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About plant species potentially promising for phytoextraction of large amounts of toxic trace elements

Abstract

There is no information yet about plant species capable of accumulating many different metals/metalloids. The plants feasible for phytoremediation aims must grow fast, have high biomass, deep roots, and should accumulate and tolerate a range of toxicants in their aerial parts. In our research, greenhouse and field experiments have been performed to investigate accumulation and tolerance of not well-studied trace elements such as Br, Eu, Sc, Th (and also U) in couch grass and wheat. We compared bioaccumulation abilities of the plants with those of some other plant species grown under the same conditions. Additionally, we tested the effects of inoculation of seeds with Cellulomonas bacteria on phytoextraction of the trace elements from contaminated soils. For determination of elements, we used neutron activation analysis and ICP-MS. It was found that couch grass and wheat can grow in heavily contaminated soils and accumulate different toxic trace elements to levels that exceed physiological requirements typical for most plant species. Infection of seeds with bacteria resulted in a significant increase in the uptake of various trace elements and their translocation to upper plant parts. The use of couch grass and/or wheat, either alone or in combination with microorganisms, is a promising way to phytoextract metals/metalloids from contaminated soils.

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References

  1. Ahmad, H. R., Zia-ur-Rehman, M., Sohail, M. I., ul HaqKhalid, M. A. H., Ayub, M. A., et al. (2018). Chapter 11—Effects of rare earth oxide nanoparticles on plants. In D. K. Tripathi, P. Ahmad, S. Sharma, D. K. Chauhan, & N. K. Dubey (Eds.), Nanomaterials in plants, algae, and microorganisms Concepts and Controversies (pp. 239–275). London: Elsevier. https://doi.org/10.1016/B978-0-12-811487-2.00011-6.

    Chapter  Google Scholar 

  2. Alford, É. R., Pilon-Smits, E. A. H., & Paschke, M. W. (2010). Metallophytes—a view from the rhizosphere. Plant and Soil, 337(1–2), 33–50. https://doi.org/10.1007/s11104-010-0482-3.

    CAS  Article  Google Scholar 

  3. Alloway, B. J. (2013). Heavy metals in soils: Trace metals and metalloids in soils and their bioavailability (3rd ed.). Dordrecht: Springer. https://doi.org/10.1007/978-94-007-4470-7.

    Book  Google Scholar 

  4. Atabayeva, S. (2016). Heavy metals accumulation ability of wild grass species from industrial areas of Kazakhstan. In A. Ansari, S. Gill, R. Gill, G. Lanza, & L. Newman (Eds.), Phytoremediation (pp. 157–208). Cham: Springer.

    Chapter  Google Scholar 

  5. Ayangbenro, A. S., & Babalola, O. O. (2017). A new strategy for heavy metal polluted environments: A review of microbial biosorbents. International Journal of Environmental Research and Public Health, 14(1), 94. https://doi.org/10.3390/ijerph14010094.

    CAS  Article  Google Scholar 

  6. Baker, A. J. M., Reeves, R. D., & Hajar, A. S. M. (1994). Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytologist, 127(1), 61–68. https://doi.org/10.1111/j.1469-8137.1994.tb04259.x.

    CAS  Article  Google Scholar 

  7. Basta, N. T., & McGowen, S. L. (2004). Evaluation of chemical immobilization treatments for reducing heavy metal transport in a smelter-contaminated soil. Environmental Pollution, 127(1), 73–82. https://doi.org/10.1016/S0269-7491(03)00250-1.

    CAS  Article  Google Scholar 

  8. Brej, T. (1998). Heavy metal tolerance in Agropyron repens (L.) P. Bauv. populations from the Legnica copper smelter area, Lower Silesia. Acta Societatis Botanicorum Poloniae, 67(3–4), 325–333. https://doi.org/10.5586/asbp.1998.041.

    CAS  Article  Google Scholar 

  9. Brooks, R. R., Malaisse, F., & Empain, A. (1985). The heavy metal tolerant flora of Southcentral Africa: A multidisciplinary approach. Rotterdam, Boston: A.A. Balkema.

    Google Scholar 

  10. Burges, A., Alkorta, I., Epelde, L., & Garbisu, C. (2018). From phytoremediation of soil contaminants to phytomanagement of ecosystem services in metal contaminated sites. International Journal of Phytoremediation, 20(4), 384–397. https://doi.org/10.1080/15226514.2017.1365340.

    CAS  Article  Google Scholar 

  11. Castaldi, P., Santona, L., & Melis, P. (2005). Heavy metal immobilization by chemical amendments in a polluted soil and influence on white lupin growth. Chemosphere, 60(3), 365–371. https://doi.org/10.1016/j.chemosphere.2004.11.098.

    CAS  Article  Google Scholar 

  12. Chandra, R., Kumar, V., Tripathi, S., & Sharma, P. (2018). Heavy metal phytoextraction potential of native weeds and grasses from endocrine-disrupting chemicals rich complex distillery sludge and their histological observations during in-situ phytoremediation. Ecological Engineering, 111, 143–156. https://doi.org/10.1016/j.ecoleng.2017.12.007.

    Article  Google Scholar 

  13. d’Aquino, L., Pinto, M. C., Nardi, L., Morgana, M., & Tommasi, F. (2009). Effect of some light rare earth elements on seed germination, seedling growth and antioxidant metabolism in Triticum durum. Chemosphere, 75(7), 900–905. https://doi.org/10.1016/j.chemosphere.2009.01.026.

    CAS  Article  Google Scholar 

  14. De Maria, S., Rivelli, A. R., Kuffner, M., Sessitsch, A., Wenzel, W. W., Gorfer, M., et al. (2011). Interactions between accumulation of trace elements and major nutrients in Salix caprea after inoculation with rhizosphere microorganisms. Chemosphere, 84(9), 1256–1261. https://doi.org/10.1016/j.chemosphere.2011.05.002.

    CAS  Article  Google Scholar 

  15. DePierre, J. W. (2003). Mammalian toxicity of organic compounds of bromine and iodine. In: A. H. Neilson (Ed.) Organic bromine and iodine compounds. The handbook of environmental chemistry, vol 3R (pp. 205–251). Berlin: Springer.

  16. Dickinson, N. M., Baker, A. J. M., Doronila, A., Laidlaw, S., & Reeves, R. D. (2009). Phytoremediation of inorganics: realism and synergies. International Journal of Phytoremediation, 11(2), 97–114. https://doi.org/10.1080/15226510802378368.

    CAS  Article  Google Scholar 

  17. Eljarrat, E., Marsh, G., Labandeira, A., & Barceló, D. (2008). Effect of sewage sludges contaminated with polybrominated diphenylethers on agricultural soils. Chemosphere, 71(6), 1079–1086. https://doi.org/10.1016/j.chemosphere.2007.10.047.

    CAS  Article  Google Scholar 

  18. Favas, P. J. C., Pratas, J., Paul, M. S., & Prasad, M. N. V. (2019). Remediation of uranium-contaminated sites by phytoremediation and natural attenuation. In V. C. Pandey & B. Kuldeep (Eds.), Phytomanagement of polluted sites: Market opportunities in sustainable phytoremediation (pp. 277–300). Imprint: Elsevier. https://doi.org/10.1016/B978-0-12-813912-7.00010-7.

    Chapter  Google Scholar 

  19. Gadd, G. M. (2004). Microbial influence on metal mobility and application for bioremediation. Geoderma, 122, 109–119. https://doi.org/10.1016/j.geoderma.2004.01.002.

    CAS  Article  Google Scholar 

  20. Gerhardt, K. E., Gerwing, P. D., & Greenberg, B. M. (2017). Opinion: Taking phytoremediation from proven technology to accepted practice. Plant Science, 256, 170–185. https://doi.org/10.1016/j.plantsci.2016.11.016.

    CAS  Article  Google Scholar 

  21. Gupta, D. K., Chatterjee, S., Mitra, A., Voronina, A., & Walther, C. (2020). Uranium and plants: Elemental translocation and phytoremediation approaches. In D. Gupta & C. Walther (Eds.), Ethics and law for chemical, biological, radiological, nuclear & explosive crises (pp. 149–161). Cham: Springer. https://doi.org/10.1007/978-3-030-14961-1_7.

    Chapter  Google Scholar 

  22. Horovitz, C. T. (2000). Biochemistry of scandium and yttrium Part 2: Biochemistry and applications. New York: Kluwer Academic Publishers. https://doi.org/10.1007/978-1-4615-4311-4.

    Book  Google Scholar 

  23. Huang, H., Zhang, S., & Christie, P. (2011). Plant uptake and dissipation of PBDEs in the soils of electronic waste recycling sites. Environmental Pollution, 159(1), 238–243. https://doi.org/10.1016/j.envpol.2010.08.034.

    CAS  Article  Google Scholar 

  24. Janoš, P., Vávrová, J., Herzogová, L., & Pilařová, V. (2010). Effects of inorganic and organic amendments on the mobility (leachability) of heavy metals in contaminated soil: A sequential extraction study. Geoderma, 159(3–4), 335–341. https://doi.org/10.1016/j.geoderma.2010.08.009.

    CAS  Article  Google Scholar 

  25. Khankhane, P. J., & Varshney, J. G. (2008). Accumulation of heavy metals by weeds grown along drains of Jabalpur. Indian Journal of Weed Science, 40(1&2), 55–59.

    Google Scholar 

  26. Kumar, A., & Thakur, N. (2019). Phytoremediation: Green technology for heavy metal clean up from contaminated soils. International Journal of Chemical Studies, 7(5), 1987–1994.

    CAS  Google Scholar 

  27. Kumar, N., Bauddh, K., Kumar, S., Dwivedi, N., Singh, D. P., & Barman, S. C. (2013). Accumulation of metals in weed species grown on the soil contaminated with industrial waste and their phytoremediation potential. Ecological Engineering, 61, 491–495. https://doi.org/10.1016/j.ecoleng.2013.10.004.

    Article  Google Scholar 

  28. Lee, J. (2013). An overview of phytoremediation as a potentially promising technology for environmental pollution control. Biotechnology & Bioprocess Engineering, 18(3), 431–439. https://doi.org/10.1007/s12257-013-0193-8.

    CAS  Article  Google Scholar 

  29. Li, J., & Zhang, Y. (2012). Remediation technology for the uranium contaminated environment: A review. Procedia Environmental Sciences, 13, 1609–1615. https://doi.org/10.1016/j.proenv.2012.01.153.

    CAS  Article  Google Scholar 

  30. Liu, W.-X., Liu, J.-W., Wu, M.-Z., Li, Y., Zhao, Y., & Li, S.-R. (2009). Accumulation and translocation of toxic heavy metals in winter wheat (Triticum aestivum L.) growing in agricultural soil of Zhengzhou, China. Bulletin of Environmental Contamination and Toxicology, 82(3), 343–347. https://doi.org/10.1007/s00128-008-9575-6.

    CAS  Article  Google Scholar 

  31. Lu, Q., Weng, Y., You, Y., Xu, Q., Li, H., Li, Y., et al. (2020). Inoculation with abscisic acid (ABA)-catabolizing bacteria can improve phytoextraction of heavy metal in contaminated soil. Environmental Pollution. https://doi.org/10.1016/j.envpol.2019.113497.

    Article  Google Scholar 

  32. Ma, Y., Oliveira, R. S., Nai, F., Rajkumar, M., Luo, Y., Rocha, I., et al. (2015). The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. Journal of Environmental Management, 156(1), 62–69. https://doi.org/10.1016/j.jenvman.2015.03.024.

    CAS  Article  Google Scholar 

  33. Mahar, A., Wang, P., Ali, A., Awasthi, M. K., Lahori, A. H., Wang, Q., et al. (2016). Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: A review. Ecotoxicology and Environmental Safety, 126, 111–121. https://doi.org/10.1016/j.ecoenv.2015.12.023.

    CAS  Article  Google Scholar 

  34. Maqbool, A., Xiao, X., Wang, H., Bian, Z., & Akram, M. W. (2019). Bioassessment of heavy metals in wheat crop from soil and dust in a coal mining area. Pollution, 5(2), 323–337. https://doi.org/10.22059/poll.2019.267256.528.

    CAS  Article  Google Scholar 

  35. Missimer, T. M., Teaf, C., Maliva, R. G., Danley-Thomson, A., Covert, D., & Hegy, M. (2019). Natural radiation in the rocks, soils, and groundwater of Southern Florida with a discussion on potential health impacts. International Journal of Environmental Research and Public Health, 16(10), 1793. https://doi.org/10.3390/ijerph16101793.

    CAS  Article  Google Scholar 

  36. Mohan, A., Girdhar, M., Rehman, H., Kumar, A., Saggu, S., & Ansari, A. A. (2015). Metal accumulation capability of weeds and their utilization in phytoremediation technology. In A. Ansari, S. Gill, R. Gill, G. Lanza, & L. Newman (Eds.), phytoremediation (pp. 343–357). Cham: Springer. https://doi.org/10.1007/978-3-319-10969-5_28.

    Chapter  Google Scholar 

  37. Paul, A. L. D., der Ent, A., & Erskine, P. D. (2019). Scandium biogeochemistry at the ultramafic Lucknow deposit, Queensland, Australia. Journal of Geochemical Exploration, 204, 74–82. https://doi.org/10.1016/j.gexplo.2019.05.005.

    CAS  Article  Google Scholar 

  38. Raven, K. P., & Loeppert, R. H. (1997). Trace element composition of fertilizers and soil amendments. Journal of Environmental Quality, 26(2), 551–557.

    CAS  Article  Google Scholar 

  39. Ren, C.-G., Kong, C.-C., Wang, S.-X., & Xie, Z.-H. (2019). Enhanced phytoremediation of uranium-contaminated soils by arbuscular mycorrhiza and rhizobium. Chemosphere, 217, 773–779. https://doi.org/10.1016/j.chemosphere.2018.11.085.

    CAS  Article  Google Scholar 

  40. Rodríguez-Bocanegra, J., Roca, N., Febrero, A., & Bort, J. (2018). Assessment of heavy metal tolerance in two plant species growing in experimental disturbed polluted urban soil. Journal of Soils and Sediments, 18(6), 2305–2317. https://doi.org/10.1007/s11368-017-1666-8.

    CAS  Article  Google Scholar 

  41. Samson, I., & Chassé, M. (2016). Scandium. In W. M. White (Ed.), Encyclopedia of geochemistry (pp. 1–14). Switzerland: Springer International Publishing. https://doi.org/10.1007/978-3-319-39193-9_281-1.

    Chapter  Google Scholar 

  42. Sarwar, N., Imran, M., Shaheen, M. R., Ishaque, W., Matloob, M. A. K. A., Rehim, A., et al. (2017). Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives. Chemosphere, 171, 710–721. https://doi.org/10.1016/j.chemosphere.2016.12.116.

    CAS  Article  Google Scholar 

  43. Selvakumar, R., Ramadoss, G., Menon, M. P., Rajendran, K., Thavamani, P., Naidu, R., et al. (2018). Challenges and complexities in remediation of uranium contaminated soils: A review. Journal of Environmental Radioactivity, 192, 592–603. https://doi.org/10.1016/j.jenvrad.2018.02.018.

    CAS  Article  Google Scholar 

  44. Sharma, V. K., Zboril, R., & McDonald, T. J. (2014). Formation and toxicity of brominated disinfection byproducts during chlorination and chloramination of water: A review. Journal of Environmental Science and Health, Part B, 49(3), 212–228. https://doi.org/10.1080/03601234.2014.858576.

    CAS  Article  Google Scholar 

  45. Shtangeeva, I., Ayrault, S., & Jain, J. (2004). Scandium bioaccumulation and its effect on uptake of macro- and trace-elements during initial phases of plant growth. Soil Science and Plant Nutrition, 50(6), 885–889. https://doi.org/10.1080/00380768.2004.10408549.

    CAS  Article  Google Scholar 

  46. Shtangeeva, I., & Ayrault, S. (2007). Effects of Eu and Ca on yield and mineral nutrition of wheat (Triticum aestivum) seedlings. Environmental and Experimental Botany, 59(1), 49–58. https://doi.org/10.1016/j.envexpbot.2005.10.011.

    CAS  Article  Google Scholar 

  47. Shtangeeva, I. (2014). Europium and cerium accumulation in wheat and rye seedlings. Water, Air, & Soil Pollution, 225, 1964. https://doi.org/10.1007/s11270-014-1964-3.

    CAS  Article  Google Scholar 

  48. Shtangeeva, I., Niemelä, M., Perämäki, P., & Timofeev, S. (2015). Response of wheat and pea seedlings on increase of bromine concentration in the growth medium. Environmental Science and Pollution Research, 22(23), 19060–19068. https://doi.org/10.1007/s11356-015-5106-2.

    CAS  Article  Google Scholar 

  49. Šola, I., Piantanida, I., Crnolatac, I., & Rusak, G. (2015). Europium improves the transport of quercetin through Arabidopsis thaliana. Biologia Plantarum, 59(3), 554–559. https://doi.org/10.1007/s10535-015-0508-z.

    CAS  Article  Google Scholar 

  50. Song, Y., Kirkwood, N., Maksimović, Č., Zheng, X., O'Connor, D., Jin, Y., et al. (2019). Nature based solutions for contaminated land remediation and brownfield redevelopment in cities: A review. Science of the Total Environment, 663, 568–579. https://doi.org/10.1016/j.scitotenv.2019.01.347.

    CAS  Article  Google Scholar 

  51. Tagami, K., Uchida, S., Hirai, I., Tsukada, H., & Takeda, H. (2006). Determination of chlorine, bromine and iodine in plant samples by inductively coupled plasma-mass spectrometry after leaching with tetramethyl ammonium hydroxide under a mild temperature condition. Analytica Chimica Acta, 570(1), 88–92. https://doi.org/10.1016/j.aca.2006.04.011.

    CAS  Article  Google Scholar 

  52. Tanhan, P., Kruatrachue, M., Pokethitiyook, P., & Chaiyarat, R. (2007). Uptake and accumulation of cadmium, lead and zinc by Siam weed [Chromolaena odorata (L.) King & Robinson]. Chemosphere, 68(2), 323–329. https://doi.org/10.1016/j.chemosphere.2006.12.064.

    CAS  Article  Google Scholar 

  53. Tian, H. E., Gao, Y. S., Li, F. M., & Zeng, F. (2003). Effects of europium ions (Eu3+) on the distribution and related biological activities of elements in Lathyrus sativus L. roots. Biological Trace Element Research, 93, 257–269. https://doi.org/10.1385/BTER:93:1-3:257.

    CAS  Article  Google Scholar 

  54. Tsuruta, T. (2004). Cell-associated adsorption of thorium or uranium from aqueous system using various microorganisms. Water, Air, & Soil Pollution, 159, 35–47. https://doi.org/10.1023/B:WATE.0000049190.05993.3b.

    CAS  Article  Google Scholar 

  55. Vijayaraghavan, K., Sathishkumar, M., & Balasubramanian, R. (2010). Biosorption of lanthanum, cerium, europium, and ytterbium by a brown marine alga, Turbinaria Conoides. Industrial and Engineering Chemistry Research, 49, 4405–4411. https://doi.org/10.1021/ie1000373.

    CAS  Article  Google Scholar 

  56. Wang, F. Y., Lin, X. G., & Yin, R. (2007). Role of microbial inoculation and chitosan in phytoextraction of Cu, Zn, Pb and Cd by Elsholtzia splendens – a field case. Environmental Pollution, 147(1), 248–255. https://doi.org/10.1016/j.envpol.2006.08.005.

    CAS  Article  Google Scholar 

  57. Wang, S., Wu, W., Liu, F., Liao, R., & Hu, Y. (2017). Accumulation of heavy metals in soil-crop systems: A review for wheat and corn. Environmental Science and Pollution Research, 24(18), 15209–15225. https://doi.org/10.1007/s11356-017-8909-5.

    CAS  Article  Google Scholar 

  58. Wang, W., Xiong, Y., Zhang, J., Lu, X., & Wei, G. (2020). Naturally selected dominant weeds as heavy metal accumulators and excluders assisted by rhizosphere bacteria in a mining area. Chemosphere, 243, 125365. https://doi.org/10.1016/j.chemosphere.2019.125365.

    CAS  Article  Google Scholar 

  59. Wei, A., Zhou, Q., & Saha, U. K. (2008). Hyperaccumulative characteristics of weed species to heavy metals. Water Air and Soil Pollution, 192(1–4), 173–181. https://doi.org/10.1007/s11270-008-9644-9.

    CAS  Article  Google Scholar 

  60. Wei, B., & Yang, L. (2010). A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchemical Journal, 94(2), 99–107. https://doi.org/10.1016/j.microc.2009.09.014.

    CAS  Article  Google Scholar 

  61. Wisniak, J. (2002). The history of bromine—from discovery to commodity. Indian Journal of Chemical Technology, 9(3), 263–271.

    CAS  Google Scholar 

  62. Withers, R. M. J., & Lees, F. P. (1986). The assessment of major hazards: The lethal toxicity of bromine. Journal of Hazardous Materials, 13(3), 279–299. https://doi.org/10.1016/0304-3894(86)85002-6.

    CAS  Article  Google Scholar 

  63. Wójcik, M., Gonnelli, C., Selvi, F., Dresler, S., Rostański, A., & Vangronsveld, J. (2017). Chapter one—Metallophytes of serpentine and calamine soils—their unique ecophysiology and potential for phytoremediation. Advances in Botanical Research, 83, 1–42. https://doi.org/10.1016/bs.abr.2016.12.002.

    CAS  Article  Google Scholar 

  64. Yang, C. Y., Chang, M. L., & WuShih, S. C. Y. H. (2017). Partition uptake of a brominated diphenyl ether by the edible plant root of white radish (Raphanus sativus L.). Environmental Pollution, 223, 178–184. https://doi.org/10.1016/j.envpol.2017.01.009.

    CAS  Article  Google Scholar 

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Acknowledgements

Irina Shtangeeva acknowledges a partial financial support of this work by Russian Foundation of Basic Research (Grant No. 18–53-80010).

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Shtangeeva, I. About plant species potentially promising for phytoextraction of large amounts of toxic trace elements. Environ Geochem Health 43, 1689–1701 (2021). https://doi.org/10.1007/s10653-020-00633-z

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Keywords

  • Phytoextraction
  • Trace elements
  • Couch grass
  • Wheat
  • Cellulomonas bacteria