Abstract
The objective of this study was to evaluate the physiological characteristics and rhizofiltration potential of Talinum paniculatum cuttings subjected to lead (Pb) and manganese (Mn) excess. The cuttings excised from T. paniculatum were transferred to a nutrient solution, to which different concentrations of Pb (0, 10, 50, 100, and 200 mg L−1) and Mn (0, 10, 50, 100, and 150 mg L−1) were added. The treatments were maintained for 30 days, then the roots and shoots were collected for the following analyses: biometry, root morphology, antioxidant enzyme activity, and lipid peroxidation. Gas exchange, relative chlorophyll content, and chlorophyll a fluorescence were analyzed at the beginning and end of the experiment. The tolerance index of T. paniculatum cuttings was over 70% for Pb and Mn. The root morphology and antioxidant system activity were the most related to the plant tolerance to excess Pb and Mn. T. paniculatum cuttings showed rapid rooting and growth, increased dry matter accumulation, high Pb and Mn accumulation in roots, and high resistance to Pb and Mn exposure in the hydroponic solution. Taking together, combined with the short life cycle, those characteristics suggest the potential of T. paniculatum use for rhizofiltration of Pb and Mn.
Similar content being viewed by others
Data Availability
Not applicable.
Code Availability
Not applicable.
References
Alaboudi, K. A., Ahmed, B., & Brodie, G. (2018). Phytoremediation of Pb and Cd contaminated soils by using sunflower (Helianthus annuus) plant. Annals of Agricultural Science, 63, 123–127. https://doi.org/10.1016/j.aoas.2018.05.007
Alamri, S. A., Siddiqui, M. H., Al-Khaishany, M. Y., et al. (2018). Ascorbic acid improves the tolerance of wheat plants to lead toxicity. J Plant Interact, 13, 409–419. https://doi.org/10.1080/17429145.2018.1491067
Alejandro, S., Höller, S., Meier, B., & Peiter, E. (2020). Manganese in plants: From acquisition to subcellular allocation. Frontiers in Plant Science, 11, 1–23. https://doi.org/10.3389/fpls.2020.00300
Amin, H., Arain, B. A., Jahangir, T. M., et al. (2018). Accumulation and distribution of lead (Pb) in plant tissues of guar (Cyamopsis tetragonoloba L.) and sesame (Sesamum indicum L.): Profitable phytoremediation with biofuel crops. Geol Ecol Landscapes, 2, 51–60. https://doi.org/10.1080/24749508.2018.1452464
Ashraf, U., Kanu, A. S., Deng, Q., et al. (2017). Lead (Pb) toxicity; physio-biochemical mechanisms, grain yield, quality, and pb distribution proportions in scented rice. Front Plant Sci, 8, Article 59. https://doi.org/10.3389/fpls.2017.00259
Ashraf, U., & Tang, X. (2017). Yield and quality responses, plant metabolism and metal distribution pattern in aromatic rice under lead (Pb) toxicity. Chemosphere, 176, 141–155. https://doi.org/10.1016/j.chemosphere.2017.02.103
Awa, S. H., & Hadibarata, T. (2020). Removal of heavy metals in contaminated soil by phytoremediation mechanism: A review. Water, Air, and Soil Pollution, 231, 47. https://doi.org/10.1007/s11270-020-4426-0
Bali, S., Jamwal, V. L., Kohli, S. K., et al. (2019). Jasmonic acid application triggers detoxification of lead (Pb) toxicity in tomato through the modifications of secondary metabolites and gene expression. Chemosphere, 235, 734–748. https://doi.org/10.1016/j.chemosphere.2019.06.188
Biemelt, S., Keetman, U., & Albrecht, G. (1998). Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiology, 116, 651–658. https://doi.org/10.1104/pp.116.2.651
Buege, J., & a., Aust SD,. (1978). [30] Microsomal lipid peroxidation. Methods in Enzymology, 52, 302–310. https://doi.org/10.1016/S0076-6879(78)52032-6
Cristaldi, A., Conti, G. O., Jho, E. H., et al. (2017). Phytoremediation of contaminated soils by heavy metals and PAHs. A Brief Review. Environmental Technology and Innovation, 8, 309–326. https://doi.org/10.1016/j.eti.2017.08.002
DalCorso, G., Fasani, E., Manara, A., et al. (2019). Heavy metal pollutions: State of the art and innovation in phytoremediation. International Journal of Molecular Sciences, 20, 3412. https://doi.org/10.3390/ijms20143412
de Souza, T. C., Castro, E. M., Magalhães, P. C., et al. (2012). Early characterization of maize plants in selection cycles under soil flooding. Plant Breeding, 131, 493–501. https://doi.org/10.1111/j.1439-0523.2012.01973.x
Demarco, C. F., Afonso, T. F., Pieniz, S., et al. (2020). Evaluation of Enydra anagallis remediation at a contaminated watercourse in south Brazil. International Journal of Phytoremediation, 22, 1216–1223. https://doi.org/10.1080/15226514.2020.1754759
Fontenele, N. M. B., de Otoch, M. L. O., Gomes-Rochette, N. F., et al. (2017). Effect of lead on physiological and antioxidant responses in two Vigna unguiculata cultivars differing in Pb-accumulation. Chemosphere, 176, 397–404. https://doi.org/10.1016/j.chemosphere.2017.02.072
Giannopolitis, C., & Ries, S. (1977). Superoxide dismutases. Plant Physiology, 59, 309–314. https://doi.org/10.1080/09553008314551231
González, Á., García-gonzalo, P., Gil-díaz, M. M., et al. (2019). Compost-assisted phytoremediation of As-polluted soil. Journal of Soils and Sediments, 19, 2971–2983. https://doi.org/10.1007/s11368-019-02284-9
Hasanuzzaman, M., Bhuyan, M. H. M. B., Anee, T. I., et al. (2019). Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants, 8, 384. https://doi.org/10.3390/antiox8090384
Havir, E., & a, McHale N a,. (1987). Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiology, 84, 450–455. https://doi.org/10.1104/pp.84.2.450
Hoagland DR, Arnon DI (1950). The water-culture method for growing plants without soil. Circ Calif Agric Exp Stn 347:
Ignatius, A., Arunbabu, V., Neethu, J., & Ramasamy, E. V. (2014). Rhizofiltration of lead using an aromatic medicinal plant Plectranthus amboinicus cultured in a hydroponic nutrient film technique (NFT) system. Environmental Science and Pollution Research, 21, 13007–13016. https://doi.org/10.1007/s11356-014-3204-1
Inostroza-Blancheteau, C., Reyes-Díaz, M., Berríos, G., et al. (2017). Physiological and biochemical responses to manganese toxicity in ryegrass (Lolium perenne L.) genotypes. Plant Physiology and Biochemistry, 113, 89–97. https://doi.org/10.1016/j.plaphy.2017.02.003
Jeevanantham, S., Saravanan, A., Hemavathy, R. V., et al. (2019). Removal of toxic pollutants from water environment by phytoremediation: A survey on application and future prospects. Environmental Technology and Innovation, 13, 264–276. https://doi.org/10.1016/j.eti.2018.12.007
Jolliffe, I. T., & Cadima, J. (2016). Principal component analysis: A review and recent developments. Philosophical Transactions of the Royal Society A - Mathematical Physical and Engineering Sciences, 374, 20150202. https://doi.org/10.1098/rsta.2015.0202
Kumar, A., & Majeti, N. V. P. (2014). Proteomic responses to lead-induced oxidative stress in Talinum triangulare Jacq. (Willd.) roots: Identification of key biomarkers related to glutathione metabolisms. Environmental Science and Pollution Research, 21, 8750–8764. https://doi.org/10.1007/s11356-014-2808-9
Kumar, A., & Prasad, M. N. (2010). Propagation of Talinum cuneifolium L. (Portulacaceae), an ornamental plant and leafy vegetable, by stem cuttings. Floric Ornam Biotechnol, 4, 68–71.
Kumar, A., Prasad, M. N. V., & Sytar, O. (2012). Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere, 89, 1056–1065. https://doi.org/10.1016/j.chemosphere.2012.05.070
Kumar, A., & Prasad, M. N. V. (2015). Lead-induced toxicity and interference in chlorophyll fluorescence in Talinum triangulare grown hydroponically. Photosynthetica, 53, 66–71. https://doi.org/10.1007/s11099-015-0091-8
Kumar, A., Prasad, M. N. V., Mohan Murali Achary, V., & Panda, B. B. (2013). Elucidation of lead-induced oxidative stress in Talinum triangulare roots by analysis of antioxidant responses and DNA damage at cellular level. Environmental Science and Pollution Research, 20, 4551–4561. https://doi.org/10.1007/s11356-012-1354-6
Lajayer, B. A., Moghadam, N. K., Maghsoodi, M. R., et al. (2019). Phytoextraction of heavy metals from contaminated soil, water and atmosphere using ornamental plants: Mechanisms and efficiency improvement strategies. Environmental Science and Pollution Research, 26, 8468–8484. https://doi.org/10.1007/s11356-019-04241-y
Lystvan, K., Listvan, V., Shcherbak, N., & Kuchuk, M. (2021). Rhizoextraction potential of Convolvulus tricolor hairy roots for Cr6+, Ni2+, and Pb2+ removal from aqueous solutions. Applied Biochemistry and Biotechnology, 193, 1215–1230. https://doi.org/10.1007/s12010-020-03471-y
Machado Filho, H. D. O., de Melo, J. I. M., & Sales, M. F. (2012). Flora da região de Xingó, Alagoas-Sergipe: Portulacaceae sensu lato. Biotemas, 25, 103–108. https://doi.org/10.5007/2175-7925.2012v25n4p103
Malavolta, E., Vitti, G., & Oliveira, S. (1997). Avaliação do estado nutricional das plantas: Princípios e aplicações (2nd ed.). Potafos.
Millaleo, R., Alvear, M., Aguilera, P., et al. (2020). Mn toxicity differentially affects physiological and biochemical features in highbush blueberry (Vaccinium corymbosum L.) cultivars. Journal of Soil Science and Plant Nutrition, 20, 795–805. https://doi.org/10.1007/s42729-019-00166-0
Millaleo, R., Rao, M., Ulloa-inostroza, E., et al. (2018). Early responses to manganese ( Mn ) excess and its relation to antioxidant performance and organic acid exudation in barley cultivars. Journal of Soil Science and Plant Nutrition, 18, 1206–1223.
Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbato specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22, 867–880.
Nelson, M., Adams, T., Ojo, C., et al. (2018). Manganese toxicity is targeting an early step in the dopamine signal transduction pathway that controls lateral cilia activity in the bivalve mollusc Crassostrea virginica. Comparative Biochemistry and Physiology, Part c: Toxicology & Pharmacology, 213, 1–6. https://doi.org/10.1016/j.cbpc.2018.07.002
Okoye, N. F., Monago-Ighorodge, C. C., & Akpobasaha, N. A. (2017). Evaluating the use of spiny pigweed (Amaranthus spinosus) and water leaf (Talinum triangulare) for bioremediation of crude oil polluted soil in Ikarama Community in Bayelsa State Nigeria. Journal of Applied Sciences and Environmental Management, 21, 903. https://doi.org/10.4314/jasem.v21i5.16
Pan, G., Liu, W., Zhang, H., & Liu, P. (2018). Morphophysiological responses and tolerance mechanisms of Xanthium strumarium to manganese stress. Ecotoxicology and Environmental Safety, 165, 654–661. https://doi.org/10.1016/j.ecoenv.2018.08.107
Pires-Lira, M. F., de Castro, E. M., Lira, J. M. S., et al. (2020). Potential of Panicum aquanticum Poir (Poaceae) for the phytoremediation of aquatic environments contaminated by lead. Ecotoxicol Environ Saf, 193, 110336.
Rahmani, G. N. H., & Sternberg, S. P. K. (1999). Bioremoval of lead from water using Lemna minor. Bioresource Technology, 70, 225–230. https://doi.org/10.1016/j.ecoenv.2020.110336
Rajkumar, K., Sivakumar, S., Senthilkumar, P., et al. (2009). Effects of selected heavy metals (Pb, Cu, Ni, and Cd) in the aquatic medium on the restoration potential and accumulation in the stem cuttings of the terrestrial plant, Talinum triangulare Linn. Ecotoxicology, 18, 952–960. https://doi.org/10.1007/s10646-009-0371-9
San Juan, M. R. F., Albornoz, C. B., Larsen, K., & Najle, R. (2018). Bioaccumulation of heavy metals in Limnobium laevigatum and Ludwigia peploides: Their phytoremediation potential in water contaminated with heavy metals. Environment and Earth Science, 77, 404. https://doi.org/10.1007/s12665-018-7566-4
Santos, E. F., Kondo Santini, J. M., Paixão, A. P., et al. (2017). Physiological highlights of manganese toxicity symptoms in soybean plants: Mn toxicity responses. Plant Physiology and Biochemistry, 113, 6–19. https://doi.org/10.1016/j.plaphy.2017.01.022
Scafidi, F., & Raimondo, F. M. (2017). Principi di spontaneizzazione in Sicilia di Talinum paniculatum (Talinaceae). Quad Di Bot Ambient e Appl, 26, 23–26.
Schück, M., & Greger, M. (2020). Plant traits related to the heavy metal removal capacities of wetland plants. International Journal of Phytoremediation, 22, 427–435. https://doi.org/10.1080/15226514.2019.1669529
Sha, S., Cheng, M., Hu, K., et al. (2019). Toxic effects of Pb on Spirodela polyrhiza (L.): Subcellular distribution, chemical forms, morphological and physiological disorders. Ecotoxicology and Environmental Safety, 181, 146–154. https://doi.org/10.1016/j.ecoenv.2019.05.085
Sharma, P., & Dubey, S. (2005). Lead toxicity in plants. Brazilian J Plant Physiol, 17, 35–52.
Souza GG de, Mendes Pinheiro AL, Silva JA, et al (2018). Morpho-physiological tolerance mechanisms of Talinum patens to lead. Water Air Soil Pollut 229:https://doi.org/10.1007/s11270-017-3658-0
Srivastava, A., Chahar, V., Sharma, V., et al. (2019). Study of toxic elements in river water and wetland using water hyacinth (Eichhornia crassipes) as pollution monitor. Glob Challenges, 3, 1800087. https://doi.org/10.1002/gch2.201800087
Syed Hasan, S. N. M., Mohd Kusin, F., Sue Lee, A. L., et al. (2017). Performance of vetiver grass (Vetiveria zizanioides) for phytoremediation of contaminated water. MATEC Web Conf, 103, 06003. https://doi.org/10.1051/matecconf/201710306003
van Kooten, O., & Snel, J. F. H. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research, 25, 147–150. https://doi.org/10.1007/BF00033156
Xue, S., Zhu, F., Wu, C., et al. (2015). Effects of manganese on the microstructures of Chenopodium ambrosioides L., A manganese tolerant plant. International Journal of Phytoremediation, 18, 710–719. https://doi.org/10.1080/15226514.2015.1131233
Xue, Z. C., Li, J. H., Li, D. S., et al. (2018). Bioaccumulation and photosynthetic activity response of sweet sorghum seedling (Sorghum bicolor L. Moench) to cadmium stress. Photosynthetica, 56, 1422–1428. https://doi.org/10.1007/s11099-018-0835-3
Zambrosi, F. C. B., Mesquita, G. L., Marchiori, P. E. R., et al. (2016). Anatomical and physiological bases of sugarcane tolerance to manganese toxicity. Environmental and Experimental Botany, 132, 100–112. https://doi.org/10.1016/j.envexpbot.2016.08.011
Zhu, G., Xiao, H., Guo, Q., et al. (2018). Heavy metal contents and enrichment characteristics of dominant plants in wasteland of the downstream of a lead-zinc mining area in Guangxi, Southwest China. Ecotoxicology and Environmental Safety, 151, 266–271. https://doi.org/10.1016/j.ecoenv.2018.01.011
Zulfiqar, U., Farooq, M., Hussain, S., et al. (2019). Lead toxicity in plants: Impacts and remediation. Journal of Environmental Management, 250, 109557. https://doi.org/10.1016/j.jenvman.2019.109557
Acknowledgements
The authors are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 for scholarships, Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial assistance.
Funding
This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (Financing Code 001).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design; the formal analysis and methodology were performed by PEdR, GFR, GdFE, and KYI. Data curation and original draft were performed by PEdR, GFR, and PCM. Review and editing were performed by KRDdS, PRdSF, and TCdS. The project was supervised by KRDdS and TCdS. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Conflict of Interest
The authors declare no competing interests.
Animal Research
Not applicable.
Clinical Trials Registration
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
dos Reis, P.E., de Souza, K.R.D., Romão, G.F. et al. Potential of Talinum paniculatum Cuttings in Lead and Manganese Rhizofiltration. Water Air Soil Pollut 233, 243 (2022). https://doi.org/10.1007/s11270-022-05731-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-022-05731-5