Advertisement

Brassica napus Growth in Lead-Polluted Soil: Bioaccumulation in Plant Organs at Different Ontogenetic Stages and Lead Fractionation in Soil

  • Gisele V. Ferreyroa
  • Jonathan Gelma
  • Mariana D. Sosa
  • Marcos A. Orellana Benitez
  • Mabel B. Tudino
  • Raúl S. Lavado
  • Fernando V. Molina
Article

Abstract

Lead is known to be a highly toxic metal; it is often found in soils with the potential to be incorporated by plants. Here, the bioaccumulation of lead by rapeseed (Brassica napus) from a soil with Pb(II) added just before sowing is studied. The effect on plant organs is also studied at the ontogenetic stages of flowering and physiological maturity. Moreover, the chemical fractionation of Pb in the rhizosphere and bulk soil portions is investigated and related to Pb accumulation in plant organs. B. napus are found to accumulate Pb in its organs: 1.5–19.6 mg kg−1 in roots, 3.3–15.6 mg kg−1 in stems, 0.5–8.6 mg kg−1 in leaves in all treatments, and in grains 1.45 mg kg−1 at physiological maturity and only for the highest Pb dose (200 mg kg−1). Plant biomass reduction was observed to be about 20% at the flowering stage and only for the highest Pb dose. The analysis of metal fractionation in soil shows Pb migration from the bulk soil to the rhizosphere, attributed to concentration gradients created by root intake. Along the time period studied, lead chemical fractionation in soil evolved toward the most stable fractions, which coupled to plant uptake depleted the soluble/exchangeable one (assumed bioavailable).

Keywords

Lead bioaccumulation Flowering Physiological maturity Rhizosphere Plant lead translocation 

Notes

Acknowledgments

The authors gratefully acknowledge financial support from the Universidad de Buenos Aires, Argentina (grant 20020130100035BA), the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, grant PIP F57269), and the Agencia Nacional de Promoción Científica y Tecnológica, Argentina (grant PICT 2014-2289). The authors are indebted to Dr. M. A. Trinelli and Dr. N. Verrengia Guerrero for help with the analytical determinations. M. B. T., R. S. L., and F. V. M. are members of the Carrera del Investigador Científico of CONICET.

Supplementary material

11270_2018_3851_MOESM1_ESM.pdf (752 kb)
ESM 1 (PDF 751 kb)

References

  1. Adams, N., Carroll, D., Madalinski, K., Rock, S., Wilson, T., & Pivetz, B. (2000). Introduction to phytoremediation. Cincinnati: USEPA.Google Scholar
  2. Arrouays, D., Mench, M., Gomez, A., & Amans, V. (1996). Short-range variability of fallout Pb in a contaminated soil. Canadian Journal of Soil Science, 76(1), 73–81.  https://doi.org/10.4141/cjss96-011.CrossRefGoogle Scholar
  3. Azimzadeh, Y., Shirvani, M., & Shariatmadari, H. (2014). Green manure and overlapped rhizosphere effects on Pb chemical forms in soil and plant uptake in maize/canola intercrop systems: a Rhizobox study. Soil and Sediment Contamination: An International Journal, 23(6), 677–690.  https://doi.org/10.1080/15320383.2014.861795.CrossRefGoogle Scholar
  4. Bharagava, R. N., Chandra, R., & Rai, V. (2008). Phytoextraction of trace elements and physiological changes in Indian mustard plants (Brassica nigra L.) grown in post methanated distillery effluent (PMDE) irrigated soil. Bioresource Technology, 99(17), 8316–8324.  https://doi.org/10.1016/j.biortech.2008.03.002.CrossRefGoogle Scholar
  5. Bilal Shakoor, M., Ali, S., Hameed, A., Farid, M., Hussain, S., Yasmeen, T., et al. (2014). Citric acid improves lead (Pb) phytoextraction in Brassica napus L. by mitigating Pb-induced morphological and biochemical damages. Ecotoxicology and Environmental Safety, 109, 38–47.  https://doi.org/10.1016/j.ecoenv.2014.07.033.CrossRefGoogle Scholar
  6. Brunetti, G., Farrag, K., Rovira, P. S., Nigro, F., & Senesi, N. (2011). Greenhouse and field studies on Cr, Cu, Pb and Zn phytoextraction by Brassica napus from contaminated soils in the Apulia region, Southern Italy. Geoderma, 160(3), 517–523.CrossRefGoogle Scholar
  7. Cartier, C., Doré, E., Laroche, L., Nour, S., Edwards, M., & Prévost, M. (2013). Impact of treatment on Pb release from full and partially replaced harvested lead service lines (LSLs). Water Research, 47(2), 661–671.  https://doi.org/10.1016/j.watres.2012.10.033.CrossRefGoogle Scholar
  8. Ferreyra, H., Romano, M., & Uhart, M. (2009). Recent and chronic exposure of wild ducks to lead in human-modified wetlands in Santa Fe Province, Argentina. Journal of Wildlife Diseases, 45(3), 823–827.CrossRefGoogle Scholar
  9. Ferreyroa, G. V., Montenegro, A. C., Tudino, M. B., Lavado, R. S., & Molina, F. V. (2014). Time evolution of Pb(II) speciation in pampa soil fractions. Chemical Speciation and Bioavailability, 26(4), 210–218.CrossRefGoogle Scholar
  10. Ferreyroa, G. V., Lagorio, M. G., Trinelli, M. A., Lavado, R. S., & Molina, F. V. (2017). Lead effects on brassica napus photosynthetic organs. Ecotoxicology and Environmental Safety, 140, 123–130.  https://doi.org/10.1016/j.ecoenv.2017.02.031.CrossRefGoogle Scholar
  11. Gonzalez, J., Cruzate, G. G., & Panigatti, J. L. (2013). Suelos de la costa NE del Río Paraná (prov. de Bs. As.) (1a.). San Pedro, pcia. Bs. As., Argentina: INTA ediciones.Google Scholar
  12. Hass, A., & Fine, P. (2010). Sequential selective extraction procedures for the study of heavy metals in soils, sediments, and waste materials—a critical review. Critical Reviews in Environmental Science and Technology, 40(5), 365–399.  https://doi.org/10.1080/10643380802377992.CrossRefGoogle Scholar
  13. Hinsinger, P., Gobran, G. R., Gregory, P. J., & Wenzel, W. W. (2005). Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes: a research review. New Phytologist, 168(2), 293–303.  https://doi.org/10.1111/j.1469-8137.2005.01512.x.CrossRefGoogle Scholar
  14. Hlavay, J., Prohaska, T., Weisz, M., Wenzel, W. W., & Stingeder, G. J. (2004). Determination of trace elements bound to soils and sediment fractions: (IUPAC Technical Report). Pure and Applied Chemistry, 76(2), 415–442.CrossRefGoogle Scholar
  15. Karak, T., Bhattacharyya, P., Kumar Paul, R., & Das, D. K. (2013). Metal accumulation, biochemical response, and yield of Indian mustard grown in soil amended with rural roadside pond sediment. Ecotoxicology and Environmental Safety, 92, 161–173.  https://doi.org/10.1016/j.ecoenv.2013.03.019.CrossRefGoogle Scholar
  16. Khan, S., Cao, Q., Chen, B., & Zhu, Y.-G. (2006). Humic acids increase the phytoavailability of Cd and Pb to wheat plants cultivated in freshly spiked, contaminated soil (7 pp). Journal of Soils and Sediments, 6(4), 236–242.  https://doi.org/10.1065/jss2006.08.178.CrossRefGoogle Scholar
  17. Kim, K.-R., Owens, G., & Kwon, S. (2010). Influence of Indian mustard (Brassica juncea) on rhizosphere soil solution chemistry in long-term contaminated soils: a rhizobox study. Journal of Environmental Sciences, 22(1), 98–105.  https://doi.org/10.1016/S1001-0742(09)60080-2.CrossRefGoogle Scholar
  18. Lavado, R. S., Rodríguez, M. S., Scheiner, J. D., Taboada, M. A., Rubio, G., Alvarez, R., et al. (1998). Heavy metals in soils of Argentina: comparison between urban and agricultural soils. Communications in Soil Science and Plant Analysis, 29(11–14), 1913–1917.CrossRefGoogle Scholar
  19. Lavado, R. S., Zubillaga, M. S., Alvarez, R., & Taboada, M. A. (2004). Baseline levels of potentially toxic elements in pampas soils. Soil and Sediment Contamination: An International Journal, 13(5), 329–339.  https://doi.org/10.1080/10588330490500383.CrossRefGoogle Scholar
  20. Lavado, R. S., Rodríguez, M., Alvarez, R., Taboada, M. A., & Zubillaga, M. S. (2007). Transfer of potentially toxic elements from biosolid-treated soils to maize and wheat crops. Agriculture. Ecosystems and Environment, 118(1–4), 312–318.  https://doi.org/10.1016/j.agee.2006.06.001.CrossRefGoogle Scholar
  21. Liu, D., Jiang, W., Liu, C., Xin, C., & Hou, W. (2000). Uptake and accumulation of lead by roots, hypocotyls, and shoots of Indian mustard [Brassica juncea (L.)]. Bioresource Technology, 71(3), 273–277.CrossRefGoogle Scholar
  22. Ma, Y. B., & Uren, N. C. (1998). Transformations of heavy metals added to the soil—application of a new sequential extraction procedure. Geoderma, 84(1–3), 157–168.  https://doi.org/10.1016/S0016-7061(97)00126-2.CrossRefGoogle Scholar
  23. Magrisso, S., Belkin, S., & Erel, Y. (2009). Lead bioavailability in soil and soil components. Water, Air, and Soil Pollution, 202(1–4), 315–323.  https://doi.org/10.1007/s11270-009-9978-y.CrossRefGoogle Scholar
  24. McBride, M. B., Shayler, H. A., Russell-Anelli, J. M., Spliethoff, H. M., & Marquez-Bravo, L. G. (2015). Arsenic and lead uptake by vegetable crops grown on an old orchard site amended with compost. Water, Air, and Soil Pollution, 226(8), 1–10.  https://doi.org/10.1007/s11270-015-2529-9.CrossRefGoogle Scholar
  25. Miralles, D. J., Windauer, L. B., & Gómez, N. V. (2003). Factores que regulan el desarrollo de los cultivos de granos. In E. H. Satorre, R. L. Benech Arnold, G. A. Slafer, E. B. de la Fuente, D. J. Miralles, M. E. Otegui, & R. Savin (Eds.), Producción de Granos. Bases Funcionales para su Manejo. Buenos Aires: Editorial Facultad de Agronomía.Google Scholar
  26. Molina, F. V. (2013). Soil colloids: Properties and ion binding. Boca Raton: CRC Press.CrossRefGoogle Scholar
  27. Needleman, H. (2004). Lead poisoning. Annual Review of Medicine, 55(1), 209–222.  https://doi.org/10.1146/annurev.med.55.091902.103653.CrossRefGoogle Scholar
  28. Rodriguez, J. H., Salazar, M. J., Steffan, L., Pignata, M. L., Franzaring, J., Klumpp, A., & Fangmeier, A. (2014). Assessment of Pb and Zn contents in agricultural soils and soybean crops near to a former battery recycling plant in Córdoba, Argentina. Journal of Geochemical Exploration, 145, 129–134.  https://doi.org/10.1016/j.gexplo.2014.05.025.CrossRefGoogle Scholar
  29. Salazar, M. J., Rodriguez, J. H., Nieto, G. L., & Pignata, M. L. (2012). Effects of heavy metal concentrations (Cd, Zn, and Pb) in agricultural soils near different emission sources on quality, accumulation and food safety in soybean [Glycine max (L.) Merrill]. Journal of Hazardous Materials, 233–234, 244–253.  https://doi.org/10.1016/j.jhazmat.2012.07.026.CrossRefGoogle Scholar
  30. Salazar, M. J., Rodriguez, J. H., Cid, C. V., & Pignata, M. L. (2016). Auxin effects on Pb phytoextraction from polluted soils by Tegetes minuta L. and Bidens pilosa L.: the extractive power of their root exudates. Journal of Hazardous Materials, 311, 63–69.  https://doi.org/10.1016/j.jhazmat.2016.02.053.CrossRefGoogle Scholar
  31. Shahid, M., Pinelli, E., & Dumat, C. (2012). Review of Pb availability and toxicity to plants in relation to metal speciation; the role of synthetic and natural organic ligands. Journal of Hazardous Materials, 219–220, 1–12.  https://doi.org/10.1016/j.jhazmat.2012.01.060.CrossRefGoogle Scholar
  32. Shrivastava, S. K., & Banerjee, D. K. (2004). Speciation of metals in sewage sludge and sludge-amended soils. Water, Air, and Soil Pollution, 152(1–4), 219–232.  https://doi.org/10.1023/B:WATE.0000015364.19974.36.CrossRefGoogle Scholar
  33. Silva Gonzaga, M. I., Santos, J. A. G., & Ma, L. Q. (2006). Arsenic chemistry in the rhizosphere of Pteris vittata L. and Nephrolepis exaltata L. Environmental Pollution, 143(2), 254–260.  https://doi.org/10.1016/j.envpol.2005.11.037.CrossRefGoogle Scholar
  34. Slafer, G. A. (Ed.). (1993). Genetic improvement of field crops. New York: CRC Press.Google Scholar
  35. Smolders, E., Oorts, K., Peeters, S., Lanno, R., & Cheyns, K. (2015). Toxicity in lead salt spiked soils to plants, invertebrates, and microbial processes: unraveling effects of acidification, salt stress, and aging reactions. Science of the Total Environment, 536, 223–231.  https://doi.org/10.1016/j.scitotenv.2015.07.067.CrossRefGoogle Scholar
  36. Sparks, D. L. (2002). Environmental soil chemistry (2nd ed.). San Diego: Academic Press.Google Scholar
  37. Tessier, A., Campbell, P. G. C., & Bisson, M. (1979). Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry, 51(7), 844–851.  https://doi.org/10.1021/ac50043a017.CrossRefGoogle Scholar
  38. Thomas, G. W. (1996). Soil pH and soil acidity. In D. L. Sparks (Ed.), Methods of soil analysis. Part 3. Chemical methods (pp. 475–490). Madison: American Society of Agronomy-Soil Science Society of America.Google Scholar
  39. Tu, C., Ma, L. Q., & Bondada, B. (2002). Arsenic accumulation in the hyperaccumulator Chinese brake and its utilization potential for phytoremediation. Journal of Environment Quality, 31(5), 1671.  https://doi.org/10.2134/jeq2002.1671.CrossRefGoogle Scholar
  40. Wang, Z., Shan, X., & Zhang, S. (2002). Comparison between fractionation and bioavailability of trace elements in rhizosphere and bulk soils. Chemosphere, 46(8), 1163–1171.  https://doi.org/10.1016/S0045-6535(01)00206-5.CrossRefGoogle Scholar
  41. Wong, C. S. C., Li, X., & Thornton, I. (2006). Urban environmental geochemistry of trace metals. Environmental Pollution, 142(1), 1–16.  https://doi.org/10.1016/j.envpol.2005.09.004.CrossRefGoogle Scholar
  42. Wright, R. J., & Stuczynski, T. (1996). Atomic absorption and flame emission spectrometry. In D. L. Sparks (Ed.), Methods of soil analysis. Part 3. Chemical methods (pp. 65–90). Madison: American Society of Agronomy-Soil Science Society of America.Google Scholar
  43. Yang, J., Hu, S., Chen, X., Yu, M., Liu, J., Li, H., et al. (2010). Transformation of lead solid fraction in the rhizosphere of Elsholtzia splendens: the importance of organic matter. Water, Air, and Soil Pollution, 205(1–4), 333–342.  https://doi.org/10.1007/s11270-009-0077-x.CrossRefGoogle Scholar
  44. Youssef, R. A., & Chino, M. (1989). Root-induced changes in the rhizosphere of plants. I. pH changes in relation to the bulk soil. Soil Science and Plant Nutrition, 35(3), 461–468.  https://doi.org/10.1080/00380768.1989.10434779.CrossRefGoogle Scholar
  45. Yu, R., Ji, J., Yuan, X., Song, Y., & Wang, C. (2012). Accumulation and translocation of heavy metals in the canola (Brassica napus L.)—soil system in Yangtze River Delta, China. Plant and Soil, 1–13.Google Scholar
  46. Zanetti, F., Monti, A., & Berti, M. T. (2013). Challenges and opportunities for new industrial oilseed crops in EU-27: a review. Industrial Crops and Products, 50, 580–595.  https://doi.org/10.1016/j.indcrop.2013.08.030.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Química Física de Materiales, Ambiente y Energía (INQUIMAE), Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina
  2. 2.Área de Contaminación y Bioindicadores - IMBIV-CONICET Cátedra de Química General - FCEFyN – UNCCórdobaArgentina
  3. 3.Instituto de Investigaciones en Biociencias Agrícolas y Ambientales (INBA), Facultad de AgronomíaUniversidad de Buenos AiresBuenos AiresArgentina

Personalised recommendations