:123919

    Article  CAS  Google Scholar 

  • Salazar MJ, Menoyo E, Faggioli V, Geml J, Cabello M, Rodriguez JH, Marro N, Pardo A, Pignata ML, Becerra AG (2018) Pb accumulation in spores of arbuscular mycorrhizal fungi. Sci Total Environ 643:238–246

    Article  CAS  Google Scholar 

  • Salt DE, Blaylock M, Kumar NP, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474

    CAS  Google Scholar 

  • Sharma S, Rana S, Thakkar A, Baldi A, Murthy RSR, Sharma RK (2016) Physical, chemical and phytoremediation technique for removal of heavy metals. J Heavy Metal Toxicol Dis 1:1–15

    Google Scholar 

  • Smimoff N (1995) Antioxidant systems and plant response to the environment; in Environment and Plant Metabolism. Bios Scientific Publishers, Oxford

    Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, New York, NY

    Google Scholar 

  • Stoltz E, Greger M (2002) Accumulation properties of As, Cd, Cu, Pb and Zn by four wetland plant species growing on submerged mine tailings. Environ Exp Bot 47:271–280

    Article  CAS  Google Scholar 

  • Sun XM, Ren LJ, Zhao QY, Ji XJ, Huang H (2018) Microalgae for the production of lipid and carotenoids: a review with focus on stress regulation and adaptation. Biotechnol Biofuels 11(1):1–16

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vivas A, Vörös A, Biró B, Barea JM, Ruiz-Lozano JM, Azcón R (2003) Beneficial effects of indigenous Cd-tolerant and Cd-sensitive Glomus mosseae associated with a Cd-adapted strain of Brevibacillus sp. in improving plant tolerance to Cd contamination. Appl Soil Ecol 24:177–186

    Article  Google Scholar 

  • Vogel-Mikuš K, Pongrac P, Kump P, Nečemer M, Regvar M (2006) Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal fungal mixture induces changes in heavy metal and nutrient uptake. Environ Pollut 139(2):362–371

    Article  CAS  Google Scholar 

  • Yang Y, Cao Y, Li Z, Zhukova A, Yang S, Wang J, Tang Z, Cao Y, Zhang Y, Wang D (2020) Interactive effects of exogenous melatonin and Rhizophagus intraradices on saline-alkaline stress tolerance in Leymus chinensis. Mycorrhiza 30:357–371

    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:e0145726

    Article  CAS  Google Scholar 

  • Yang Y, Liang Y, Han X, Chiu TY, Ghosh A, Chen H, Tang M (2016) The roles of arbuscular mycorrhizal fungi (AMF) in phytoremediation and tree-herb interactions in Pb contaminated soil. SCI REP-UK 6:1–14

    CAS  Google Scholar 

  • Yang Y, Song Y, Scheller HV, Ghosh A, Ban Y, Chen H, Tang M (2015b) Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol Biochem 86:146–158

    Article  CAS  Google Scholar 

  • Yang Y, Tang M, Sulpice R, Chen H, Tian S, Ban Y (2014) Arbuscular mycorrhizal fungi alter fractal dimension characteristics of Robinia pseudoacacia L. seedlings through regulating plant growth, leaf water status, photosynthesis, and nutrient concentration under drought stress. J Plant Growth Regul 33:612–625

    Article  CAS  Google Scholar 

  • Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368(2–3):456–464

    Article  CAS  Google Scholar 

  • Yousuf PY, Hakeem KUR, Chandna R, Ahmad P (2012) Role of glutathione reductase in plant abiotic stress. In Abiotic stress responses in plants (pp. 149-158). Springer, New York, NY

  • Zhan F, Li B, Jiang M, Yue X, He Y, Xia Y, Wang Y (2018) Arbuscular mycorrhizal fungi enhance antioxidant defense in the leaves and the retention of heavy metals in the roots of maize. Environ Sci Pollut Res 25:24338–24347

    Article  CAS  Google Scholar 

  • Zhang HH, Tang M, Chen H, Zheng CL, Niu ZC (2010) Effect of inoculation with AM fungi on lead uptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasing lead concentrations. Eur J Soil Biol 46:306–311

    Article  Google Scholar 

Download references

Funding

This research was supported by the National Natural Science Foundation of China (41807052) and the Program of Introducing Talents of Discipline to Universities (B16011).

Author information

Authors and Affiliations

Authors

Contributions

YY and XW designed and conceived the experiment. YY, BH, and JX carried out the experiments and collected the empirical data. ZT and ZL performed the data analysis. YY and XW wrote the paper with contributions from ZT and ZL.

Corresponding author

Correspondence to Xuefeng Wu.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible editor: Elena Maestri

Publisher's note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 521 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Huang, B., Xu, J. et al. Heavy metal domestication enhances beneficial effects of arbuscular mycorrhizal fungi on lead (Pb) phytoremediation efficiency of Bidens parviflora through improving plant growth and root Pb accumulation. Environ Sci Pollut Res 29, 32988–33001 (2022). https://doi.org/10.1007/s11356-022-18588-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-18588-2

Keywords

Navigation