Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Arbuscular mycorrhizal fungi enhance antioxidant defense in the leaves and the retention of heavy metals in the roots of maize

Abstract

In this study, we investigated the effects of the arbuscular mycorrhizal fungi (AMF) Funneliformis mosseae and Diversispora spurcum on the growth, antioxidant physiology, and uptake of phosphorus (P), sulfur (S), lead (Pb), zinc (Zn), cadmium (Cd), and arsenic (As) by maize (Zea mays L.) grown in heavy metal-polluted soils though a potted plant experiment. F. mosseae significantly increased the plant chlorophyll a content, height, and biomass; decreased the H2O2 and malondialdehyde (MDA) contents; and enhanced the superoxide dismutase (SOD) and catalase (CAT) activities and the total antioxidant capacity (T-AOC) in maize leaves; this effect was not observed with D. spurcum. Both F. mosseae and D. spurcum promoted the retention of heavy metals in roots and increased the uptake of Pb, Zn, Cd, and As, and both fungi restricted heavy metal transfer, resulting in decreased Pb, Zn, and Cd contents in shoots. Therefore, the fungi reduced the translocation factors for heavy metal content (TF) and uptake (TF′) in maize. Additionally, F. mosseae promoted P and S uptake by shoots, and D. spurcum increased P and S uptake by roots. Moreover, highly significant negative correlations were found between antioxidant capacity and the H2O2, MDA, and heavy metal contents, and there was a positive correlation with the biomass of maize leaves. These results suggested that AMF alleviated plant toxicity and that this effect was closely related to antioxidant activation in the maize leaves and increased retention of heavy metals in the roots.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

  2. Aghababaei F, Raiesi F, Hosseinpur A (2014a) The influence of earthworm and mycorrhizal co-inoculation on Cd speciation in a contaminated soil. Soil Biol Biochem 78:21–29

  3. Aghababaei F, Raiesi F, Hosseinpur A (2014b) The combined effects of earthworms and arbuscular mycorrhizal fungi on microbial biomass and enzyme activities in a calcareous soil spiked with cadmium. Appl Soil Ecol 75:33–42

  4. Bao S (2000) Soil and agricultural chemistry analysis, 3rd edn. China Agriculture Press, Beijing

  5. Baum C, Hrynkiewicz K, Leinweber P, Meißner R (2006) Heavy-metal mobilization and uptake by mycorrhizal and nonmycorrhizal willows (Salix × dasyclados). J Plant Nutr Soil Sci 169:516–522

  6. Behie SW, Bidochka MJ (2014) Nutrient transfer in plant-fungal symbioses. Trends Plant Sci 19:734–740

  7. Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76

  8. Berch SM, Kendrick B (1982) Vesicular-arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74:769–776

  9. Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol 59:411–416

  10. Burghelea C, Zaharescu DG, Dontsova K, Maier R, Huxman T, Chorover J (2015) Mineral nutrient mobilization by plants from rock: influence of rock type and arbuscular mycorrhiza. Biogeochemistry 124:187–203

  11. Chen L, Zhang D, Yang W, Liu Y, Zhang L, Gao S (2016) Sex-specific responses of Populus deltoides to Glomus intraradices colonization and Cd pollution. Chemosphere 155:196–206

  12. Cornejo P, Pérez-Tienda J, Meier S, Valderas A, Borie F, Azcón-Aguilar C, Ferrol N (2013) Copper compartmentalization in spores as a survival strategy of arbuscular mycorrhizal fungi in Cu-polluted environments. Soil Biol Biochem 57:925–928

  13. Degola F, Fattorini L, Bona E, Sprimuto CT, Argese E, Berta G, di Toppi LS (2015) The symbiosis between Nicotiana tabacum and the endomycorrhizal fungus Funneliformis mosseae increases the plant glutathione level and decreases leaf cadmium and root arsenic contents. Plant Physiol Biochem 92:11–18

  14. Dietterich LH, Gonneau C, Casper BB (2017) Arbuscular mycorrhizal colonization has little consequence for plant heavy metal uptake in contaminated field soils. Ecol Appl 27:1862–1875. https://doi.org/10.1002/eap.1573

  15. Doubková P, Sudová R (2016) Limited impact of arbuscular mycorrhizal fungi on clones of Agrostis capillaris with different heavy metal tolerance. Appl Soil Ecol 99:78–88

  16. Ferrol N, González-Guerrero M, Valderas A, Benabdellah K, Azcón-Aguilar C (2009) Survival strategies of arbuscular mycorrhizal fungi in Cu-polluted environments. Phytochem Rev 8:551–559

  17. Ferrol N, Tamayo E, Vargas P (2016) The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications. J Exp Bot 67:6253–6265

  18. Garg N, Aggarwal N (2012) Effect of mycorrhizal inoculations on heavy metal uptake and stress alleviation of Cajanus cajan (L.) Millsp. genotypes grown in cadmium and lead contaminated soils. Plant Growth Regul 66:9–26

  19. Garg N, Kaur H (2013) Response of antioxidant enzymes, phytochelatins and glutathione production towards Cd and Zn stresses in Cajanus cajan (L.) Millsp. genotypes colonized by arbuscular mycorrhizal fungi. J Agron Crop Sci 199:118–133

  20. Giller KE, Witter E, McGrath SP (2009) Heavy metals and soil microbes. Soil Biol Biochem 41:2031–2037

  21. Giovannetti M, Tolosano M, Volpe V, Kopriva S, Bonfante P (2014) Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol 204:609–619

  22. Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122

  23. Gomes MP, Andrade ML, Nascentes CC, Scotti MR (2014) Arsenic root sequestration by a tropical woody legume as affected by arbuscular mycorrhizal fungi and organic matter: implications for land reclamation. Water Air Soil Pollut 225:1919

  24. Gu H, Zhou Z, Gao Y, Yuan X, Ai Y, Zhang J, Zu W, Taylor AA, Nan S, Li F (2017) The influences of arbuscular mycorrhizal fungus on phytostabilization of lead/zinc tailings using four plant species. Int J Phytoremediation 19:739–745

  25. Hassan SE, Hijri M, St-Arnaud M (2013) Effect of arbuscular mycorrhizal fungi on trace metal uptake by sunflower plants grown on cadmium contaminated soil. New Biotechnol 30:780–787

  26. Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3:267–273

  27. Hu J, Wang H, Wu F, Wu S, Cao Z, Lin X, Wong MH (2014) Arbuscular mycorrhizal fungi influence the accumulation and partitioning of Cd and P in bashfulgrass (Mimosa pudica L.) grown on a moderately Cd-contaminated soil. Appl Soil Ecol 73:51–57

  28. Huang Y, Tao S, Chen Y (2005) The role of arbuscular mycorrhiza on change of heavy metal speciation in rhizosphere of maize in wastewater irrigated agriculture soil. J Environ Sci 17:276–280

  29. Huang X, Ho S, Zhu S, Ma F, Wu J, Yang J, Wang L (2017) Adaptive response of arbuscular mycorrhizal symbiosis to accumulation of elements and translocation in Phragmites australis affected by cadmium stress. J Environ Manag 197:448–455

  30. Janero DR (1990) Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 9:515–540

  31. Janouskova M, Pavlikova D (2010) Cadmium immobilization in the rhizosphere of arbuscular mycorrhizal plants by the fungal extraradical mycelium. Plant Soil 332:511–520

  32. Jiang Q, Tan S, Zhuo F, Yang D, Ye Z, Jing Y (2016a) Effect of Funneliformis mosseae on the growth, cadmium accumulation and antioxidant activities of Solanum nigrum. Appl Soil Ecol 98:112–120

  33. Jiang Q, Zhuo F, Long S, Zhao H, Yang D, Ye Z, Li S, Jing Y (2016b) Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Sci Rep 6:21805

  34. Joner EJ, Leyval C (1997) Uptake of 109Cd by roots and hyphae of a Glomus mosseae/Trifolium subterraneum mycorrhiza from soil amended with high and low concentrations of cadmium. New Phytol 135:353–360

  35. Leung HM, Wang ZW, Ye ZH, Yung KL, Peng XL, Cheung KC (2013) Interactions between arbuscular mycorrhizae and plants in phytoremediation of metal-contaminated soils: a review. Pedosphere 23:549–563

  36. Li Z, Ma Z, van der Kuijp TJ, Yuan Z, Huang L (2014) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ 468:843–853

  37. Lichtenthaler H (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

  38. Liu H, Yuan M, Tan S, Yang X, Lan Z, Jiang Q, Ye Z, Jing Y (2015) Enhancement of arbuscular mycorrhizal fungus (Glomus versiforme) on the growth and Cd uptake by Cd-hyperaccumulator Solanum nigrum. Appl Soil Ecol 89:44–49

  39. McCord JM, Fridovich I (1969) Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

  40. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

  41. Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569

  42. Na G, Salt DE (2011) The role of sulfur assimilation and sulfur-containing compounds in trace element homeostasis in plants. Environ Exp Bot 72:18–25

  43. 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 Environ 29:60–66

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

  45. Redon P, Béguiristain T, Leyval C (2009) Differential effects of AM fungal isolates on Medicago truncatula growth and metal uptake in a multimetallic (Cd, Zn, Pb) contaminated agricultural soil. Mycorrhiza 19:187–195

  46. Rozpądek P, Wężowicz K, Stojakowska A, Malarz J, Surówka E, Anielska T, Ważny R, Miszalski Z, Turnau K (2014) Mycorrhizal fungi modulate phytochemical production and antioxidant activity of Cichorium intybus L.(Asteraceae) under metal toxicity. Chemosphere 112:217–224

  47. 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. Front Plant Sci 8:906

  48. Sheikh-Assadi M, Khandan-Mirkohi A, Alemardan A, Moreno-Jiménez E (2015) Mycorrhizal Limonium sinuatum (L.) mill. enhances accumulation of lead and cadmium. Int J Phytoremediation 17:556–562

  49. Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60

  50. Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic Press, Elsevier Ltd., Oxford

  51. Subramanian KS, 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. Appl Soil Ecol 43:32–39

  52. Sytar O, Latowski D, Kumar A, Kuczynska P, Strzalka K, Prasad M (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999

  53. Tan S, Jiang Q, Zhuo F, Liu H, Wang Y, Li S, Ye Z, Jing Y (2015) Effect of inoculation with Glomus versiforme on cadmium accumulation, antioxidant activities and phytochelatins of Solanum photeinocarpum. PLoS One 10:e132347

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

  55. Wang X, Hoffland E, Feng G, Kuyper TW (2017b) Phosphate uptake from phytate due to hyphae-mediated phytase activity by arbuscular mycorrhizal maize. Front Plant Sci 8:684

  56. Wu Z, McGrouther K, Huang J, Wu P, Wu W, Wang H (2014) Decomposition and the contribution of glomalin-related soil protein (GRSP) in heavy metal sequestration: field experiment. Soil Biol Biochem 68:283–290

  57. Wu S, Zhang X, Sun Y, Wu Z, Li T, Hu Y, Su D, Lv J, Li G, Zhang Z (2015) Transformation and immobilization of chromium by arbuscular mycorrhizal fungi as revealed by SEM-EDS, TEM-EDS, and XAFS. Environ Sci Technol 49:14036–14047

  58. 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. Environ Exp Bot 122:10–18

  59. Yang Y, Liang Y, Ghosh A, Song Y, Chen H, Tang M (2015) Assessment of arbuscular mycorrhizal fungi status and heavy metal accumulation characteristics of tree species in a lead-zinc mine area: potential applications for phytoremediation. Environ Sci Pollut Res 22:13179–13193

  60. Zarei M, Hempel S, Wubet T, Schäfer T, Savaghebi G, Jouzani GS, Nekouei MK, Buscot F (2010) Molecular diversity of arbuscular mycorrhizal fungi in relation to soil chemical properties and heavy metal contamination. Environ Pollut 158:2757–2765

  61. Zhan F, He Y, Yue X, Qin L, Xia Y (2016) Effect of mycorrhizal inoculation on plant growth, nutrients and heavy metals uptake by Leucaena leucocephala. Fresenius Environ Bull 25:1760–1767

  62. Zhou X, Fu L, Xia Y, Zheng L, Chen C, Shen Z, Chen Y (2017) Arbuscular mycorrhizal fungi enhance the copper tolerance of Tagetes patula through the sorption and barrier mechanisms of intraradical hyphae. Metallomics 9:936–948

Download references

Funding

The National Natural Science Foundation of China (Nos. 41461093, 41661056 and 41561057), the Natural Science Foundation of Yunnan Province (No. 2016FB032), and the Science and Technology Innovation Team of Yunnan Province (No. 2017HC015) provided financial support for this work.

Author information

Correspondence to Yongmei He or Yunsheng Xia.

Additional information

Responsible editor: Yi-ping Chen

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhan, F., Li, B., Jiang, M. et al. 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 (2018). https://doi.org/10.1007/s11356-018-2487-z

Download citation

Keywords

  • Symbiont
  • Plant growth
  • Antioxidant physiology
  • Nutrient content
  • Heavy metal content