Abstract
This study intended to investigate the responses of glutathione (GSH) metabolism and calcium (Ca) secretion in mulberry (Morus alba L.) leaves under different levels of Pb contaminated soil and their correlations with leaf Pb ion accumulations. Using a greenhouse experiment, we measured the growth, Pb and calcium contents, glutathione metabolism, and leaf morphology traits of mulberry seedlings under four soil Pb levels. Mulberry exhibited a considerable adaptability to soil Pb, and no significant decrease in biomass was observed across the various soil Pb treatments. The glutathione metabolism of mulberry was related to the soil Pb, and the relative expression level of the glutathione synthetase gene was sensitive to the presence of Pb ions. The Pb ions absorbed by mulberry accumulated primarily in the roots, and only under heavy Pb concentrations (800 mg kg−1) would Pb ions be significantly transferred to leaves. The cystoliths excreted from leaves might not play a role in the detoxification of Pb; however, soil resident Pb affected cystolith development patterns and associated calcium regulation. Calcium oxalate crystals may directly participate in the Pb detoxification process in leaves, particularly under severe soil Pb stress. Under extreme soil Pb treatments, the mulberry leaves thickened, while epidermal cells and veins increased to facilitate the transport of Pb ions to the aerial organs. Mulberry can acclimatize to severely Pb-contaminated soil by enhancing glutathione metabolism, adjusting leaf morphologies, and enhancing calcium oxalate crystal excretion. The excretion of Pb-Ca oxalate complexes might serve as detoxification for Pb-contaminated soils.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bityutskii NP, Yakkonen KL, Petrova AI, Lukina KA, Shavarda AL (2019) Calcium carbonate reduces the effectiveness of soil-added monosilicic acid in cucumber plants. J Soil Sci Plant Nutr 19:660–670. https://doi.org/10.1007/s42729-019-00066-3
Bottari E, de Tommaso G, Festa MR, Iuliano M, Zennaro G (2020) Behavior of glutathione as ligand of lead (II). Chemosphere 246:125718. https://doi.org/10.1016/j.chemosphere.2019.125718
Elder Antonio SP (2019) Are calcium oxalate crystals a dynamic calcium store in plants? New Phytol 223:1707–1711
Fayza F, Ahmed M, Shereen AE (2013) Physiological and ultrastructural studies on calcium oxalate crystal formation in some plants. Turk J Bot:139–152
Gostin I (2016) Air pollution stress and plant response. In: Kulshrestha U, Saxena P (eds) Plant responses to air pollution, vol 48. Springer Singapore, Singapore, pp 99–117
Gressel J, Dodds J (2013) Commentary: hormesis can be used in enhancing plant productivity and health; but not as previously envisaged. Plant Sci 213:123–127. https://doi.org/10.1016/j.plantsci.2013.09.007
Günthardt-Goerg MS, Vollenweider P, Hermle S, Schulin R (2019) Growth and metal accumulation of young forest trees and understorey plants on contaminated topsoil: influence of subsoil and time. Plant Soil 437:375–395. https://doi.org/10.1007/s11104-019-03986-2
Gupta DK, Huang HG, Corpas FJ (2013) Lead tolerance in plants: strategies for phytoremediation. Environ Sci Pollut Res Int 20:2150–2161. https://doi.org/10.1007/s11356-013-1485-4
Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plants 23:249–268. https://doi.org/10.1007/s12298-017-0422-2
He H, Veneklaas EJ, Kuo J, Lambers H (2014) Physiological and ecological significance of biomineralization in plants. Trends Plant Sci 19:166–174. https://doi.org/10.1016/j.tplants.2013.11.002
Huihui Z, Xin L, Zisong X, Yue W, Zhiyuan T, Meijun A, Yuehui Z, Wenxu Z, Nan X, Guangyu S (2020) Toxic effects of heavy metals Pb and cd on mulberry (Morus alba L.) seedling leaves: photosynthetic function and reactive oxygen species (ROS) metabolism responses. Ecotoxicol Environ Saf 195:110469. https://doi.org/10.1016/j.ecoenv.2020.110469
Jalilvand N, Akhgar A, Alikhani HA, Rahmani HA, Rejali F (2020) Removal of heavy metals zinc, lead, and cadmium by biomineralization of urease-producing bacteria isolated from Iranian mine calcareous soils. J Soil Sci Plant Nutr 20:206–219. https://doi.org/10.1007/s42729-019-00121-z
Jáuregui-Zùñiga D, Ferrer MA, Calderón AA, Muñoz R, Moreno A (2005) Heavy metal stress reduces the deposition of calcium oxalate crystals in leaves of Phaseolus vulgaris. J Plant Physiol 162:1183–1187. https://doi.org/10.1016/j.jplph.2005.03.002
Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13:3145–3175. https://doi.org/10.3390/ijms13033145
Kabiri P, Motaghian H, Hosseinpur A (2020) Impact of biochar on release kinetics of Pb (II) and Zn (II) in a calcareous soil polluted with mining activities. J Soil Sci Plant Nutr 58:7296. https://doi.org/10.1007/s42729-020-00336-5
Khan I, Iqbal M, Shafiq F (2019) Phytomanagement of lead-contaminated soils: critical review of new trends and future prospects. Int J Environ Sci Technol 16:6473–6488. https://doi.org/10.1007/s13762-019-02431-2
Korth KL, Doege SJ, Park S-H, Goggin FL, Wang Q, Gomez SK, Liu G, Jia L, Nakata PA (2006) Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiol 141:188–195. https://doi.org/10.1104/pp.106.076737
Liu W, Hou J, Wang Q, Yang H, Luo Y, Christie P (2015) Collection and analysis of root exudates of Festuca arundinacea L. and their role in facilitating the phytoremediation of petroleum-contaminated soil. Plant Soil 389:109–119. https://doi.org/10.1007/s11104-014-2345-9
McBride MB, Kelch S, Schmidt M, Zhou Y, Aristilde L, Martinez CE (2019) Lead solubility and mineral structures of coprecipitated lead/calcium oxalates. Environ Sci Technol 53:13794–13801. https://doi.org/10.1021/acs.est.9b05638
Nakamura S-I, Suzui N, Yin Y-G, Ishii S, Fujimaki S, Kawachi N, Rai H, Matsumoto T, Sato-Izawa K, Ohkama-Ohtsu N (2020) Effects of enhancing endogenous and exogenous glutathione in roots on cadmium movement in Arabidopsis thaliana. Plant Sci 290:110304. https://doi.org/10.1016/j.plantsci.2019.110304
Nakata PA (2012) Plant calcium oxalate crystal formation, function, and its impact on human health. Front Biol 7:254–266. https://doi.org/10.1007/s11515-012-1224-0
Rojas-Loria CC, Favela-Torres E, González-Márquez H, Volke-Sepúlveda TL (2014) Role of glutathione and glutathione S-transferase in lead tolerance and bioaccumulation by Dodonaea viscosa (L.) Jacq. Acta Physiol Plant 36:2501–2510. https://doi.org/10.1007/s11738-014-1623-8
Rowley MC, Estrada-Medina H, Tzec-Gamboa M, Rozin A, Cailleau G, Verrecchia EP, Green I (2017) Moving carbon between spheres, the potential oxalate-carbonate pathway of Brosimum alicastrum Sw.; Moraceae. Plant Soil 412:465–479. https://doi.org/10.1007/s11104-016-3135-3
Snejana BD (2019) Deposition of calcium oxalate crystals and tolerance of deciduous trees to pollution. eJournal of Applied Forest Ecology 7:8–13. https://doi.org/10.1007/978-981-10-1201-3_10
Sun X, Han G, Ye S, Luo Y, Zhou X (2020) Effects of selenium on serotonin synthesis and the glutathione redox cycle in plum leaves. J Soil Sci Plant Nutr 64:215–2221. https://doi.org/10.1007/s42729-020-00288-w
Tan L, Xue X, Du J, Xie Y, Tang S-F, Hou X (2020) Probing the molecular toxic mechanism of lead (II) ions with glutathione peroxidase 6 from Arabidopsis thaliana. Spectrochim Acta A Mol Biomol Spectrosc 226:117597. https://doi.org/10.1016/j.saa.2019.117597
Tarasova E, Drogobuzhskaya S, Tapia-Pizarro F, Morev DV, Brykov VA, Dovletyarova EA, Slukovskaya M, Navarro-Villarroel C, Paltseva AA, Neaman A (2020) Vermiculite-Lizardite industrial wastes promote plant growth in a peat soil affected by a Cu/Ni smelter: a case study at the Kola Peninsula, Russia. J Soil Sci Plant Nutr 20:1013–1018. https://doi.org/10.1007/s42729-020-00188-z
Thanchanit T, Surawej N, Pornanong A (2018) Mulberry leaves and their potential effects against cardiometabolic risks: a review of chemical compositions, biological properties and clinical efficacy. Pharm Biol 56:109–118. https://doi.org/10.1080/13880209.2018.1424210
Tooulakou G, Giannopoulos A, Nikolopoulos D, Bresta P, Dotsika E, Orkoula MG, Kontoyannis CG, Fasseas C, Liakopoulos G, Klapa MI, Karabourniotis G (2016) Alarm photosynthesis: calcium oxalate crystals as an internal CO2 source in plants. Plant Physiol 171:2577–2585. https://doi.org/10.1104/pp.16.00111
Wang C-R, Tian Y, Wang X-R, Yu H-X, Lu X-W, Wang C, Wang H (2010) Hormesis effects and implicative application in assessment of lead-contaminated soils in roots of Vicia faba seedlings. Chemosphere 80:965–971. https://doi.org/10.1016/j.chemosphere.2010.05.049
Wójcik M, Dresler S, Tukiendorf A (2015) Physiological mechanisms of adaptation of Dianthus carthusianorum L. to growth on a Zn-Pb waste deposit—the case of chronic multi-metal and acute Zn stress. Plant Soil 390:237–250. https://doi.org/10.1007/s11104-015-2396-6
Zhang B-L, Guo C-C, Ding F, Lu Y-T, Fu Z-W (2019a) 14-3-3s function in plant cadmium response by changes of glutathione and glutathione synthesis in Arabidopsis. Environ Exp Bot 163:69–77. https://doi.org/10.1016/j.envexpbot.2019.04.009
Zhang X-M, Liu L-X, Su Z-M, Shen Z-J, Gao G-F, Yi Y, Zheng H-L (2019b) Transcriptome analysis of Medicago lupulina seedlings leaves treated by high calcium provides insights into calcium oxalate formation. Plant Soil 444:299–314. https://doi.org/10.1007/s11104-019-04283-8
Zulfiqar U, Farooq M, Hussain S, Maqsood M, Hussain M, Ishfaq M, Ahmad M, Anjum MZ (2019) Lead toxicity in plants: impacts and remediation. J Environ Manag 250:109557. https://doi.org/10.1016/j.jenvman.2019.109557
Acknowledgements
We would like to thank Dr. Jialing Cheng for his assistance with greenhouse work and thank Mr. Yongqing Lin for providing the seedlings.
Funding
This study was funded by the Innovative Foundation of Mulberry and Silkworm Research Institute, Chinese Academy of Agricultural Sciences (16JK005).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(PNG 74 kb)
Rights and permissions
About this article
Cite this article
Wang, L., Ji, G. Glutathione and calcium biomineralization of mulberry (Morus alba L.) involved in the heavy metal detoxification of lead-contaminated soil. J Soil Sci Plant Nutr 21, 1182–1190 (2021). https://doi.org/10.1007/s42729-021-00431-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-021-00431-1