Abstract
We propose to identify the influence of organic acids as well as total proteins in the accumulation and translocation of heavy metals from the rhizosphere to the plant organs of cultivated yellow melon var. Natal throughout the vegetative cycle. Physical and chemical attributes and the concentration of Cu, Zn, and Pb were determined in soil samples. Samples of plant tissue and rhizosphere at 0, 15, 30, 45, and 60 days after transplantation were collected and determined the concentration of heavy metals along with the content of total protein in the tissues and organic acids in the rhizosphere. Subsequently, the transfer factor (TF) and bioconcentration factor (BF) were calculated. Oxalic and citric acids and heavy metal contents were slightly higher in the rhizosphere than those found in the soil. The organic acids and total protein showed correlations with the concentration of heavy metals in different organs of the plant. The protein content in the plant tissues and the contents of oxalic and citric acid released by the plant in the rhizosphere can increase or decrease the absorption, accumulation, and translocation of Cu, Zn, and Pb in the different organs of the yellow melon var. Natal. Even the BF and TF showed values higher than one, being indicative of phytoextraction potential in several stages of the vegetative cycle for Cu and Zn, the yellow melon var. Natal cannot be considered as a hyperaccumulator plant for not meeting all necessary criteria for that purpose.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alloway, B. J., Jackson, A. P., & Morgan, H. (1990). The accumulation of cadmium by vegetables grown on soils contaminated from a variety of sources. The Science of the Total Environment, 91(C), 223–236. https://doi.org/10.1016/0048-9697(90)90300-J.
Arumugam, G., Rajendran, R., Ganesan, A., & Sethu, R. (2018). Bioaccumulation and translocation of heavy metals in mangrove rhizosphere sediments to tissues of Avicennia marina – A field study from tropical mangrove forest. Environmental Nanotechnology, Monitoring and Management, 10, 272–279. https://doi.org/10.1016/j.enmm.2018.07.005.
Ashraf, S., Ali, Q., Zahir, Z. A., Ashraf, S., & Asghar, H. N. (2019). Phytoremediation: Environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicology and Environmental Safety, 174, 714–727. https://doi.org/10.1016/j.ecoenv.2019.02.068.
Baker, A. J. M. (1989). Terrestrial higher plants which hyperaccumulate metallic elements - A review of their distribution. Ecology and Phytochemistry Biorecovery, 1, 81–126 Retrieved from https://www.researchgate.net/publication/247713966. Accessed 5 Nov 2019.
Baziramakenga, R., Simard, R. R., & Leroux, G. D. (1995). Determination of organic acids in soil extracts by ion chromatography. Soil Biology and Biochemistry, 27(3), 349–356. https://doi.org/10.1016/0038-0717(94)00178-4.
Bonanno, G., Borg, J. A., & Di Martino, V. (2017). Levels of heavy metals in wetland and marine vascular plants and their biomonitoring potential: A comparative assessment. Science of the Total Environment, 576, 796–806. https://doi.org/10.1016/j.scitotenv.2016.10.171.
Bose, S., Chandrayan, S., Rai, V., Bhattacharyya, A. K., & Ramanathan, A. (2008). Translocation of metals in pea plants grown on various amendment of electroplating industrial sludge. Bioresource Technology, 99(10), 4467–4475. https://doi.org/10.1016/j.biortech.2007.08.020.
Cecchi, H. M. (2003). Fundamentos teóricos e práticos em análise de alimentos. 2°ed.rev. Campinas: Editora Unicamp.
Chandra, R., Yadav, S., & Yadav, S. (2017). Phytoextraction potential of heavy metals by native wetland plants growing on chlorolignin containing sludge of pulp and paper industry. Ecological Engineering, 98, 134–145. https://doi.org/10.1016/j.ecoleng.2016.10.017.
Chandrasekhar, C., & Ray, J. G. (2019). Lead accumulation, growth responses and biochemical changes of three plant species exposed to soil amended with different concentrations of lead nitrate. Ecotoxicology and Environmental Safety, 171, 26–36. https://doi.org/10.1016/j.ecoenv.2018.12.058.
Chen, Q., Lu, X., Guo, X., Pan, Y., Yu, B., Tang, Z., & Guo, Q. (2018). Differential responses to Cd stress induced by exogenous application of Cu, Zn or Ca in the medicinal plant Catharanthus roseus. Ecotoxicology and Environmental Safety, 157, 266–275. https://doi.org/10.1016/j.ecoenv.2018.03.055.
Chen, X. W., Wu, L., Luo, N., Mo, C. H., Wong, M. H., & Li, H. (2019). Arbuscular mycorrhizal fungi and the associated bacterial community influence the uptake of cadmium in rice. Geoderma, 337, 749–757. https://doi.org/10.1016/j.geoderma.2018.10.029.
Cheng, S., Lin, Q., Wang, Y., Luo, H., Huang, Z., Fu, H., Chen, H., & Xiao, R. (2020). The removal of Cu, Ni, and Zn in industrial soil by washing with EDTA-organic acids. Arabian Journal of Chemistry, 13(4), 5160–5170. https://doi.org/10.1016/j.arabjc.2020.02.015.
De Araújo, J. D. C. T., & Do Nascimento, C. W. A. (2010). Phytoextraction of lead from soil from a battery recycling site: The use of citric acid and NTA. Water, Air, and Soil Pollution, 211(1–4), 113–120. https://doi.org/10.1007/s11270-009-0285-4.
Do Nascimento, C. W. A., Hesterberg, D., Tappero, R., Nicholas, S., & da Silva, F. B. V. (2020). Citric acid-assisted accumulation of Ni and other metals by Odontarrhena muralis: Implications for phytoextraction and metal foliar distribution assessed by μ-SXRF. Environmental Pollution, 260, 114025. https://doi.org/10.1016/j.envpol.2020.114025.
Dos Santos, J. S., dos Santos, M. L. P., Conti, M. M., dos Santos, S. N., & de Oliveira, E. (2009). Evaluation of some metals in Brazilian coffees cultivated during the process of conversion from conventional to organic agriculture. Food Chemistry, 115(4), 1405–1410. https://doi.org/10.1016/j.foodchem.2009.01.069.
EMBRAPA. (2017). Manual de métodos de análise de solo. 3.ed. rev. e ampl. Brasília: Embrapa. 573 p.
Fitz, W. J., & Wenzel, W. W. (2002). Arsenic transformations in the soil-rhizosphere-plant system: Fundamentals and potential application to phytoremediation. Journal of Biotechnology, 99(3), 259–278. https://doi.org/10.1016/S0168-1656(02)00218-3.
Funceme - Fundação Cearense de Meteorologia e Recursos Hídricos - Chuvas Diárias. (2019). Retrieved December 9, 2019, from http://www3.funceme.br/index.php/areas/23-monitoramento/meteorológico/406-chuvas-diárias.
Gee, G. W., & Bauder, J. W. (1986). Particle-size analysis. In A. Klute (Ed.), Methods of soil analysis. Part 1: Physical and mineralogical methods (pp. 383–412). Madison, Soil Science Society of America. https://doi.org/10.2136/sssabookser5.1.2ed.c15
Gessesse, T. A., & Khamzina, A. (2018). How reliable is the Walkley-Black method for analyzing carbon-poor, semi-arid soils in Ethiopia? Journal of Arid Environments, 153, 98–101. https://doi.org/10.1016/j.jaridenv.2018.01.008.
Guo, L., Cutright, T. J., & Duirk, S. (2015). Effect of citric acid, rhizosphere bacteria, and plant age on metal uptake in reeds cultured in acid mine drainage. Water, Air, and Soil Pollution, 226(1), 2264. https://doi.org/10.1007/s11270-014-2264-7.
Instituto de Pesquisa e Estratégia Econômica do Ceará (IPECE). (2007) Ceará em Mapas. Disponível em: <http://www2.ipece.ce.gov.br/atlas/> Accessed in fev 2018.
Jain, S., Muneer, S., Guerreiro, G., Liu, S., Vishwakarma, K., Chauhan, D. K., Dubey, N. K., Tripathi, D. K., & Sharma, S. (2018). Tracing the role of plant proteins in the response to metal toxicity: A comprehensive review. Plant Signaling & Behavior, 13(9), e1507401. https://doi.org/10.1080/15592324.1507401.
Jones, D. L. (1998). Organic acids in the rhizosphere – A critical review. Plant and Soil, 205, 25–44. https://doi.org/10.1023/A:1004356007312.
Liang, C., Xiao, H., Hu, Z., Zhang, X., & Hu, J. (2018). Uptake, transportation, and accumulation of C60 fullerene and heavy metal ions (Cd, Cu, and Pb) in rice plants grown in an agricultural soil. Environmental Pollution, 235, 330–338. https://doi.org/10.1016/j.envpol.2017.12.062.
Ma, H., Li, X., Hou, S., Peng, D., Wang, Y., Xu, F., & Xu, H. (2019). The activation and extraction systems using organic acids and Lentinus edodes to remediate cadmium contaminated soil. Environmental Pollution, 255. https://doi.org/10.1016/j.envpol.2019.113252.
Ma, H., Li, X., Wei, M., Zeng, G., Hou, S., Li, D., & Xu, H. (2020). Elucidation of the mechanisms into effects of organic acids on soil fertility, cadmium speciation and ecotoxicity in contaminated soil. Chemosphere, 239. https://doi.org/10.1016/j.chemosphere.2019.124706.
Mallek-Ayadi, S., Bahloul, N., & Kechaou, N. (2018). Chemical composition and bioactive compounds of Cucumis melo L. seeds: Potential source for new trends of plant oils. Process Safety and Environmental Protection, 113, 68–77. https://doi.org/10.1016/j.psep.2017.09.016.
Marschner, H. (1995). Functions of mineral nutrients: Macronutrients. In H. Marschner (Ed.), Mineral nutrition of higher plants (pp. 299–312). New York: Academic Press.
Marta, J., Rorat, A., & Grobelak, A. (2019). Enzymatic assays confirm the toxicity reduction after manure treatment of heavy metals contaminated soil. South African Journal of Botany, 124, 47–53. https://doi.org/10.1016/j.sajb.2019.04.035.
Mathivanan, K., & Rajaram, R. (2014). Tolerance and biosorption of cadmium (II) ions by highly cadmium resistant bacteria isolated from industrially polluted estuarine environment. Indian Journal of Geo-Marine Sciences, 43(4), 580–588.
Mench, M., Morel, J. L., & Guekert, A. (1987). A. Metal binding properties of high molecular weight soluble exudates from maize (Zea mays L.) roots. Biology and Fertility of Soils, 123(3), 165-169. https://doi.org/10.1016/B978-0-12-325550-1.50007-0.
Mench, M., Morel, J. L., Guckert, A., & Guillet, B. (1988). Metal binding with root exudates of low molecular weight. Journal of Soil Science, 39(4), 521–527. https://doi.org/10.1111/j.1365-2389.1988.tb01236.x.
Miyazawa, M., Pavan, M., Muraoka, T., Carmo, C. A. F. S., & Mello, W. J. (2009). Análise química de tecido vegetal. In Fabio Cesar da Silva (Ed.), Manual de análises químicas de solos, plantas e fertilizantes (Vol. 1, 2nd ed., pp. 191–234). Brasília: Embrapa Informação Tecnológica.
Montiel-Rozas, M. M., Madejón, E., & Madejón, P. (2016). Effect of heavy metals and organic matter on root exudates (low molecular weight organic acids) of herbaceous species: An assessment in sand and soil conditions under different levels of contamination. Environmental Pollution, 216, 273–281. https://doi.org/10.1016/j.envpol.2016.05.080.
Otero, X. L., Álvarez, E., Fernández-Sanjurjo, M. J., & Macías, F. (2012). Micronutrients and toxic trace metals in the bulk and rhizospheric soil of the spontaneous vegetation at an abandoned copper mine in Galicia (NW Spain). Journal of Geochemical Exploration, 112, 84–92. https://doi.org/10.1016/j.gexplo.2011.07.007.
Piri, M., Sepehr, E., & Rengel, Z. (2019). Citric acid decreased and humic acid increased Zn sorption in soils. Geoderma, 341, 39–45. https://doi.org/10.1016/j.geoderma.2018.12.027.
Qiao, D., Lu, H., & Zhang, X. (2020). Change in phytoextraction of Cd by rapeseed (Brassica napus L.) with application rate of organic acids and the impact of Cd migration from bulk soil to the rhizosphere. Environmental Pollution, 267, 115452. https://doi.org/10.1016/j.envpol.2020.115452.
Raimundo, J., Vale, C., Duarte, R., & Moura, I. (2010). Association of Zn, Cu, Cd and Pb with protein fractions and sub-cellular partitioning in the digestive gland of Octopus vulgaris living in habitats with different metal levels. Chemosphere, 81(10), 1314–1319. https://doi.org/10.1016/j.chemosphere.2010.08.029.
Rauser, W. E. (1999). Structure and function of metal chelator produced by plants. Cell Biochemistry and Biophysics, 31(1), 19–48. https://doi.org/10.1007/BF02738153.
Rosselli, W., Keller, C., & Boschi, K. (2003). Phytoextraction capacity of trees growing on a metal contaminated soil. Plant and Soil, 256(2), 265–272. https://doi.org/10.1023/A:1026100707797.
Schwab, A. P., Zhu, D. S., & Banks, M. K. (2008). Influence of organic acids on the transport of heavy metals in soil. Chemosphere, 72(6), 986–994. https://doi.org/10.1016/j.chemosphere.2008.02.047.
Seshadri, B., Bolan, N. S., & Naidu, R. (2015). Rhizosphere-induced heavy metal(oid) transformation in relation to bioavailability and remediation. Journal of Soil Science and Plant Nutrition, 15(2), 524–548. https://doi.org/10.4067/S0718-95162015005000043.
Silva, M. A., Albuquerque, T. G., Alves, R. C., Oliveira, M. B. P. P., & Costa, H. S. (2018). Melon (Cucumis melo L.) by-products: Potential food ingredients for novel functional foods? Trends in Food Science and Technology. https://doi.org/10.1016/j.tifs.2018.07.005.
Sorrentino, M. C., Capozzi, F., Amitrano, C., Giordano, S., Arena, C., & Spagnuolo, V. (2018). Performance of three cardoon cultivars in an industrial heavy metal-contaminated soil: Effects on morphology, cytology and photosynthesis. Journal of Hazardous Materials, 351, 131–137. https://doi.org/10.1016/j.jhazmat.2018.02.044.
Suanon, F., Sun, Q., Dimon, B., Mama, D., & Yu, C. P. (2016). Heavy metal removal from sludge with organic chelators: Comparative study of N, N-bis (carboxymethyl) glutamic acid and citric acid. Journal of Environmental Management, 166, 341–347. https://doi.org/10.1016/j.jenvman.2015.10.035.
Van der Ent, A., Baker, A. J. M., Reeves, R. D., Pollard, A. J., & Schat, H. (2013). Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant and Soil, 362, 319e334. https://doi.org/10.1007/s11104-012-1287-3.
Wang, Z., Liu, X., & Qin, H. (2019). Bioconcentration and translocation of heavy metals in the soil-plants system in Machangqing copper mine, Yunnan Province, China. Journal of Geochemical Exploration, 200, 159–166. https://doi.org/10.1016/J.GEXPLO.2019.02.005.
Yang, X., Liu, L., Tan, W., Liu, C., Dang, Z., & Qiu, G. (2020). Remediation of heavy metal contaminated soils by organic acid extraction and electrochemical adsorption. Environmental Pollution, 264, 114745. https://doi.org/10.1016/j.envpol.2020.114745.
Yoon, J., Cao, X., Zhou, Q., & Ma, L. Q. (2006). Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Science of the Total Environment, 368(2–3), 456–464. https://doi.org/10.1016/j.scitotenv.2006.01.016.
Acknowledgments
We are grateful to OEA (Organization of American States) and to CAPES (Brazilian Federal Agency for Support and Evaluation of Graduate Education) for the scholarship granting to the authors, to the “Pró-Integração” project 55/2013 for partially funding this research, to the Graduate Program in Soil Science of the Federal University of Ceará, to Soil Quality and Environmental Chemistry Research Group—QSQA, and to the Fazenda Agrícola Famosa.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Irias Zelaya, C., Gadelha, J.C., Hernandez, F.F.F. et al. Heavy Metals Behavior in the Presence of Organic Acids and Proteins in the Rhizosphere and Plant Tissues of Yellow Melon var. Natal (Cucumis melo L.) Cultivated in a Quartzarenic Neosol. Water Air Soil Pollut 231, 572 (2020). https://doi.org/10.1007/s11270-020-04931-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-020-04931-1