Effects of Calcium Phosphates on the (Im)Mobilization of Metals and Nutrients, on the Biological Activity and on the Plant Health from Multi-contaminated Urban Soils

  • Marie Hechelski
  • Brice Louvel
  • Pierrick Dufrénoy
  • Alina Ghinet
  • Christophe WaterlotEmail author


Two smelters in the North of France emitted potentially toxic metals for more than a century and today, the resulting contamination represents a risk to human health and affects also the biodiversity. To limit health risks and to improve the soil quality, a study using calcium phosphates (monocalcium phosphate, dicalcium phosphate and a mixture of both salts) and Lolium perenne L was conducted. Through this preliminary investigation, we will try to shed some light about (i) the effects of a sustainable amount of calcium phosphates on the agronomic, biological (microbial and fungi communities) and physiological parameters (chlorophyll a and b, antocyanins, carotenoids) as well as the phytoavailability of potentially toxic metals and nutrients in time, and (ii) the potential use of contaminated biomass from ryegrass as a source of new valorisation ways instead of using it as contaminated compost by gardeners. Although slight variations in pH and significant increases of assimilable phosphorus after adding calcium phosphates were registered, the physiology of plants and the biological parameters were statistically unchanged. The germination of the ryegrass seeds was favoured with calcium phosphates regardless the contamination level of the studied soils. No clear effects of calcium phosphates on the microbial and fungi communities were detected. In contrast, results indicated relationships between the physicochemical parameters of soils, their contamination level and the composition of fungal communities. Indeed, for one of the soils studied, calcium could limit the transport of nutrients, causing an increase in fungi to promote again the transfer of nutrients. Surprisingly, the phytoavailability of Pb increased in the most contaminated soil after adding dicalcium phosphate and the mixture of phosphates whereas a slight decrease was highlighted for Cd and Mn. Although minor changes in the phytoavailability of potentially toxic metals were obtained using calcium phosphates, the ability of ryegrass to accumulate Zn and Ca (up to 600 and 20,000 mg kg−1, respectively) make possible to qualify this plant as a bio ‘ore’ resource.


Metals Nutrients Calcium phosphates Ryegrass Biomarkers Microbes 



The authors warmly thank the ‘Fondation de la Catho de Lille, France’ and Yncréa Hauts-de-France for the financial support of this work and Dr. Elisabeth Gross for her assistance in the implementation of the protocol on the determination of pigment contents in plants.


  1. Abbaspour, A., & Golchin, A. (2011). Immobilization of heavy metals in a contaminated soil in Iran using di-ammonium phosphate, vermicompost and zeolite. Environmenal Earth Science, 63, 935–943.CrossRefGoogle Scholar
  2. Ali, A., Gue, D., Mahar, A., Wang, P., Shen, F., Li, R. H., & Zhang, Z. (2017). Mycoremediation of potentially toxic trace elements - a biological tool for soil cleanup: a review. Pedosphere, 27, 205–222.CrossRefGoogle Scholar
  3. Ahmad, M., Lee, S. S., Yang, J. E., Ro, H. M., Lee, Y. H., & Ok, Y. S. (2012). Effects of soil dilution and amendments (mussel shell, cow bone, and biochar) on Pb availability and phytotoxicity in military shooting range soil. Ecotoxicology and Environmental Safety, 79, 225–231.CrossRefGoogle Scholar
  4. Alvarez, F. J., Douglas, L. M., & Konopka, J. B. (2007). Sterol-rich plasma membrane domains in fungi. Eukaryotic Cell, 6, 755–763.CrossRefGoogle Scholar
  5. Arienzo, M., Adamo, P., & Cozzolino, V. (2004). The potential of Lolium perenne for revegetation of contaminated soil from a metallurgical site. Science of the Total Environment, 319, 13–25.CrossRefGoogle Scholar
  6. Austruy, A., Shahid, M., Xiong, T., Castrec, M., Payre, V., Niazi, N. K., Sabir, M., & Dumat, C. (2014). Mechanism of meatal-phosphates formation in the rhizosphere soils of pea and tomato: environmental and sanitary consequences. Journal of Soils and Sediments, 14, 666–678.CrossRefGoogle Scholar
  7. Balestrini, R., & Lumini, E. (2018). Focus on mycorrhizal symbioses. Applied Soil Ecology, 123, 299–304.CrossRefGoogle Scholar
  8. Baskin, C. C., & Baskin, J. M. (2001). Seeds: ecology, biogeography, and evolution of dormancy and germination. San Diego, London: Academic Press.Google Scholar
  9. Brahim, M. B., Loustau, D., Gaudillère, J. P., & Saur, E. (1996). Effects of phosphate deficiency on photosynthesis and accumulation of starch and soluble sugars in 1-year-old seedlings of maritime pine (Pinus pinaster Ait). Annales des Sciences Forestières, INRA/EDP Sciences, 53, 801–810.CrossRefGoogle Scholar
  10. Carvalho, A., Nabis, C., Roiloa, S. R., & Rodriguez-Echeverria, S. (2013). Revegetation of abandoned copper mines: the role of seed banks and soil amendments. Web Ecology, 13, 69–77.CrossRefGoogle Scholar
  11. Chen, Y., Hu, L., Liu, X., Deng, Y., Liu, M., Xu, B., Wang, M., & Wang, G. (2017). Influences of king grass (Pennisetum sinese Roxb)-enhanced approaches for phytoextraction and microbial communities in multi-metal contaminated soil. Geoderma, 307, 253–266.CrossRefGoogle Scholar
  12. Chen, S. Y., Ou, S. F., Teng, N. C., Kung, C. M., Tsai, H. L., Chu, K. T., & Ou, K. L. (2013). Phase transformation on bone cement: monocalcium phosphate monohydrate into calcium-deficient hydroxyapatite during setting. Ceramics International, 39, 2451–2455.CrossRefGoogle Scholar
  13. Couder, E., Mattielli, N., Drouet, T., Smolders, E., Delvaux, B., Iserentant, A., Meeus, C., Maerschalk, C., Opfergelt, S., & Houben, D. (2015). Transpiration flow controls Zn transport in Brassica napus and Lolium multiflorum under toxic levels as evidenced from isotopic fractionation; hydrology, environment. Comptes Rendus Geoscience, 347, 386–396.CrossRefGoogle Scholar
  14. Dabrowski, P., Pawluśkiewicz, B., Baczewska, A. H., Oglecki, P., & Kalaji, H. (2015). Chlorophyll a fluorescence of perennial ryegrass (Lolium perenne L.) varieties under long-term exposure to shade. Zemdirbyste-Agriculture, 102, 305–312.CrossRefGoogle Scholar
  15. Dada, E. O., Njoku, K. L., Osuntoki, A. A., & Akinola, M. O. (2015). A review of current techniques of in situ physico-chemical and biological remediation of heavy metals polluted soil. Ethiopian Journal of Environmental Studies & Management, 8, 606–615.CrossRefGoogle Scholar
  16. Dehbi, H. (1986). Synthèse mécanochimique et réactivité du phosphate bicalcique. Thesis report, pp.1–151.Google Scholar
  17. Dent, D. L., Downing, E. J. B., & Rogaar, H. (1976). Changes in the structure of marsh soils following drainage and arable. Journal of Soil Science, 27, 250–265.CrossRefGoogle Scholar
  18. Ermakova, E., & Zuev, Y. (2017). Effect of ergosterol on the fungal membrane properties. All-atom and coarse-grained molecular dynamics study. Chemistry and Physics of Lipids, 209, 45–53.Google Scholar
  19. Fontvieille, D. A., Outaguerouine, A., & Thevenor, D. R. (1992). Fluorescein diacetate hydrolysis as a measure of microbial activity in aquatic systems: application to activated sludges. Environmental Technology, 13, 531–540.CrossRefGoogle Scholar
  20. Franssens, M., Flament, P., Deboudt, K., Weis, D., & Perdrix, E. (2004). Evidencing lead deposition at the urban scale using “short-lived” isotopic signatures of the source term (Pb-Zn refinery). Atmospheric Environment, 38, 5157–5168.CrossRefGoogle Scholar
  21. Feng, M. H., Shan, X. Q., Zhang, S. Z., & Wen, B. (2005). Comparison of a rhizosphere-based method with other one-step extraction methods for assessing the bioavailability of soil metals to wheat. Chemosphere, 59, 939–949.CrossRefGoogle Scholar
  22. Green, V. S., Stott, D. E., & Diack, M. (2006). Assay for fluorescein diacetate hydrolytic activity: optimization for soil samples. Soil Biology and Biochemistry, 38, 693–701.CrossRefGoogle Scholar
  23. Gong, P., Guan, X., & Witter, E. (2001). A rapid method to extract ergosterol from soil by physical disruption. Applied Soil and Ecology, 17, 285–289.CrossRefGoogle Scholar
  24. Hannaway, D., Fransen, S., Cropper, J., Teel, M., Chaney, M., Griggs, T., Halse, R., Hart, J., Cheek, P., Hansen, D., Klinger, R., & Lane, W. (1999). Perennial ryegrass (Lolium perenne L.). PNW, 503, 1–19.Google Scholar
  25. Hazelden, J., & Boorman, L. A. (2001). Soils and ‘managed retreat’ in South East England. Soil Use and Management, 17, 150–154.CrossRefGoogle Scholar
  26. Hazotte, C., Laubie, B., Rees, F., Morel, J. L., & Simonnot, M. O. (2017). A novel process to recover cadmium and zinc from the hyperaccumulator plant Noccaea caerulescens. Hydrometallurgy, 174, 56–65.CrossRefGoogle Scholar
  27. Hechelski, M., Ghinet, A., Louvel, B., Dufrénoy, P., Rigo, B., Daïch, A., & Waterlot, C. (2018). From conventional Lewis acids to heterogeneous montmorillonite K10, eco-friendly plant-based catalysts used as green Lewis acids. Chemistry & Sustainability Energy & Materials, 11, 1249–1277.Google Scholar
  28. Heiri, O., Lotter, A. F., & Lemcke, G. (2001). Loss on ignition as a method for estimation organic and carbonate content in sediments: reproducibility and comparability of results. Journal of Paleolimnology, 25, 101–110.CrossRefGoogle Scholar
  29. Hseu, Z. Y., Su, S. W., Lai, H. Y., Guo, H. Y., Chen, T. C., & Chen, Z. S. (2010). Remediation techniques and heavy metal uptake by different rice varieties in metal contaminated soils of Taiwan: new aspects for food safety regulation and sustainable agriculture. Soil Science and Plant Nutrition, 56, 31–52.CrossRefGoogle Scholar
  30. Hussain, A., Abbas, N., Arshad, F., Akram, M., Khan, Z. I., Ahmad, K., Mansha, M., & Mirzaei, F. (2013). Effects of diverse doses of lead (Pb) on different growth attributes of Zea mays L. Agriculture Sciences, 4, 262–265.CrossRefGoogle Scholar
  31. Hussain Lahori, A., Zhang, Z., Guo, Z., Mahar, A., Li, R., Kumar Awasthia, M., Ali Sial, T., Kumbhard, F., Wang, P., Shen, F., Zhao, J., & Huang, H. (2017). Potential use of lime combined with additives on (im) mobilization and phytoavailability of heavy metals from Pb/Zn smelter contaminated soils. Ecotoxicology and Environmental Safety, 145, 313–323.CrossRefGoogle Scholar
  32. Jakobsen, S.T. (2009). Interaction between plant nutrients: III. Antagonism between potassium, magnesium and calcium. Acta Agric. Scand. B — Soil & Plant Science, 43, 1–5.CrossRefGoogle Scholar
  33. Jakovljević, M. D., Kostić, N. M., & Antić-Mladenović, S. B. (2003). The availability of base elements (Ca, Mg, Na, K) in some important soil types in Serbia. Proceedings for Natural Sciences. Matica Srpska Novi Sad, 104, 11–21.Google Scholar
  34. Jia, Y., Tang, S., Wang, R., Ju, X., Ding, Y., Tu, S., & Smith, D. L. (2010). Effects of elevated CO2 on growth, photosynthesis, elemental composition, antioxidant level, and phytochelatin concentration in Lolium multiforum and Lolium perenne under Cd stress. Journal of Hazardous Materials, 180, 384–394.CrossRefGoogle Scholar
  35. Jones, D. L., Dennis, P. G., Owen, A. G., & van Hees, P. A. W. (2003). Organic acid behaviour in soils—misconceptions and knowledge gaps. Plant and Soil, 248, 31–41.CrossRefGoogle Scholar
  36. Joret-Hébert Method. NF X 31-161. Association Française de Normalisation, Paris.Google Scholar
  37. Khalid, S., Shahid, M., Niazi, N. K., Murtaza, B., Bibi, I., & Dumat, C. (2017). A comparison of technologies for remediation of heavy metal contaminated soils. Journal of Geochemical Exploration, 182, 247–268.CrossRefGoogle Scholar
  38. Küpper, H., Šetlik, I., Spiller, M., Küpper, F., & Prášil, O. (2002). Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. Journal of Phycology, 38, 429–441.Google Scholar
  39. Kutrowska, A., & Szelag, M. (2014). Low-molecular weight organic acids and peptides involved in the long-distance transport of trace metals. Acta Physiologiae Plantarum, 36, 1957–1968.CrossRefGoogle Scholar
  40. Landi, M., Tattini, M., & Gould, K. S. (2015). Multiple functional roles of anthocyanins in plant-environment interactions. Environmental and Experimental Botany, 119, 4–17.CrossRefGoogle Scholar
  41. Lazo, D. E., Dyer, L. G., & Alorro, R. D. (2017). Silicate, phosphate and carbonate mineral dissolution behaviour in the presence of organic acids: a review. Minerals Engineering, 100, 115–123.CrossRefGoogle Scholar
  42. Le Mare, P. (1977). Experiments on effects of phosphorous on the manganese nutrition of plants. III. The effect of calcium: phosphorous ratio on manganese in cotton grown in Buganda soil. Plant and Soil, 47, 621–630.CrossRefGoogle Scholar
  43. Li, X., Meng, D., Li, J., Yin, H., Liu, H., Liu, X., Cheng, C., Xiao, Y., Liu, Z., & Yan, M. (2017). Response of soil microbial communities and microbial interactions to long-term heavy metal contamination. Environmental Pollution, 231, 908–917.CrossRefGoogle Scholar
  44. Lichtenthaler, H. K., Ač, A., Marek, M. V., Kalina, J., & Urban, O. (2007). Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree spaces. Plant Physiology and Biochemistry, 45, 577–588.CrossRefGoogle Scholar
  45. Lichtenthaler, H. K., & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemistry Society Transactions, 11, 591–592.CrossRefGoogle Scholar
  46. Lopareva-Pohu, A., Verdin, A., Garçon, G., Lounès-Hadj Sahraoui, A., Pourrut, B., Debiane, D., Waterlot, C., Laruelle, F., Bidar, G., Douay, F., & Shiralli, P. (2011). Influence of fly ash aided phytostabilisation of Pb, Cd and Zn highly contaminated soils on Lolium perenne and Trifolium repens metal transfer and physiological stress. Environmental Pollution, 159, 1721–1729.CrossRefGoogle Scholar
  47. Ma, Y., Oliveira, R. S., Nai, F., Rajkumar, M., Luo, Y., Rocha, I., & Freitas, H. (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, 62–69.CrossRefGoogle Scholar
  48. Ma, Q. Y., Traina, S. J., Logan, T. L., & Ryan, J. A. (1993). In situ lead immobilization by apatite. Environmental Science and Technology, 27, 1803–1810.CrossRefGoogle Scholar
  49. Mahar, A., Ping, W., Ronghua, L., & Zengqiang, Z. (2015). Immobilization of lead and cadmium in contaminated soil using amendments: a review. Pedosphere, 25, 555–558.CrossRefGoogle Scholar
  50. Marschner, H., Römheld, V., Horst, W. J., & Martin, P. (1986). Root-induced changes in the rhizosphere: importance for the mineral nutrition of plants. Journal of Plant Nutrition and Soil Science, 149, 441–456.Google Scholar
  51. Mench, M., Morel, J. L., Guckert, A., & Guillet, B. (1988). Metal binding with root exudates of low molecular weight. Journal of Soil Science, 39, 521–527.CrossRefGoogle Scholar
  52. Moreno-Jiménez, E., Sepulveda, R., Esteban, E., & Beesley, L. (2017). Efficiency of organic and mineral based amendments to reduce metal (loid) mobility and uptake (Lolium perenne) from a pyrite-waste contaminated soil. Journal of Geochemical Exploration, 174, 46–52.CrossRefGoogle Scholar
  53. Mucha, A. P., Marisa, C., Almeida, R., Bordalo, A. A., Teresa, M., & Vasconcelos, S. D. (2010). LMWOA exudation buy salt marsh plants: natural variation and response to Cu contamination. Estuarine, Coastal and Shelf Science, 88, 63–70.CrossRefGoogle Scholar
  54. Mulder, E. G. (1948). Investigation on the nitrogen nutrition of pea plants. Plant and Soil I, 2, 179–212.CrossRefGoogle Scholar
  55. Murray, J. R., & Hackett, W. P. (1991). Dihydroflavonol reductase activity in relation to differential anthocyanin accumulation in juvenile and mature phase Hedera helix L. Plant Physiology, 97, 343–351.CrossRefGoogle Scholar
  56. Neumann, G., Massonneau, A., Martinoia, E., Römheld, V. (1999). Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta, 208, 373–382CrossRefGoogle Scholar
  57. Novozamsky, I., Lexmond, T. M., & Houba, V. J. G. (1993). A single extraction procedure of soil for evaluation of uptake of some heavy metals by plants. International Journal of Environmental Analytical Chemistry, 51, 47–58.CrossRefGoogle Scholar
  58. Nsanganwimana, F., Pourrut, B., Waterlot, C., Louvel, B., Bidar, G., Labidi, S., Fontaine, J., Muchembled, J., Lounès-Hadj Sahraoui, A., Fourrier, H., & Douay, F. (2015). Metal accumulation and shoot yield of Miscanthus × giganteus growing in contaminated agricultural soils: insights into agronomic practices. Agricultura, Ecosystems & Environment, 213, 61–71.CrossRefGoogle Scholar
  59. Nsanganwimana, F., Waterlot, C., Louvel, B., Pourrut, B., & Douay, F. (2016). Metal, nutrient and biomass accumulation during the growing cycle of Miscanthus established on metal-contaminated soils. Journal of Plant Nutrition and Soil Science, 179, 257–269.CrossRefGoogle Scholar
  60. Nuttens, A., Chatellier, S., Devin, S., Guingnard, C., Lenouvel, A., & Gross, E. M. (2016). Does nitrate co-pollution affect biological responses of an aquatic plant to two common herbicides? Aquatic Toxicology, 177, 355–364.CrossRefGoogle Scholar
  61. Op De Beeck, M., Lievens, B., Busschaert, P., Rineau, F., Smits, M., Vangronsveld, J., & Colpaert, J. V. (2015). Impact of metal pollution on fungal diversity and community structures. Environmental Microbiology, 17, 2035–2047.CrossRefGoogle Scholar
  62. Ouhadi, V. R., Yong, R. N., Shariatmadari, N., Saeidijam, S., Goodarzi, A. R., & Safari-Zanjan, M. (2010). Impact of carbonate on the efficiency of heavy metal removal from kaolinite soil by the electrokinetic soil remediation method. Journal of Hazardous Materials, 173, 87–94.CrossRefGoogle Scholar
  63. Pavel, L. V., Sobariu, D. L., Diaconu, M., Statescu, F., & Gavrilescu, M. (2013). Effects of heavy metals on Lepidium sativum germination and growth. Environmental Engineering and Management Journal, 12, 727–733.CrossRefGoogle Scholar
  64. Pelfrêne, A., Waterlot, C., Mazzuca, M., Nisse, C., Cuny, D., Richard, A., Denys, S., Heyman, C., Roussel, H., Bidar, G., & Douay, F. (2012). Bioaccessibility of trace elements as affected by soil parameters in smelter-contaminated agricultural soils: a statistical modelling approach. Environmental Pollution, 160, 130–138.CrossRefGoogle Scholar
  65. Philippe, S., Courcot, L., Douay, F., Waterlot, C., Pruvot, C., Caillaud, J., & Dörr, W. (2007). Contribution of two main smelters on urban soils pollution in northern France investigated by lead isotopes. Goldschmidt Conference. Geochimica Cosmochimica Acta, 71, A785–A785.Google Scholar
  66. Pourrut, B., Shahid, M., Dumat, C., Winterton, P., & Pinelli, E. (2011). Lead uptake, toxicity, and detoxification in plants. Reviews of Environmental Contamination and Toxicology, 213, 113–136.Google Scholar
  67. Pulford, I., & Watson, C. (2003). Phytoremediation of heavy metal-contaminated land by trees—a review. Environment International, 29, 529–540.CrossRefGoogle Scholar
  68. Rahoui, S., Chaoui, A., & El Ferjani, E. (2010). Membrane damage and solute leakage from germinating pea seed under cadmium stress. Journal of Hazardous Materials, 178, 1128–1131.CrossRefGoogle Scholar
  69. Ralph, P., & Burchett, M. D. (1998). Photosynthetic response of Halophila ovalis to heavy metal stress. Environmental Pollution, 103, 91–101.CrossRefGoogle Scholar
  70. Rascio, N., & Navari-Izzo, F. (2011). Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Science, 180, 168–181.CrossRefGoogle Scholar
  71. Raven, P. H., Evert, R. F., & Eichhorn, S. E. (2014). Biologie végétale (Third ed.). Louvain-la-Neuve: De Boeck.Google Scholar
  72. Rietra, R. P. J. J., Heinen, M., Dimpka, C. O., & Bindraban, P. S. (2017). Effects of nutrient antagonism and synergism on yield and fertilizer use efficiency. Communications in Soil Science and Plant Analysis, 48, 1895–1920.CrossRefGoogle Scholar
  73. Robinson, B., Schulin, R., Nowack, B., Roulier, S., Menon, M., Clothier, B., Green, S., & Mills, T. (2006). Phytoremediation for the management of metal flux in contaminated sites. For. Snow and Landscape Research, 80, 221–234.Google Scholar
  74. Rousk, J., Brookes, P. C., & Bååth, E. (2009). Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Applied and Environmental Microbiology, 75, 1589–1596.CrossRefGoogle Scholar
  75. Sabir, M., Waraich, E.A., Hakeem, K.R., Öztürk, M., Ahmad, H.R., & Shahid, M. (2015). Phytoremediation, soil remediation and plants. Elsevier Inc. Scholar
  76. Sarret, G., Balesdent, J., Bouziri, L., Garnier, J. M., Marcus, M. A., Geoffroy, N., Panfili, F., & Manceau, A. (2004). Zn speciation in the organic horizon of a contaminated soil by micro-X-ray fluorescence, micro- and power-EXAFS spectroscopy, and isotopic dilution. Environmental Science and Technology, 38, 2792–2801.CrossRefGoogle Scholar
  77. Savio, M., Cerutti, S., Martinez, L. D., Smichowski, P., & Gil, R. A. (2010). Study of matrix and spectral interferences in the determination of lead in sediments, sludges and soils by SR-ETAAS using slurry sampling. Talanta, 82, 523–527.CrossRefGoogle Scholar
  78. Schnürer, J., & Rosswall, T. (1982). Fluorescein diacetate hydrolysis as a measure of total microbial activity in soil and litter. Applied and Environmental Microbiology, 43, 1256–1261.Google Scholar
  79. Seshadri, B., Bolan, N. S., Choppala, G., Kunhikrishnan, A., Sanderson, P., Wang, H., Currie, L. D., Tsang, D., Ok, Y. S., & Kim, K. (2017). Potential value of phosphate compounds in enhancing immobilization and reducing bioavailability of mixed heavy metal contaminants in shooting range soil. Chemosphere, 184, 197–206.CrossRefGoogle Scholar
  80. Sfaxi-Bousbih, A., Chaoui, A., & El Ferjani, E. (2010). Cadmium impairs mineral and carbohydrate mobilization during the germination of bean seeds. Ecotoxicology and Environmental Safety, 73, 1123–1129.CrossRefGoogle Scholar
  81. Shafi, G., Ara, N., & Khan, F. U. (2014). The effect of seed priming and soaking durations with Di Ammonium Phosphate (DAP) on seedling emergence and morphological traits in okra (Hibiscus esculentus L.). International Journal of Environmental, 3, 113–125.CrossRefGoogle Scholar
  82. Siddique, A., & Prakash Dubey, A. (2017). Phyto-toxic effect of heavy metal (CdCl2) on seed germination, seedling growth and antioxidant defence metabolism in wheat (Triticum aestivum L.) variety HUW-234. International Journal of Bio-resource and Stress Management, 8, 261–267.CrossRefGoogle Scholar
  83. Srinivasarao, C., Gayatri, S. R., Venkateswarlu, B., Jakkula, V. S., Wani, S. P., Kundu, S., Sahrawat, K. L., Rajasekhara Rao, B. K., Marimuthu, S., & Krishna, G. G. (2014). Heavy metals concentration in soils under rainfed agro-ecosystems and their relationship with soil properties and management practices. International journal of Environmental Science and Technology, 11, 1959–1972.CrossRefGoogle Scholar
  84. Sterckeman, T., Douay, F., Proix, N., Fourrier, H., & Perdrix, E. (2002). Assessment of the contamination of cultivated soils by eighteen trace elements around smelters in the North of France. Water, Air and Soil Pollution, 135, 173–194.CrossRefGoogle Scholar
  85. Subin, M. P., & Steffy, F. (2013). Phytotoxic effects of cadmium on seed germination, early seedling growth and antioxidant enzyme activities in Cucurbita maxima Duchesne. International Research Journal of Biological Sciences, 2, 40–47.Google Scholar
  86. Sylvain, B., Mikael, M. H., Florie, M., Emmanuel, J., Marilyne, S., Sylvain, B., & Domenico, M. (2016). Phytostabilization of As, Sb and Pb by two willow species (S. viminalis and S. purpurea) on former mine technosols. Catena, 136, 44–52.CrossRefGoogle Scholar
  87. Thakur, S. K., Tomar, N. K., & Pandeya, S. B. (2006). Influence of phosphate on cadmium sorption by calcium carbonate. Geoderma, 130, 240–249.CrossRefGoogle Scholar
  88. Treeby, M., Marschner, H., & Romheld, V. (1989). Mobilization of iron and other micronutrient cations from a calcareous soil by plant-borne, microbial, and synthetic metal chelators. Plant and Soil, 114, 217–226.CrossRefGoogle Scholar
  89. Tripathy, D. K., Singh, V. P., Chauhan, D. K., Prasad, S. M., & Dubey, N. K. (2014). Role of macronutrients in plant growth and acclimation: recent advances and future prospective. In P. Ahmad, M. R. Wani, M. M. Azooz, & L.-S. P. Tran (Eds.), Improvement of crops in the era of climatic changes (pp. 197–216). New York: Springer.Google Scholar
  90. USEPA. (1996). Method 3050B: acid digestion of sediments, sludges, and soils, revision 2. DC: Washington.Google Scholar
  91. Wang, B., Xie, Z., Chen, J., Jiang, J., & Su, Q. (2008). Effects of field application of phosphate fertilizers on the availability and uptake of lead, zinc and cadmium by cabbage (Brassica chinensis L.) in a mining tailing contaminated soil. Journal of Environmental Science, 20, 1109–1117.CrossRefGoogle Scholar
  92. Wang, X., & Jia, Y. (2010). Study on adsorption and remediation of heavy metals by poplar and larch in contaminated soil. Environmental Science and Pollution Research, 17, 1331–1338.CrossRefGoogle Scholar
  93. Wang, W., Shi, J., Xie, Q., Jiang, Y., Yu, N., & Wang, E. (2017). Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Molecular Plant, 10, 1147–1158.CrossRefGoogle Scholar
  94. Waterlot, C., Bidar, G., Pruvot, C., & Douay, F. (2011b). Analysis of cadmium in water extracts from contaminated soils with high arsenic and iron concentration levels. Journal of Environmental Science and Engineering, 5, 271–280.Google Scholar
  95. Waterlot, C., & Douay, F. (2009). The problem of arsenic interference in the analysis of Cd to evaluate its extractability in soils contaminated by arsenic. Talanta, 80, 716–722.CrossRefGoogle Scholar
  96. Waterlot, C., Pelfrêne, A., & Douay, F. (2016). Determining the influence of the physicochemical parameters of urban soils on As availability using chemometric methods: a preliminary study. Journal of Environmental Sciences, 47, 183–192.CrossRefGoogle Scholar
  97. Waterlot, C., Pruvot, C., Ciesielski, H., & Douay, F. (2011a). Effects of a P amendment and the pH of water used for watering on the mobility and phytoavailability of Cd, Pb and Zn in highly contaminated kitchen garden soils. Ecological Engineering, 37, 1081–1093.CrossRefGoogle Scholar
  98. Waterlot, C., Pruvot, C., Marot, F., & Douay, F. (2017). Impact of a phosphate amendment on the environmental availability and phytoavailability of Cd and Pb in moderately and highly carbonated kitchen garden soils. Pedosphere, 27, 588–605.CrossRefGoogle Scholar
  99. Wolfe-Simon, F., Switzer Blum, J., Kulp, T. R., Gordon, G. W., Hoeft, S. E., Pett-Ridge, J., Stolz, J. F., Webb, S. M., Weber, P. K., Davies, P. C. W., Anbar, A. D., & Oremland, R. S. (2011). A bacterium that can grow by using arsenic instead of phosphorous. Science, 332, 1163–1166.CrossRefGoogle Scholar
  100. Xu, Y., Yan, X., Fan, L., & Fang, Z. (2016). Remediation of Cd (II)-contaminated soil by three kinds of ferrous phosphate nanoparticles. RSC Advances, 6, 17390–17395.CrossRefGoogle Scholar
  101. Yao, Z., Li, J., Xie, H., & Yu, C. (2012). Review on remediation technologies of soil contaminated by heavy metals. Procedia Environmental Sciences, 16, 722–729.CrossRefGoogle Scholar
  102. Yao, Q., Yang, R., Long, L., & Zhu, H. (2014). Phosphate application enhances the resistance of arbuscular mycorrhizae in clover plants to cadmium via polyphosphate accumulation in fungal hyphae. Environmental and Experimental Botany, 108, 63–70.CrossRefGoogle Scholar
  103. Zalewska, M. (2012). Response of perennial ryegrass (Lolium perenne L.) to soil contamination with zinc. Journal of Elementology, 329–343.Google Scholar
  104. Zeng, G., Wan, J., Huang, D., Hu, L., Huang, C., Cheng, M., Xu, W., Gong, X., Wang, R., & Jiang, D. (2017). Precipitation, adsorption and rhizosphere effect: the mechanisms for phosphate-induced Pb immobilization in soils—a review. Journal of Hazardous Materials, 339, 354–367.CrossRefGoogle Scholar
  105. Zengin, F. K., & Munzuroglu, O. (2005). Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (phaseolus vulgaris L.) seedlings. Acta Biologica Cracoviensia Series Botanica, 47, 157–164.Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Laboratoire Génie Civil et géoEnvironnement (LGCgE), Institut Supérieur d’AgricultureYncréa Hauts-de-FranceLille CedexFrance
  2. 2.Laboratoire de chimie durable et santé, Ecole des Hautes Etudes d’IngénieurYncréa Hauts-de-FranceLille CedexFrance
  3. 3.UNILEHAVRE, FR 3038 CNRS, URCOM EA 3221, UFR Sciences & TechniquesNormandie UniversitéLe Havre CedexFrance
  4. 4.Faculté de médecine – Pôle recherche Inserm U995, LIRIC, CHU de LilleUniversité de LilleLille CedexFrance
  5. 5.Faculty of Chemistry‘Alexandru Ioan Cuza’ University of IasiIasiRomania
  6. 6.Equipe Biotechnologie et Gestion des Agents Pathogènes en agriculture (BioGAP), Institut Supérieur d’AgricultureYncréa Hauts-de-FranceLille CedexFrance

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