Abstract
Perennial ryegrass (Lolium perenne L.) was planted in uranium-contaminated soil mixtures supplemented with different amounts of citric acid to investigate the defense strategies of perennial ryegrass against U and the enhanced mechanism of citric acid on the remediation efficiency in the laboratory. The uranium content in the plant tissues showed that the roots were the predominant tissue for uranium accumulation. In both root and shoot cells, the majority of U was located in the cell wall fraction. Furthermore, antioxidant enzymes were also stimulated when exposed to U stress. These results suggested that perennial ryegrass had evolved defense strategies, such as U sequestration in root tissue, compartmentalization in the cell wall, and antioxidant enzyme systems, to minimize uranium stress. For an enhanced mechanism, the optimal concentration of citric acid was 5 mmol/kg, and the removal efficiency of U in the shoots and roots increased by 47.37% and 30.10%, respectively. The treatment with 5 mmol/kg citric acid had the highest contents of photosynthetic pigment and soluble protein, the highest activity of antioxidant enzymes, and the lowest content of MDA (malondialdehyde) and relative electrical conductivity. Moreover, the TEM (transmission electron microscope) results revealed that after 5 mmol/kg citric acid was added, the cell structure of plant branches partially returned to normal, the number of mitochondria increased, chloroplast surfaces seemed normal, and the cell wall became visible. The damage to the cell ultrastructure of perennial ryegrass was significantly alleviated by treatment with 5 mmol/kg citric acid. All the results above indicated that perennial ryegrass could accumulate uranium with elevated uranium tolerance and enrichment ability with 5 mmol/kg citric acid.
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The datasets generated and/or analyzed during the current study are property of Lishan Rong (University of South China, China); they are available from the corresponding author who will inform Lishan Rong that the data will be released on reasonable request.
References
Afshan S, Ali S, Bharwana SA, Rizwan M, Farid M, Abbas F, Ibrahim M, Mehmood MA, Abbasi GH (2015) Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L. Environmental Science and Pollution Research 22:11679–11689
Al Mahmud J, Hasanuzzaman M, Nahar K, Bhuyan MHMB, Fujita M (2018) Insights into citric acid-induced cadmium tolerance and phytoremediation in Brassica juncea L.: coordinated functions of metal chelation, antioxidant defense and glyoxalase systems. Ecotox Environ Safe 147:990–1001
Baker MR, Coutelot FM, Seaman JC (2019) Phosphate amendments for chemical immobilization of uranium in contaminated soil. Environ Int 129:565–572
Begum ZA, Rahman IMM, Tate Y, Sawai H, Maki T, Hasegawa H (2012) Remediation of toxic metal contaminated soil by washing with biodegradable aminopolycarboxylate chelants. Chemosphere 87:1161–1170
Bin X, Guohui Y, Hui L, Zheni X, Wuwu W, Jing Z, Bingru H (2019) Knockdown of STAYGREEN in perennial ryegrass (Lolium perenne L.) leads to transcriptomic alterations related to suppressed leaf senescence and improved forage quality. Plant Cell Physiol 60:202–212
Burges A, Epelde L, Blanco FJM, Becerril JM, Garbisu C (2017) Ecosystem services and plant physiological status during endophyte-assisted phytoremediation of metal contaminated soil. Sci Total Environ 584–585:329–338
Chaturvedi N, Dhal NK, Patra HK (2015) EDTA and citric acid-mediated phytoextraction of heavy metals from iron ore tailings using Andrographis paniculata: a comparative study. Int J Min Reclam Env 29:33–46
Chen L, Long C, Wang D, Yang JY (2020a) Phytoremediation of cadmium (Cd) and uranium (U) contaminated soils by Brassica juncea L. enhanced with exogenous application of plant growth regulators. Chemosphere 242:125112
Chen L, Yang JY, Wang D (2020b) Phytoremediation of uranium and cadmium contaminated soils by sunflower (Helianthus annuus L.) enhanced with biodegradable chelating agents. J Clean Prod 263:121491
Chen L, Yang JY, Wang D (2020c) Phytoremediation of uranium and cadmium contaminated soils by sunflower ( Helianthus annuus L.) enhanced with biodegradable chelating agents. J Clean Prod 263:121491
Chen L, Liu JR, Zhang WX, Zhou JQ, Luo DQ, Li ZM (2021) Uranium (U) source, speciation, uptake, toxicity and bioremediation strategies in soil-plant system: a review. J Hazard Mater 413:125319
Dai H, Wei S, Twardowska I, Han R, Xu L (2017) Hyperaccumulating potential of Bidens pilosa L. for Cd and elucidation of its translocation behavior based on cell membrane permeability. Environ Sci Pollut Res 24:23161–23167
Dixon PD, Hawkins T, Hussey JP, Edwards R (2009) Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J Exp Bot 60:1207–1218
Duquène L, Tack F, Meers E, Baeten J, Wannijn J, Vandenhove H (2008) Effect of biodegradable amendments on uranium solubility in contaminated soils. Sci. Total Environ 391:26–33
Garg N, Kaur H (2013) Response of antioxidant enzymes, phytochelatins and glutathione production towards Cd and Zn stresses in Cajanus cajan (L.) Millsp. genotypes colonized by arbuscular mycorrhizal fungi. J Agron Crop Sci 199:118–133
Geebelen W, Vangronsveld J, Adriano DC, Poucke LCV, Clijsters H (2002) Effects of Pb–EDTA and EDTA on oxidative stress reactions and mineral uptake in Phaseolus vulgaris. Physiol Plant 115:377–384
Grachet NG, Walker NR (2016) First report of brown ring patch caused by Waitea circinata on perennial ryegrass (Lolium perenne) in Oklahoma. Plant Dis 100:855–855
Gunawardana B, Singhal N, Johnson A (2011) Effects of Amendments on copper, cadmium, and lead phytoextraction by Lolium perenne from multiple-metal contaminated solution. Int J Phytorem 13:215–232
Han Y, Zhang L, Gu J, Zhao J, Fu J (2016) Citric acid and EDTA on the growth, photosynthetic properties and heavy metal accumulation of Iris halophila Pall. cultivated in Pb mine tailings. Int Biodeterior Biodegradation 128:15–21
Hasan MM, Uddin MN, Ara-Sharmeen I, Alharby HF, Alzahrani Y, Hakeem KR, Zhang L (2019) Assisting phytoremediation of heavy metals using chemical amendments. Plants-Basel 8:295
Hseu ZY, Jien SH, Wang SH, Deng HW (2013) Using EDDS and NTA for enhanced phytoextraction of Cd by water spinach. J Environ Manage 117:58–64
Hu N, Lang T, Ding DX, Hu JS, Li CW, Zhang H, Li GY (2019) Enhancement of repeated applications of chelates on phytoremediation of uranium contaminated soil by Macleaya cordata. J Environ Radioact 199:58–65
Huang ZL, Tang SQ, Zhang L, Ma LJ, Ding SD, Du L, Zhang D, Jin YD, Wang RB, Huang C, Xia CQ (2017) Interaction between U and Th on their uptake, distribution, and toxicity in V S-alfredii based on the phytoremediation of U and Th. Environmental Science and Pollution Research 24:2996–3005
Khair KU, Farid M, Ashraf U, Zubair M, Rizwan M, Farid S, Ishaq HK, Iftikhar U, Ali S (2020) Citric acid enhanced phytoextraction of nickel (Ni) and alleviate Mentha piperita (L.) from Ni-induced physiological and biochemical damages. Environ Sci Pollut Res 5:1–13
Laurette J, Larue C, Mariet C, Brisset F, Khodja H, Bourguignon J, Carriere M (2012) Influence of uranium speciation on its accumulation and translocation in three plant species: oilseed rape, sunflower and wheat. Environ Exp Bot 77:96–107
Li C, Wang ML, Luo XG, Liang LL, Han X, Lin XY (2019) Accumulation and effects of uranium on aquatic macrophyte Nymphaea tetragona Georgi: potential application to phytoremediation and environmental monitoring. J Environ Radioact 198:43–49
Li CW, Hu N, Ding DX, Hu JS, Wang YD (2014) Phytoextraction of uranium from contaminated soil by Macleaya cordata before and after application of EDDS and CA. Environ Sci Pollut Res Int 22:6155–6163
Liu XY, Cao LY, Zhang XY, Chen J, Huo ZH, Mao Y (2018) Influence of alkyl polyglucoside, citric acid, and nitrilotriacetic acid on phytoremediation in pyrene-Pb co-contaminated soils. Int J Phytorem 20:1055–1061
Monroy-Figueroa J, Mendoza-Castillo DI, Bonilla-Petriciolet A, Perez-Cruz MA (2015) Chemical modification of Byrsonima crassifolia with citric acid for the competitive sorption of heavy metals from water. Int J Environ Sci Te 12:2867–2880
Moslehi A, Feizian M, Higueras P, Eisvand HR (2019) Assessment of EDDS and vermicompost for the phytoextraction of Cd and Pb by sunflower (Helianthus annuus L.). Int J Phytorem 21:191–199
Muhammad D, Chen F, Zhao J, Zhang GP, Wu FB (2009) Comparison of EDTA- and citric acid-enhanced phytoextraction of heavy metals in artificially metal contaminated soil by Typha angustifolia. Int J Phytorem 11:558–574
Najeeb U, Xu L, Ali S, Jilani G, Gong HJ, Shen WQ, Zhou WJ (2009) Citric acid enhances the phytoextraction of manganese and plant growth by alleviating the ultrastructural damages in Juncus effusus L. J Hazard Mater 170:1156–1163
Najeeb U, Jilani G, Ali S, Sarwar M, Xu L, Zhou WJ (2011) Insights into cadmium induced physiological and ultra-structural disorders in juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186:565–574
Nascimento CWAd, Hesterberg D, Tappero R, Nicholas S, Silva FBVd (2020) Citric acid-assisted accumulation of Ni and other metals by Odontarrhena muralis: implications for phytoextraction and metal foliar distribution assessed by μ-SXRF. Environ. Pollut 260:114025
Newete SW, Erasmus BFN, Weiersbye IM, Byrne MJ (2016) Sequestration of precious and pollutant metals in biomass of cultured water hyacinth (Eichhornia crassipes). Environmental Science and Pollution Research 23:20805–20818
Nezami S, Malakouti MJ, Samani AB, Maragheh MG (2016) Effect of low molecular weight organic acids on the uptake of Ra-226 by corn (Zea mays L.) in a region of high natural radioactivity in Ramsar-Iran. J Environ Radioact 164:145–150
Nie X, Dong F, Liu N, Liu M, Zhang W, Sun S, Yang J (2014) An investigation on the subcellular distribution and compartmentalization of uranium in Phaseolus vulgaris L. J Radioanal Nucl Chem 299:1351–1357
Nie X, Dong F, Liu N, Liu M, Zhang D, Kang W, Sun S, Zhang W, Yang J (2015) Subcellular distribution of uranium in the roots of Spirodela punctata and surface interactions. Appl Surf Sci 347:122–130
Pan X, Chen Z, Chen F, Cheng Y, Lin Z, Guan X (2015) The mechanism of uranium transformation from U(VI) into nano-uramphite by two indigenous Bacillus thuringiensis strains. J Hazard Mater 297:313–319
Qi FF, Zha ZY, Du L, Feng XJ, Wang DN, Zhang D, Fang ZD, Ma LJ, Jin YD, Xia CQ (2014) Impact of mixed low-molecular-weight organic acids on uranium accumulation and distribution in a variant of mustard (Brassica juncea var. tumida). J Radioanal Nucl Ch 302:149–159
Qi X, Hao XC, Chen XM, Xiao SQ, Chen SL, Luo XG, Wang SQ, Tian J, Wang D, Tang YL (2019) Integrated phytoremediation system for uranium-contaminated soils by adding a plant growth promoting bacterial mixture and mowing grass. J Soil Sediment 19:1799–1808
Sebastian A, Prasad MNV (2018) Exogenous citrate and malate alleviate cadmium stress in Oryza sativa L.: probing role of cadmium localization and iron nutrition. Ecotoxicol Environ Saf 166:215–222
Sha YH, Hu N, Wang YD, Chen SY, Zou C, Dai ZR, Zhang H, Ding DX (2019) Enhanced phytoremediation of uranium contaminated soil by artificially constructed plant community plots. J. Environ. Radioact 208:106036
Shi Y, Chen M, Fengguo LI, Tao M, Lanwen HU, Yang Q (2018) Advances in remediation techniques for soil heavy metal pollution. Nonferrous Metals Science and Engineering 9:66–71
Singh A, Prasad SM (2011) Reduction of heavy metal load in food chain: technology assessment. Reviews in Environmental Science & Bio/technology 10:199–214
Slomka A, Libik-Konieczny M, Kuta E, Miszalski Z (2008) Metalliferous and non-metalliferous populations of Viola tricolor represent similar mode of antioxidative response. J Plant Physiol 165:1610–1619
Smeets K, Cuypers A, Lambrechts A, Semane B, Hoet P, Laere AV, Vangronsveld J (2005) Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiol Biochem 43:437–444
Wang K, Liu YH, Song ZG, Wang D, Qiu WW (2019) Chelator complexes enhanced Amaranthus hypochondriacus L. phytoremediation efficiency in Cd-contaminated soils. Chemosphere 237:124480
Wang P, Du L, Tan Z, Su R, Li T (2016) Effects of organic acids and sylvite on phytoextraction of 241Am contaminated soil. Bull Environ Contam Toxicol 98:1–6
Xin W, Ying W, Mahmood Q, Islam E, Jin X, Li T, Yang X, Dan L (2009) The effect of EDDS addition on the phytoextraction efficiency from Pb contaminated soil by Sedum alfredii Hance. J Hazard Mater 168:530–535
Ye TZ, Liu ZR, Cai ZW (2020) Adsorption of uranium(VI) from aqueous solution by novel dibutyl imide chelating resin. J Radioanal Nucl Ch 323:223–232
Yu HY, Wang KJ, Huang HG, Zhang XZ, Li TX (2021) The regulatory role of root in cadmium accumulation in a high cadmium-accumulating rice line (Oryza sativa L.). Environmental Science and Pollution Research 28:25432–25441
Zhao YP, Cui JL, Chan TS, Dong JC, Chen DL, Li XD (2018) Role of chelant on Cu distribution and speciation in Lolium multiflorum by synchrotron techniques. Sci Total Environ 621:772–781
Funding
This work was financially supported by the National Natural Science Foundation of China (11475080, 51904155), Education Department Fund of Hunan Province of China (19C1588), and Hengyang’s Science and Technology Planning Projects (2018KJ130). national natural science foundation of china,11475080,Shuibo Xie,51904155,Guohua Wang,education department of hunan province,19C1588,Lishan Rong,hengyang’s science and technology planning projects,2018KJ130,Guohua Wang
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All authors contributed to the study conception and design. Method implementation and optimization, analysis, and data evaluation were performed by Lishan Rong and Shiqi Zhang. The first draft of the manuscript was written by Shiyou Li and Guohua Wang. Shuibo Xie, Jiali Wang, and Guohua Wang commented on previous versions of the manuscript. All authors read and approved the final submitted manuscript.
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Rong, L., Zhang, S., Wang, J. et al. Phytoremediation of uranium-contaminated soil by perennial ryegrass (Lolium perenne L.) enhanced with citric acid application. Environ Sci Pollut Res 29, 33002–33012 (2022). https://doi.org/10.1007/s11356-022-18600-9
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DOI: https://doi.org/10.1007/s11356-022-18600-9