The benefit of the Arabidopsis halleri ssp. gemmifera root exudate in cadmium extraction from the cadmium contaminated soil
DOI:
https://doi.org/10.15243/jdmlm.2023.102.4107Keywords:
Arabidopsis halleri ssp., cadmium, phytoremediation, root exudate, soil leachingAbstract
This study focuses on how to solve cadmium (Cd) contamination in soil because this contaminant decreases soil quality. Soil remediation using the hyperaccumulator plants is an optional process to solve soil contamination. Arabidopsis halleri ssp. gemmifera (hereinafter referred to as A. halleri), is one of the candidate plants expected to be used for phytoremediation of Cd contaminated soil. The A. halleri promote solubilization of Cd in the soil directly or indirectly using its secreted root exudate. However, the effect of the metabolites profile of this plant to Cd uptake from contaminated soil is still unclear. The purpose of this study is to examine the contribution of root exudates of A. halleri to extract Cd in the soil. Cd-contaminated soil used in this study was a farmland soil containing 5.8 mg kg-1 of Cd and 648 mg kg-1 of Zn taken from Tome City, Miyagi Prefecture, Japan. Soil leaching tests were conducted using the solution containing the root exudates from A. halleri plant. The accelerating effect of root exudates of A. halleri on solubilization of Cd is fundamental information to construct the benefit of phytoremediation.
References
Abedi, T. and Mojiri, A. 2020. Cadmium uptake by wheat (Triticum aestivum L.): an overview. Plants 9(4):1-14, doi:10.3390/plants9040500.
Alaboudi, K.A., Ahmed, B. and Brodie, G. 2020. Soil washing technology for removing heavy metals from a contaminated soil: a case study. Polish Journal of Environmental Studies 29(2):1029-1036, doi:10.15244/pjoes/104655.
Andrunik, M., Wołowiec, M., Wojnarski, D., Zelek-Pogudz, S. and Bajda, T. 2020. Transformation of Pb, Cd, and Zn minerals using phosphates. Minerals 10(4):342, doi:10.3390/min10040342.
Azzi, V., Kanso, A., Kazpard, V., Kobeissi, A., Lartiges, B. and El Samrani, A. 2017. Lactuca sativa growth in compacted and non-compacted semi-arid alkaline soil under phosphate fertilizer treatment and cadmium contamination. Soil and Tillage Research 165:1-10, doi:10.1016/j.still.2016.07.014.
Barceló, J. and Poschenrieder, C. 2002. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environmental and Experimental Botany 48(1):75-92, doi:10.1016/S0098-8472(02)00013-8.
Bilgin, M. and Tulun, S. 2016. Removal of heavy metals (Cu, Cd and Zn) from contaminated soils using EDTA and FeCl3. Global Nest Journal 18(1):98-107, doi:10.30955/gnj.001732.
Canarini, A., Kaiser, C., Merchant, A., Richter, A. and Wanek, W. 2019. Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Frontiers in Plant Science 10:157, doi:10.3389/fpls.2019.00157.
Chang, H.F., Wang, S.L., Lee, D.C., Hsiao, S.S.Y., Hashimoto, Y. and Yeh, K.C. 2020. Assessment of indium toxicity to the model plant Arabidopsis. Journal of Hazardous Materials 387(October 2019):121983, doi:10.1016/j.jhazmat.2019.121983.
Dresler, S., Hanaka, A., Bednarek, W. and Maksymiec, W. 2014. Accumulation of low-molecular-weight organic acids in roots and leaf segments of Zea mays plants treated with cadmium and copper. Acta Physiologiae Plantarum 36(6):1565-1575, doi:10.1007/s11738-014-1532-x.
Fukuda, N., Kitajima, N., Terada, Y., Abe, T., Nakai, I. and Hokura, A. 2020. Visible cellular distribution of cadmium and zinc in the hyperaccumulator: Arabidopsis halleri ssp. gemmifera determined by 2-D X-ray fluorescence imaging using high-energy synchrotron radiation. Metallomics 12(2):193-203, doi:10.1039/c9mt00243j.
Guo, S.H., Hu, N., Li, Q.S., Yang, P., Wang, L.L., Xu, Z. M., Chen, H.J., He, B.Y., and Zeng, E.Y. 2018. Response of edible amaranth cultivar to salt stress led to Cd mobilization in rhizosphere soil: A metabolomic analysis. Environmental Pollution 241:422-431, doi:10.1016/j.envpol.2018.05.018.
Hamid, Y., Tang, L., Hussain, B., Usman, M., Lin, Q., Rashid, M.S., He, Z. and Yang, X. 2020. Organic soil additives for the remediation of cadmium contaminated soils and their impact on the soil-plant system: a review. Science of the Total Environment 707:136121, doi:10.1016/j.scitotenv.2019.136121.
He, S., Yang, X., He, Z. and Baligar, V.C. 2017. Morphological and physiological responses of plants to cadmium toxicity: a review. Pedosphere 27(3):421-438, doi:10.1016/S1002-0160(17)60339-4.
He, W., Long, A., Zhang, C., Cao, M. and Luo, J. 2021. Mass balance of metals during the phytoremediation process using Noccaea caerulescens: a pot study. Environmental Science and Pollution Research 28(7):8476-8485, doi:10.1007/s11356-020-11216-x.
Hinsinger, P., Gobran, G.R., Gregory, P.J. and Wenzel, W.W. 2005. Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytologist 168(2):293-303, doi:10.1111/j.1469-8137.2005.01512.x.
Hokura, A., Onuma, R., Kitajima, N., Terada, Y., Saito, H., Abe, T., Yoshida, S. and Nakai, I. 2006. 2-D X-ray fluorescence imaging of cadmium hyperaccumulating plants by using high-energy synchrotron radiation X-ray microbeam. Chemistry Letters 35(11):1246-1247, doi:10.1246/cl.2006.1246.
Hussain, B., Li, J., Ma, Y., Tahir, N. and Ullah, A. 2020. Effects of Fe and Mn cations on Cd uptake by rice plant in hydroponic culture experiment. PLoS ONE 15(12 December):1-15, doi:10.1371/journal.pone.0243174.
Isaguirre, A.C., Moyano, M.F., Gil, R.A. and Moglia, M.M. 2020. A novel and simple method for elements determination in aerobiological samples by Inductively Coupled Plasma Mass Spectrometry (ICP-MS) analysis. Water, Air, and Soil Pollution 231(2), doi:10.1007/s11270-020-4416-2.
Kashem, M.A., Singh, B.R., Kubota, H., Nagashima, R.S., Kitajima, N., Kondo, T. and Kawai, S. 2007. Assessing the potential of Arabidopsis halleri ssp. gemmifera as a new cadmium hyperaccumulator grown in hydroponics. Canadian Journal of Plant Science 87(3):499-502, doi:10.4141/CJPS06058.
Kashem, M.A., Singh, B.R., Kubota, H., Sugawara, R., Kitajima, N., Kondo, T. and Kawai, S. 2010. Zinc tolerance and uptake by Arabidopsis halleri ssp. gemmifera grown in nutrient solution. Environmental Science and Pollution Research 17(5):1174-1176, doi:10.1007/s11356-009-0193-6.
Khan, M.A., Khan, S., Khan, A. and Alam, M. 2017. Soil contamination with cadmium, consequences and remediation using organic amendments. Science of the Total Environment 601-602:1591-1605, doi:10.1016/j.scitotenv.2017.06.030.
Khum-in, V., Suk-in, J., In-ai, P., Piaowan, K., Phaimisap, Y., Supanpaiboon, W. and Phenrat, T. 2020. Combining biochar and zerovalent iron (BZVI) as a paddy field soil amendment for heavy cadmium (Cd) contamination decreases Cd but increases zinc and iron concentrations in rice grains: a field-scale evaluation. Process Safety and Environmental Protection 141:222-233, doi:10.1016/j.psep.2020.05.008.
Kubier, A., Wilkin, R.T. and Pichler, T. 2019. Cadmium in soils and groundwater: a review. Applied Geochemistry 108(July), doi:10.1016/j.apgeochem.2019.104388.
Kudo, H., Inoue, C. and Sugawara, K. 2021. Effects of growth stage and cd chemical form on cd and zn accumulation in Arabidopsis halleri ssp. Gemmifera. International Journal of Environmental Research and Public Health 18(8), doi:10.3390/ijerph18084214.
Li, H., Yang, Z., Dai, M., Diao, X., Dai, S., Fang, T. and Dong, X. 2020. Input of Cd from agriculture phosphate fertilizer application in China during 2006–2016. Science of the Total Environment 698:134149, doi:10.1016/j.scitotenv.2019.134149.
Li, X., Yu, Z., Xu, J., Pan, Y., Bo, W., Liu, B., Zhang, P., Bai, J. and Zhang, Q. 2020. The technique of high-pressure powder pressing with polyester film covering for XRF of geochemical samples. X-Ray Spectrometry (July 2019), doi:10.1002/xrs.3147.
Li, Y., Liao, X. and Li, W. 2019. Combined sieving and washing of multi-metal-contaminated soils using remediation equipment: a pilot-scale demonstration. Journal of Cleaner Production 212:81-89, doi:10.1016/j.jclepro.2018.11.294.
Liu, K., Lv, J., He, W., Zhang, H., Cao, Y. and Dai, Y. 2015. Major factors influencing cadmium uptake from the soil into wheat plants. Ecotoxicology and Environmental Safety 113:207-213, doi:10.1016/j.ecoenv.2014.12.005.
Lu, Y., Zhou, Y., Nakai, S., Hosomi, M., Zhang, H., Kronzucker, H.J. and Shi, W. 2014. Stimulation of nitrogen removal in the rhizosphere of aquatic duckweed by root exudate components. Planta 239(3):591-603, doi:10.1007/s00425-013-1998-6.
Luo, P., Xiao, X., Han, X., Ma, Y., Sun, X., Jiang, J. and Wang, H. 2019. Application of different single extraction procedures for assessing the bioavailability of heavy metal(loid)s in soils from overlapped areas of farmland and coal resources. Environmental Science and Pollution Research 26(15):14932-14942, doi:10.1007/s11356-019-04833-8.
Luo, Q., Wang, S., Sun, L.N. and Wang, H. 2017. Metabolic profiling of root exudates from two ecotypes of Sedum alfredii treated with Pb based on GC-MS. Scientific Reports 7(November 2016):1-9, doi:10.1038/srep39878.
Manohar, M., Shigaki, T. and Shigaki, L. 2012. Past, present and future approaches for reducing cadmium content. United States Department of Agriculture / Agricultural Research August 2015:5-33, doi:10.13140/RG.2.1.1215.4086.
Marolt, G. and Kolar, M. 2021. Analytical methods for determination of phytic acid and other inositol phosphates: a review. Molecules 26(1), doi:10.3390/MOLECULES26010174.
Mench, M. and Martin, E. 1991. Mobilization of cadmium and other metals from two soils by root exudates of Zea mays L., Nicotiana tabacum L. and Nicotiana rustica L. Plant and Soil 132(2):187-196, doi:10.1007/BF00010399.
Moon, D.H., Lee, J.R., Wazne, M. and Park, J.H. 2012. Assessment of soil washing for Zn contaminated soils using various washing solutions. Journal of Industrial and Engineering Chemistry 18(2):822-825, doi:10.1016/j.jiec.2011.11.137.
Naveed, M., Brown, L.K., Raffan, A.C., George, T.S., Bengough, A.G., Roose, T., Sinclair, I., Koebernick, N., Cooper, L., Hackett, C.A. and Hallett, P.D. 2017. Plant exudates may stabilize or weaken soil depending on species, origin and time. European Journal of Soil Science 68(6):806-816, doi:10.1111/ejss.12487.
Peng, Q., Chen, W., Wu, L. and Bai, L. 2017. The uptake, accumulation, and toxic effects of cadmium in barnyard grass (Echinochloa crus-galli). Polish Journal of Environmental Studies 26(2):779-784, doi:10.15244/pjoes/65780.
Peralta-Videa, J.R., Lopez, M.L., Narayan, M., Saupe, G. and Gardea-Torresdey, J. 2009. The biochemistry of environmental heavy metal uptake by plants: implications for the food chain. International Journal of Biochemistry and Cell Biology 41(8-9):1665-1677, doi:10.1016/j.biocel.2009.03.005.
Piri, M., Sepehr, E., Samadi, A., Farhadi, K.H. and Alizadeh, M. 2020. Contaminated soil amendment by diatomite: chemical fractions of zinc, lead, copper and cadmium. International Journal of Environmental Science and Technology 18(5):1191-1200, doi:10.1007/s13762-020-02872-0.
Robertsa, T.L. 2014. Cadmium and phosphorous fertilizers: the issues and the science. Procedia Engineering 83:52-59, doi:10.1016/j.proeng.2014.09.012.
Rolfe, S.A., Griffiths, J. and Ton, J. 2019. Crying out for help with root exudates: adaptive mechanisms by which stressed plants assemble health-promoting soil microbiomes. Current Opinion in Microbiology 49:73-82, doi:10.1016/j.mib.2019.10.003.
Sahito, Z.A., Zehra, A., Chen, S., Yu, S., Tang, L., Ali, Z., Hamza, S., Irfan, M., Abbas, T., He, Z. and Yang, X. 2022. Rhizobium rhizogenes-mediated root proliferation in Cd/Zn hyperaccumulator Sedum alfredii and its effects on plant growth promotion, root exudates and metal uptake efficiency. Journal of Hazardous Materials 424(PB):127442, doi:10.1016/j.jhazmat.2021.127442.
Schaider, L.A., Senn, D.B., Estes, E.R., Brabander, D.J. and Shine, J.P. 2014. Sources and fates of heavy metals in a mining-impacted stream: Temporal variability and the role of iron oxides. Science of the Total Environment 490:456-466, doi:10.1016/j.scitotenv.2014.04.126.
Sidhu, G.P.S., Bali, A.S. and Bhardwaj, R. 2019. Role of organic acids in mitigating cadmium toxicity in plants. Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches 2019:255-279, doi:10.1016/B978-0-12-815794-7.00010-2.
Tessier, A., Campbell, P.G.C. and Bisson, M. 1979. Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry 51(7):844-851, doi:10.1021/ac50043a017.
Wamere, L.K. 2019. Heavy Metals Pollution using XRF Spectrometry- A Case Study of Kilimapesa Gold Mines Processing Plant, Narok County. Thesis, University of Nairobi.
Wang, D., Zhang, G., Dai, Z., Zhou, L., Bian, P., Zheng, K., Wu, Z. and Cai, D. 2018. Sandwich-like nanosystem for simultaneous removal of Cr(VI) and Cd(II) from water and soil. ACS Applied Materials and Interfaces 10(21):18316-18326, doi:10.1021/acsami.8b03379.
Wang, L., Cui, X., Cheng, H., Chen, F., Wang, J., Zhao, X., Lin, C. and Pu, X. 2015. A review of soil cadmium contamination in China including a health risk assessment. Environmental Science and Pollution Research 22(21):16441-16452, doi:10.1007/s11356-015-5273-1.
Wang, P., Chen, H., Kopittke, P.M. and Zhao, F. J. 2019. Cadmium contamination in agricultural soils of China and the impact on food safety. Environmental Pollution 249:1038-1048, doi:10.1016/j.envpol.2019.03.063.
Wang, Y.M., Tang, D.D., Zhang, X.H., Uchimiya, M., Yuan, X.Y., Li, M. and Chen, Y.Z. 2019. Effects of soil amendments on cadmium transfer along the lettuce-snail food chain: Influence of chemical speciation. Science of the Total Environment 649(1):801-807, doi:10.1016/j.scitotenv.2018.08.323.
Wilschefski, S. and Baxter, M. 2019. Inductively Coupled Plasma Mass Spectrometry: introduction to analytical aspects. Clinical Biochemist Reviews 40(3):115-133, doi:10.33176/aacb-19-00024.
Wiyono, C.D.A.P., Inoue, C. and Chien, M.F. 2021. HMA4 and IRT3 as indicators accounting for different responses to Cd and Zn by hyperaccumulator Arabidopsis halleri ssp. gemmifera. Plant Stress 2, doi:10.1016/j.stress.2021.100042.
Xie, X., Yang, S., Liu, H., Pi, K. and Wang, Y. 2020. The behavior of cadmium leaching from contaminated soil by nitrilotriacetic acid: implication for Cd-contaminated soil remediation. Water, Air, and Soil Pollution 231(4), doi:10.1007/s11270-020-04545-7.
Zhai, X., Li, Z., Huang, B., Luo, N., Huang, M., Zhang, Q. and Zeng, G. 2018. Remediation of multiple heavy metal-contaminated soil through the combination of soil washing and in situ immobilization. Science of the Total Environment 635:92-99, doi:10.1016/j.scitotenv.2018.04.119.
Zhao, M., Zhao, J., Yuan, J., Hale, L., Wen, T., Huang, Q., Vivanco, J.M., Zhou, J., Kowalchuk, G.A. and Shen, Q. 2021. Root exudates drive soil-microbe-nutrient feedbacks in response to plant growth. Plant Cell and Environment 44(2):613-628, doi:10.1111/pce.13928.
Downloads
Submitted
Accepted
Published
How to Cite
Issue
Section
License
Submission of a manuscript implies: that the work described has not been published before (except in the form of an abstract or as part of a published lecture, or thesis) that it is not under consideration for publication elsewhere; that if and when the manuscript is accepted for publication, the authors agree to automatic transfer of the copyright to the publisher.
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Scientific Journal by Eko Handayanto is licensed under a Creative Commons Attribution 4.0 International License.
Based on a work at https://ub.ac.id.
Permissions beyond the scope of this license may be available at https://ircmedmind.ub.ac.id/.