Abstract
In this study, we aimed to elucidate the defense mechanism of Alcea rosea (Linn.) Cavan. and Hydrangea macrophylla (Thunb.) Ser. against the single and compound toxicity of lead (Pb) and zinc (Zn) along with the synergistic effect of ethylenediaminetetraacetic acid (EDTA) in accumulation of metals in these two species. The two plant species were subjected to single metal treatment (Pb 1000 mg kg−1, Zn 600 mg kg−1) and compound metal treatment (Pb 1000 mg kg−1 + Zn 600 mg kg−1) in a greenhouse. Besides, different levels of EDTA were applied (2.5, 5.0, and 10.0 mmol kg−1) with compound metal treatment. Several physiological and biochemical parameters, including plant photosynthetic parameters, enzymatic antioxidant system, accumulation concentration of metals, and subcellular distribution were estimated. The results showed that the antioxidative enzymes, proline, root morphological changes, and metal localization all played important roles in resisting Pb and Zn toxicity. A notable difference was that Zn was concentrated in the roots (58.5%) of H. macrophylla to reduce the damage but in the leaves (38.5%) of A. rosea to promote photosynthesis and resist the toxicity of metals. In addition, Zn reduced the toxicity of Pb to plants by regulating photosynthesis, Pb absorption and Pb distribution in subcells. The biological concentration factors (BCF) and translocation factors (TF) for Pb in two plants were less than 1, indicating that they could be considered as phytostabilizators in Pb-contaminated soils. Moreover, EDTA could enhance the enrichment and transport capacity of Pb and Zn to promote the phytoremediation effect. In summary, both plants have a certain application potential for repairing Pb–Zn-contaminated soil.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Alia PP, Saradhi (1991) Proline accumulation under heavy metal stress. J Plant Physiol 138:554–558. https://doi.org/10.1016/s0176-1617(11)80240-3
Basta NT, Tabatabai MA (1992) Effect of cropping systems on adsorption of metals by soils. Soil Sci 153(2):108–114. https://doi.org/10.1097/00010694-199203000-00004
Barceló J, Poschenrieder Ch (1990) Plant water relations as affected by heavy-metal stress-a review. J Plant Nutr 13(1):1–37. https://doi.org/10.1080/01904169009364057
Batool R, Hameed M, Ashraf M, Sajid M, Ahmad A, Fatima S (2015) Physioanatomical responses of plants to heavy metals. In: Oztürk M, Ashraf M, Aksoy A, Ahmad MSA (eds) Phytoremediation for Green Energy. Springer, Netherlands, pp 79–96
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assay and an assay applicable to PAGE. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Chandrasekhar C, Ray JG (2019) Lead accumulation, growth responses and biochemical changes of three plant species exposed to soil amended with different concentrations of lead nitrate. Ecotox Environ Safe 171:26–36. https://doi.org/10.1016/j.ecoenv.2018.12.058
Chen DM, Chen DQ, Xue RR, Long J, Lin XH, Lin YB, Jia LH, Zeng RS, Song YY (2019) Effects of boron, silicon and their interactions on cadmium accumulation and toxicity in rice plants. J Hazard Mater 367:447–455. https://doi.org/10.1016/j.jhazmat.2018.12.111
Chen JR, Zhong B, Shaff M, Guo J, Wang Y, Wu JS, Ye ZQ, He LZ, Liu D (2017) Effect of lead (Pb) on antioxidation system and accumulation ability of Moso bamboo (Phyllostachys pubescens). Ecotox Environ Safe 138:71–77. https://doi.org/10.1016/j.ecoenv.2016.12.020
Chen LH, Gao S, Zhu P, Liu Y, Hu TD, Zhang J (2014) Comparative study of metal resistance and accumulation of lead and zinc in two poplars. Physiol Plant 151(4):390–405. https://doi.org/10.1111/ppl.12120
Dong X, Yang F, Yang S, Yan C (2019) Subcellular distribution and tolerance of cadmium in Canna indica L. Ecotox Environ Safe 185(15):109692. https://doi.org/10.1016/j.ecoenv.2019.109692
Forte J, Mutiti S (2017) Phytoremediation potential of Helianthus annuus and Hydrangea paniculata in copper and lead-contaminated soil. Water Air Soil Pollut 228:77. https://doi.org/10.1007/s11270-017-3249-0
Gao HB, Yu PY, Sun YJ, Jiang LJ (2019) Analysis of carbon metabolism and differential expression of related enzyme genes in castor leaves under Pb and Zn stress. J Plant Physiology 55(4):483–492. https://doi.org/10.13592/j.cnki.ppj.2018.0456
Gao JF (2006) Experimental guidance of plant physiology. Higher Education Press, Beijing, pp 210–211
Garcia S, Zornoza P, Hernndez LE, Esteban E, Carpena RO (2017) Response of Lupinusalbus to Pb-EDTA indicates relatively high tolerance. Toxicol Environ Chem 99(9–10):1378–1388. https://doi.org/10.1080/02772248.2017.1387263
Glinska S, Michlewska S, Grapinska M, Seliger P (2014) The effect of EDTA and EDDS on lead uptake and localization in hydroponically grown Pisumsativum L. Acta Physiol Plant 36(2):399–408. https://doi.org/10.1007/s11738-013-1421-8
He C, Zhao YP, Wang FF, Kokyo O, Zhao ZZ, Wu CL, Zhang XY, Chen XP, Liu XY (2020) Phytoremediation of soil heavy metals (Cd and Zn) by castor seedlings: Tolerance, accumulation and subcellular distribution. Chemosphere 252:126471. https://doi.org/10.1016/j.chemosphere.2020.126471
Huang Y, Zu LH, Zhang M, Yang T, Zhou MZ, Shi C, Shi FC, Zhang WJ (2020) Tolerance and distribution of cadmium in an ornamental species Althaea rosea Cavan. Int J Phytoremediat 22(7):713–724. https://doi.org/10.1080/15226514.2019.1707771
Hossain MA, Fujita M, Jaime A, Silva T, Piyatida P (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37. https://doi.org/10.1155/2012/872875
Irfan M, Ahmad A, Hayat S (2014) Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea. Saudi J Biol Sci 21:125. https://doi.org/10.1016/j.sjbs.2013.08.001
Jiang MY, Liu SL, Li YF, Li X, Luo ZH, Song HX, Chen QB (2019) EDTA-facilitated toxic tolerance, absorption and translocation and phytoremediation of lead by dwarf bamboos. Ecotox Environ Safe 170:502–512. https://doi.org/10.1016/j.ecoenv.2018.12.020
Kalyvas G, Tsitselis G, Gasparatos D, Massas I (2018) Efficacy of EDTA and olive mill wastewater to enhance As, Pb, and Zn phytoextraction by Pteris vittata L. from a soil heavily polluted by mining activities. Sustainability 10(6):1962. https://doi.org/10.3390/su10061962
Kavousi HR, Karimi MR, Neghab MG (2021) Assessment the copper-induced changes in antioxidant defense mechanisms and copper phytoremediation potential of common mullein (Verbascum thapsus L.). Environ Sci Pollut Res 28(14):18070–18080. https://doi.org/10.1007/s11356-020-11903-9
Kumar B, Smita K, Cumbal FL (2017) Plant mediated detoxification of mercury and lead. Arab J Chem 102:S2335–S2342. https://doi.org/10.1016/j.arabjc.2013.08.010
Lanier C, Bernard F, Dumez S, Dransart JL, Lemire S, Vandenbulcke F, Nesslany F, Platel A, Devred I, Hayet A, Cuny D, Deram A (2019) Combined toxic effects and DNA damage to two plant species exposed to binary metal mixtures (Cd/Pb). Ecotox Environ Safe 167:278–287. https://doi.org/10.1016/j.ecoenv.2018.10.010
Lasat MM, Baker A, Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspicaerulescens. Plant Physiol 118(3):875–883. https://doi.org/10.1104/pp.118.3.875
Li F, Qiu Y, Xu X, Yang F, Wang Z, Feng J, Wang J (2020) EDTA-enhanced phytoremediation of heavy metals from sludge soil by Italian ryegrass (Lolium perenne L.). Ecotox Environ Safe 191:110185. https://doi.org/10.1016/j.ecoenv.2020.110185
Li HS (2000) Principles and techniques of plant physiological biochemical experiment. Higher Education Press, Beijing
Lingua G, Todeschini V, Grimaldi M, Baldantoni D, Proto A, Cicatelli A, Castiglione S (2014) Polyaspartate, a biodegradable chelant that improves the phytoremediation potential of poplar in a highly metal-contaminated agricultural soil. J Environ Manage 132:9–15. https://doi.org/10.1016/j.jenvman.2013.10.015
Lin Y, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69(19):3187–3206. https://doi.org/10.1007/s00018-012-1089-z
Liu J, Xin X, Zhou Q (2018) Phytoremediation of contaminated soils using ornamental plants. Environ Rev 26(1):43–54. https://doi.org/10.1139/er-2017-0022
Liu Y, Yu XF, Feng YM, Zhang C, Wang C, Zeng J, Huang Z, Kang HY, Fan X, Sha L, Zhang HQ, Zhou YH, Gao SP, Chen QB (2017) Physiological and transcriptome response to cadmium in cosmos (Cosmos bipinnatus Cav.) seedlings. Sci Rep 7(1):14691. https://doi.org/10.1038/s41598-017-14407-8
Liu Z, Bai Y, Yang TM (2019) Effect of Cd on the uptake and translocation of Pb, Cu, Zn, and Ni in potato and wheat grown in Sierozem. Soil Sediment Contam 28(7):650–669. https://doi.org/10.1080/15320383.2019.1643289
Li X, Wang YJ, Pan YS, Yu H, Zhang XL, Shen YP, Jiao S, Wu K, La GX, Yuan Y (2017) Mechanisms of Cd and Cr removal and tolerance by macrofungus Pleurotusostreatus. J Hazard Mater 330:1–8. https://doi.org/10.1016/j.jhazmat.2017.01.047
Marques MC, Nascimento CW, Silva AJ (2017) Tolerance of an energy crop (Jatropha curcas L.) to zinc and lead assessed by chlorophyll fluorescence and enzyme activity. S Afr J Bot 112:275–282. https://doi.org/10.1016/j.sajb.2017.06.009
Meers E, Ruttens A, Hopgood MJ, Samson D, Tack MG (2005) Comparison of EDTA and EDDS as potential soil amendments for enhanced phytoextraction of heavy metals. Chemosphere 58(8):1011–1022. https://doi.org/10.1016/j.chemosphere.2004.09.047
Meng Q, Zou J, Zou JH, Jiang WS, Liu DH (2007) Effect of Cu2+ concentration on growth, antioxidant enzyme activity and malondialdehyde content in garlic (Allium sativum L). Acta Biol Crac 49:95–101
Muro DA, Mussali P, Valencia L, Flores K, Tovar E (2020) Morphological, physiological, and genotoxic effects of heavy metal bioaccumulation in Prosopislaevigata reveal its potential for phytoremediation. Environ Sci Pollut Res 27:40187–40204. https://doi.org/10.1007/s11356-020-10026-5
Peco JD, Higueras P, Campos JA, Olmedilla A, Romero MC, Sandalio LM (2020) Deciphering lead tolerance mechanisms in a population of the plant species Biscutella auriculata L. from a mining area: Accumulation strategies and antioxidant defenses. Chemosphere 261:127721. https://doi.org/10.1016/j.chemosphere.2020.127721
Qureshi FF, Ashraf MA, Rasheed R, Ali S, Hussain I, Ahmed A, Iqbal M (2020) Organic chelates decrease phytotoxic effects and enhance chromium uptake by regulating chromium-speciation in castor bean (Ricinus communis L.). Sci Total Environ 716:137061. https://doi.org/10.1016/j.scitotenv.2020.137061
Ramana S, Tripathi AK, Bharati K, Singh AB, Kumar A, Sahu A, Rajput PS, Dey P, Saha JK, Patra AK (2021) Tolerance of cotton to elevated levels of Pb and its potential for phytoremediation. Environ Sci Pollut Res 28(25):32299–32309. https://doi.org/10.1007/s11356-021-13067-6
Rizvi A, Khan MS (2017) Biotoxic impact of heavy metals on growth, oxidative stress and morphological changes in root structure of wheat (Triticumaestivum L.) and stress alleviation by Pseudomonas aeruginosa strain CPSB1. Chemosphere 185:942–952. https://doi.org/10.1016/j.chemosphere.2017.07.088
Shahid M, Austruy A, Echevarria G, Arshad M, Sanaullah M, Aslam M, Nadeem M, Nasim W, Dumat C (2014) EDTA-enhanced phytoremediation of heavy metals: A Review. Soil Sediment Contam 23(4):389–416. https://doi.org/10.1080/15320383.2014.831029
Shen X, Li RL, Chai MW, Cheng SS, Niu ZY, Qiu GY (2019) Interactive effects of single, binary and trinary trace metals (lead, zinc and copper) on the physiological responses of Kandeliaobovata seedlings. Environ Geochem Health 41(1):135–148. https://doi.org/10.1007/s10653-018-0142-8
Sheoran V, Sheoran A, Poonia P (2011) Role of hyperaccumulators in phytoextraction of metals from contaminated mining sites: a review. Crit Rev Environ Sci Technol 41:168–214. https://doi.org/10.1080/10643380902718418
Sidhu S, Batish K (2016) Effect of lead on oxidative status, antioxidative response and metal accumulation in Coronopusdidymus. Plant Physiol Biochem 105:290–296. https://doi.org/10.1016/j.plaphy.2016.05.019
Srivastava RK, Pandey P, Rajpoot R, Rani A, Dubey RS (2014) Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. Protoplasma 251(5):1047–1065. https://doi.org/10.1007/s00709-014-0614-3
Tabelin CB, Toshifumi I, Tabelin V, Mylah IP, Einstine M, Naoki H (2018) Arsenic, selenium, boron, lead, cadmium, copper, and zinc in naturally contaminated rocks: A review of their sources, modes of enrichment, mechanisms of release, and mitigation strategies. Sci Total Environ 645:1522–1553. https://doi.org/10.1016/j.scitotenv.2018.07.103
Usharani B, Vasudevan N (2017) Root exudates of Cyperusalternifolius in partial hydroponic condition under heavy metal stress. Pharmacogn Res 9(3):294–300. https://doi.org/10.4103/pr.pr_107_16
Wang S, Zhao Y, Guo JH, Liu Y (2018) Antioxidative response in leaves and allelochemical changes in root exudates of Ricinuscommunis under Cu, Zn, and Cd stress. Environ Sci Pollut Res 25(32):32747–32755. https://doi.org/10.1007/s11356-018-3283-5
Wang ZY, Wang H, Xu C, Lv GH, Luo ZC, Zhu HH, Wang S, Zhu QH, Huang DY, Li BZ (2020) Foliar application of Zn-EDTA at early filling stage to increase grain Zn and Fe, and reduce grain Cd, Pb and grain yield in rice (Oryza sativa L.). Bull Environ Contam Toxicol 105(3):428–432. https://doi.org/10.1007/s00128-020-02949-z
Weigel HJ, Jager HJ (1980) Subcellular distribution and chemical form of cadmium in bean plants. Plant Physiol 65(3):480–482. https://doi.org/10.1104/pp.65.3.480
Xin J, Zhang Y, Tian R (2018) Tolerance mechanism of Triarrhenasaccharifiora (Maxim.) Nakai. seedlings to lead and cadmium: Translocation, subcellular distribution, chemical forms and variations in leaf ultrastructure. Ecotox Environ Safe 165:611–621. https://doi.org/10.1016/j.ecoenv.2018.09.022
Xu P, Wang Z (2014) A comparison study in cadmium tolerance and accumulation in two cool-season turfgrasses and Solanum nigrum L. Water Air Soil Pollut 225(5):1–9. https://doi.org/10.1007/s11270-014-1938-5
Yang W, Wang Y, Liu D, Hussain B, Ding Z, Zhao F, Yang X (2020) Interactions between cadmium and zinc in uptake, accumulation and bioavailability for Salix integra with respect to phytoremediation. Int J Phytoremediat 22(6):628–637. https://doi.org/10.1080/15226514.2019.1701981
Yi XY (2018) Study on the responses of Ricinus communis L. to Lead and Zinc stress and their mechanisms. Hunan: Central South University of Forestry and Technology 162–163.
Zeng J, Li XY, Wang XX, Zhang KH, Wang Y, Kang HY, Chen GD, Lan T, Zhang ZW, Yuan S, Wang CQ, Zhou YH (2020) Cadmium and lead mixtures are less toxic to the Chinese medicinal plant Ligusticum chuanxiong Hort. than either metal alone. Ecotox Environ Safe 193:110342. https://doi.org/10.1016/j.ecoenv.2020.110342
Zhang Q, Chen YH, Du L, Zhang MY, Han LZ (2019) Accumulation and subcellular distribution of heavy metal in Paulownia fortunei cultivated in lead-zinc slag amended with peat. Int J Phytoremediat 21(11):1153–1160. https://doi.org/10.1080/15226514.2019.1612844
Zhang W, Hu YJ, Cao YR, Huang FG, Xu H (2012) Tolerance of lead by the fruiting body of Oudemansiellaradicata. Chemosphere 88:467–475. https://doi.org/10.1016/j.chemosphere.2012.02.079
Funding
This work was supported by the General Project of the Key Research and Development Plan of Shaanxi Province (2021NY-070); Project of Science and Technology Plan of Xi’an (20NYYF0064).
Author information
Authors and Affiliations
Contributions
This work was carried out in collaboration with all authors. BZ put forward to the concept, ensured the feasibility and rationality of the experiment, and also proofread the manuscript. All authors designed the experiment and prepared the manuscript. YPD and YZ carried out the experimental work and data analyses. All of authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Additional information
Responsible Editor: Elena Maestri
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
Duan, Y., Zhang, Y. & Zhao, B. Lead, zinc tolerance mechanism and phytoremediation potential of Alcea rosea (Linn.) Cavan. and Hydrangea macrophylla (Thunb.) Ser. and ethylenediaminetetraacetic acid effect. Environ Sci Pollut Res 29, 41329–41343 (2022). https://doi.org/10.1007/s11356-021-18243-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-18243-2