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The bioaccumulation potential of heavy metals by Gliricidia sepium (Fabaceae) in mine tailings

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Abstract

As a result of mining activities, waste of different types is generated. One example is mine tailings that contain potentially toxic elements such as heavy metals that negatively impact the environment and human health. Hence, developing treatments to guarantee its efficient elimination from the environment is necessary. Among these treatments, phytoremediation takes advantage of the potential of different plant species, to remove heavy metals from polluted sites. Gliricidia sepium is a tree that grows up to 15 m high and distributed from southern Mexico to Central America. This study evaluates the heavy metal bioaccumulation capacity in roots and leaves, and the effect of such bioaccumulation on fifteen macro- and one micro-morphological characters of G. sepium growing during 360 days in control, and in mine tailing substrates. G. sepium individuals growing on the exposed substrate registered the following average heavy metal bioaccumulation pattern in the roots: Fe > Pb > Zn > Cu, while in the leaf tissue, the bioaccumulation pattern was Cu > Fe > Pb > Zn. Macro- and micro-morphological characters evaluated in G. sepium decreased in plants exposed to metals. The translocation factor showed that Cu and Pb registered average values greater than 1. In conclusion, G. sepium is a species with potential for the phytoremediation of soils contaminated with Fe, Cu, and Pb, and for phytostabilizing soils polluted with Fe, Pb, Zn, and Cu, along with its ability to establish itself and turn into an abundant plant species in polluted sites, its capacity to bioaccumulate heavy metals in roots and leaves, and its high rate of HM translocation.

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References

  • Abhilash PC, Pandey VC, Srivastava P, Rakesh PS, Chandran S, Singh N, Thomas AP (2009) Phytofiltration of cadmium from water by Limnocharis flava (L.) Buchenau grown in free-floating culture system. J Hazard Mater 170:791–797. https://doi.org/10.1016/j.jhazmat.2009.05.035

    Article  CAS  Google Scholar 

  • Ahmad I, Akhtar MJ, Zahir ZA, Jamil A (2012) Effect of cadmium on seed germination and seedling growth of four wheat (Triticum aestivum L.) cultivars. Pakistan J Bot 44:1569–1574

    Google Scholar 

  • Ajeesh Krishna TP, Maharajan T, Victor Roch G, Ignacimuthu S, Antony Ceasar S (2020) Structure, function, regulation, and phylogenetic relationship of ZIP family transporters of plants. Front Plant Sci 11:1–18. https://doi.org/10.3389/fpls.2020.00662

    Article  Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals concepts and applications. Chemosphere 91:869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075

    Article  CAS  Google Scholar 

  • Appenroth KJ (2010) Definition of “heavy metals” and their role in biological systems. In: Sherameti I, Varma A (eds) Soil heavy metals. Soil Biology, Springer, Berlin, Heidelberg, pp 19–29. https://doi.org/10.1007/978-3-642-02436-8_2

  • Asati A, Pichhode M, Nikhil K (2016) Effect of heavy metals on plants: an overview. Int J Appl Innov Engin Manag 5:56–66

    Google Scholar 

  • Bacchetta G, Ballestreros D, Belletti P, Brullo S, Bueno A, Cagelli L, Cano Castillo M, Carasso V, Carriò E, Casas JL, Caujapé Castells J, Cervelli C, Draper D, Escribà Baeza MC, Fenu G, Gomez-Campo C, Gorian F, Grillo O, Güemes J, Jimenez-Alfaro B, Marques I, Mattana E, Mulè P, Nepi M, Pacini E, Pavone P, Piotto B, Pontecorvo C, Prada A, Serrano Martinez F, Venora G, Vietto L, Virevaire M (2008) Conservaciòn ex situ de plantas silvestres. Principado de Asturias, Spain, pp 1–375

    Google Scholar 

  • Batty LC, Younger PL (2003) Effects of external iron concentration upon seedling growth and uptake of Fe and phosphate by the common reed, Phragmites australis (Cav.) Trin ex. Steudel Ann Bot-London 92:801–806. https://doi.org/10.1093/aob/mcg205

    Article  CAS  Google Scholar 

  • Breton-Deval L, Guevara-Garcia A, Juarez K, Lara P, Rubio-Noguez D, Tovar-Sanchez E (2022) Role of rhizosphere microbiome during phytoremediation of heavy metals. In: Das S, Dash H (eds) Microbial biodegradation and bioremediation. Elsevier, Amsterdam, Netherlands, pp 263–291

    Chapter  Google Scholar 

  • Canul-Solís J, Alvarado-Canché C, Castillo-Sánchez L, Sandoval-Gío J, Alayón-Gamboa J, Piñeiro-Vázquez A, Chay-Canul A, Casanova-Lugo F, Ku-Vera J (2018) Gliricidia sepium (Jacq.) Kunth ex Walp. una especie arbórea multipropósito para la sustentabilidad de los agroecosistemas tropicales. Agroproductividad 11:195–201

    Google Scholar 

  • Csog Á, Mihucz VG, Tatár E, Fodor F, Virág I, Majdik C, Záray G (2011) Accumulation and distribution of iron, cadmium, lead and nickel in cucumber plants grown in hydroponics containing two different chelated iron supplies. J Plant Physiol 168:1038–1044. https://doi.org/10.1016/j.jplph.2010.12.014

    Article  CAS  Google Scholar 

  • Ćurguz VG, Raičević V, Veselinović M, Tabakovic-Tošić M, Vilotić D (2012) Influence of heavy metals on seed germination and growth of Picea abies L. Karst Pol J Environ Stud 21:355–361

    Google Scholar 

  • Dinu C, Vasile GG, Buleandra M, Popa DE, Gheorghe S, Ungureanu EM (2020) Traslocation and accumulation of heavy metals in Ocimum basilicum L. plants grown in a mining-contaminated soil. J Soil Sedim 1–14. https://doi.org/10.1007/s11368-019-02550-w

  • Feng NX, Yu J, Zhao HM, Cheng YT, Mo CH, Cai QY, Li YW, Li H, Wong MH (2017) Efficient phytoremediation of organic contaminants in soils using plant–endophyte partnerships. Sci Total Environ 583:352–368. https://doi.org/10.1016/j.scitotenv.2017.01.075

    Article  CAS  Google Scholar 

  • García-Sánchez IE, Barradas VL, de León P, Hill CA, Esperón-Rodríguez M, Pérez IR, Ballinas M (2019) Effect of heavy metals and environmental variables on the assimilation of CO2 and stomatal conductance of Ligustrum lucidum, an urban tree from Mexico City. Urban for Urban Green 42:72–81. https://doi.org/10.1016/j.ufug.2019.05.002

    Article  Google Scholar 

  • Gbedzi DD, Ofosu EA, Mortey EM, Obiri-Yeboah A, Nyantakyi EK, Siabi EK, Abdallah F, Domfeh MK, Amankwah-Minkah A (2022) Impact of mining on land use land cover change and water quality in the Asutifi North District of Ghana. West Africa Environ Challenges 6:100441. https://doi.org/10.1016/j.envc.2022.100441

    Article  CAS  Google Scholar 

  • Ghori NH, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16:1807–1828. https://doi.org/10.1007/s13762-019-02215-8

    Article  CAS  Google Scholar 

  • Gill M (2014) Heavy metal stress in plants: a review. Int J Adv Res 2:1043–1055

    Google Scholar 

  • Gold KP, León-Lobos Y, Way M (2004) Manual de recolección de semillas de plantas silvestres para conservación a largo plazo y restauración ecológico. Instituto de Investigaciones Agropecuarias, Centro Regional de Investigación Intihuasi, La Serena Boletín INIA 10:62

  • Gómez L, Contreras A, Bolonio D, Quintana J, Oñate-Sánchez L, Merino I (2019) Phytoremediation with trees. Adv Bot Res Elsevier 89:281–321. https://doi.org/10.1016/bs.abr.2018.11.010

    Article  CAS  Google Scholar 

  • Grillet L, Mari S, Schmidt W (2014) Iron in seeds–loading pathways and subcellular localization. Front Plant Sci 4:535. https://doi.org/10.3389/fpls.2013.00535

    Article  Google Scholar 

  • Hall JS, Ashton MS, Garen EJ, Jose S (2011) The ecology and ecosystem services of native trees: implications for reforestation and land restoration in Mesoamerica. For Ecol Manag 261:1553–1557. https://doi.org/10.1016/j.foreco.2010.12.011

    Article  Google Scholar 

  • He H, Bleby TM, Veneklaas EJ, Lambers H, Kuo J (2012) Morphologies and elemental compositions of calcium crystals in phyllodes and branchlets of Acacia robeorum (Leguminosae: Mimosoideae). Ann Bot 109:887–896. https://doi.org/10.1093/aob/mcs004

    Article  CAS  Google Scholar 

  • Hernández-Lorenzo B (2015) Análisis de la anatomía y morfología de Prosopis laevigata, por acumulación de metales pesados en la Sierra de Huautla, Morelos. Dissertation, Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos, Cuernavaca, Mexico

  • Juge C, Cossette N, Jeanne T, Hogue R (2021) Long-term revegetation on iron mine tailings in northern Québec and Labrador and its effect on arbuscular mycorrhizal fungi. Appl Soil Ecol 168:104145. https://doi.org/10.1016/j.apsoil.2021.104145

    Article  Google Scholar 

  • Kahle H (1993) Response of roots of trees to heavy metals. Environ Exp Bot 33:99–119. https://doi.org/10.1016/0098-8472(93)90059-o

    Article  Google Scholar 

  • Kamari A, Pulford ID, Hargreaves JSJ (2012) Metal accumulation in Lolium perenne and Brassica napus as afected by application of chitosans. Int J Phytoremediation 14(9):894–907. https://doi.org/10.1080/15226514.2011.636401

    Article  CAS  Google Scholar 

  • Kamari A, Mohd-Yusoff SN, Putra WP, Ishak CF, Hashim N, Mohamed A, Phillip E (2014) Metal uptake in water spinach grown on contaminated soil amended with chicken manure and coconut tree sawdust. Environ Eng Manag J 13(9):2219–2228

  • Kinoshita T, Toh S, Torii KU (2021) Chemical control of stomatal function and development. Curr Opin Plant Biol 60:102010. https://doi.org/10.1016/j.pbi.2021.102010

    Article  CAS  Google Scholar 

  • Kumarathilaka P, Vithanage M (2017) Influence of Gliricidia sepium biochar on attenuate perchlorate-induced heavy metal release in serpentine soil. J Chem 1-8.https://doi.org/10.1155/2017/6180636

  • Lam EJ, Cánovas M, Gálvez ME, Montofré ÍL, Keith BF, Faz Á (2017) Evaluation of the phytoremediation potential of native plants growing on a copper mine tailing in northern Chile. J Geochem Explor 182:210–217. https://doi.org/10.1016/j.gexplo.2017.06.015

    Article  CAS  Google Scholar 

  • Lam EJ, Gálvez ME, Cánovas M, Montofré ÍL, Keith BF (2018) Assessment of the adaptive capacity of plant species in copper mine tailings in arid and semiarid environments. J Soils Sediments 18:2203–2216. https://doi.org/10.1007/s11368-017-1835-9

    Article  CAS  Google Scholar 

  • EJ, Keith BF, Bech J, Alvarez FA, Zetola V, Pereira LH, Montofré ÍL (2022) Characteristic curve modeling of plant species behavior in soils with heavy metals. Environ Geochem Health 1-14https://doi.org/10.1007/s10653-022-01342-5

  • Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytol 181:13–34. https://doi.org/10.1111/j.1469-8137.2008.02685.x

    Article  CAS  Google Scholar 

  • Liu W, Ni J, Zhou Q (2013) Uptake of heavy metals by trees: prospects for phytoremediation. Mater Sci Forum 743–744:768–781. https://doi.org/10.4028/www.scientific.net/MSF.743-744.768

    Article  CAS  Google Scholar 

  • Lorenzo-Barrera N (2017) Bioacumulación y efecto de los metales pesados en Acacia farnesiana expuesta a jales mineros: análisis de su potencial para fitorremediación. Dissertation, Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos, Cuernavaca, Mexico

  • Louca S, Doebeli M (2018) Efficient comparative phylogenetics on large trees. Bioinformatics 34:1053–1055. https://doi.org/10.1093/bioinformatics/btx701

    Article  CAS  Google Scholar 

  • Mihucz VG, Csog Á, Fodor F, Tatár E, Szoboszlai N, Silaghi-Dumitrescu L, Záray G (2012) Impact of two iron(III) chelators on the iron, cadmium, lead and nickel accumulation in poplar grown under heavy metal stress in hydroponics. J Plant Physiol 169:561–566. https://doi.org/10.1016/j.jplph.2011.12.012

    Article  CAS  Google Scholar 

  • Muro-González DA, Mussali-Galante P, Valencia-Cuevas L, Flores-Trujillo K, Tovar-Sánchez E (2020) Morphological, physiological, and genotoxic effects of heavy metal bioaccumulation in Prosopis laevigata reveal its potential for phytoremediation. Environ Sci Pollut Res 27:40187–40204. https://doi.org/10.1007/s11356-020-10026-5

    Article  CAS  Google Scholar 

  • Mussali-Galante P, Tovar-Sánchez E, Valverde M, Valencia-Cuevas L, Rojas E (2013) Evidence of population genetic effects in Peromyscus melanophrys chronically exposed to mine tailings in Morelos, Mexico. Environ Sci Pollut Res 20:7666–7679. https://doi.org/10.1007/s11356-012-1263-8

  • Ogbonna CE, Nwafor FI, Ogbonnaya OO (2020) Dust accumulation, heavy metal content and stomata morphology of some medicinal plants at Rock Quarrying locations at Lokpaukwu, Nigeria. Br J Environ Clim Chang 10:540–549

    Google Scholar 

  • Olguín EJ, Sánchez-Galván G (2012) Heavy metal removal in phytofiltration and phycoremediation: the need to differentiate between bioadsorption and bioaccumulation. New Biotechnol 30:3–8. https://doi.org/10.1016/j.nbt.2012.05.020

    Article  CAS  Google Scholar 

  • Orroño DI, Schindler V, Lavado RS (2012) Heavy metal availability in pelargonium hortorum rhizosphere: interactions, uptake and plant accumulation. J Plant Nutr 35:1374–1386. https://doi.org/10.1080/01904167.2012.684129

    Article  CAS  Google Scholar 

  • Pajević S, Borišev M, Nikolić N, Arsenov DD, Orlović S, Župunski M (2016) Phytoextraction of heavy metals by fast-growing trees: a review. Phytoremediation 29-64.https://doi.org/10.1007/978-3-319-40148-5_2

  • Parrotta JA (1992). Gliricidia sepium (Jacq.) Walp. Leguminosae (Papilionoideae). Agrof Syst 22:25

  • Peng JS, Guan YH, Lin XJ, Xu XJ, Xiao L, Wang HH, Meng S (2021) Comparative understanding of metal hyperaccumulation in plants: a mini-review. Environ Geochem Health 43:1599–1607. https://doi.org/10.1007/s10653-020-00533-2

    Article  CAS  Google Scholar 

  • Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181. https://doi.org/10.1016/j.plantsci.2010.08.016

    Article  CAS  Google Scholar 

  • Recena R, García-López AM, Delgado A (2021) Zinc uptake by plants as affected by fertilization with Zn sulfate, phosphorus availability, and soil properties. Agronomy 11:390. https://doi.org/10.3390/agronomy11020390

    Article  CAS  Google Scholar 

  • Robin Supriyono E, Nirmala K, Harris E, Affandi R, Jusadi D (2017) Bio-elimination of lead (Pb) from the organs of red tilapia (Oreochromis sp.) using Gliricidia sepium compost as a feed additive. AACL Bioflux 10:38–47

    Google Scholar 

  • Rosas-Ramírez M (2018) Relación entre la bioacumulación de metales pesados y la concentración de clorofila en Sanvitalia procumbens. Dissertation, Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos, Cuernavaca, Mexico

  • Rubiya S, Dhriti K, Bhat AA (2018) Heavy metal toxicity in plants: a review. Plant Arch 18:1229–1238

    Google Scholar 

  • Santoyo-Martínez M (2020) Estudio ecotoxicológico sobre la bioacumulación de metales pesados en dos especies vegetales asociadas a los jales de Huautla, Morelos. Ph.D. dissertation, Universidad Autónoma del Estado de Morelos, Cuernavaca, Mexico

  • Santoyo-Martínez M, Mussali-Galante P, Hernández-Plata I, Valencia-Cuevas L, Flores-Morales A, Ortiz-Hernández L, Flores-Trujillo K, Ramos-Quintana F, Tovar-Sánchez E (2020) Heavy metal bioaccumulation and morphological changes in Vachellia campechiana (Fabaceae) reveal its potential for phytoextraction of Cr, Cu, and Pb in mine tailings. Environ Sci Pollut Res 27:11260–11276. https://doi.org/10.1007/s11356-020-07730-7

    Article  CAS  Google Scholar 

  • SEMARNAT (2005). Evaluación de tecnologías de remediación para suelos contaminados con metales, Etapa II. Secretaría del Medio Ambiente y Recursos Naturales – Instituto Nacional de Ecología, SEMARNAT-INE, Mexico City, Mexico pp 36

  • Solís-Miranda M (2016) Aislamiento de bacterias de jales mineros y análisis de su potencial para la remediación de sitios contaminados con metales pesados. MSc dissertation, Universidad Autónoma del Estado de Morelos, Cuernavaca, Mexico

  • Stacey MG, Patel A, McClain WE, Mathieu M, Remley M, Rogers EE, Gassmann W, Blevins DG, Stacey G (2008) The ArabidopsisAtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol 146:589–601

    Article  CAS  Google Scholar 

  • Statsoft INC (2007) Statistica for windows. Tulsa, USA

    Google Scholar 

  • Suganya E, Saranya N, Patra C, Alen L, Selvaraju N (2019) Biosorption potential of Gliricidia sepium leaf powder to sequester hexavalent chromium from synthetic aqueous solution. J Environ Chem Eng 7:103112. https://doi.org/10.1016/j.jece.2019.103112

    Article  CAS  Google Scholar 

  • Sytar O, Ghosh S, Malinska H, Zivcak M, Brestic M (2021) Physiological and molecular mechanisms of metal accumulation in hyperaccumulator plants. Physiol Plant 173:148–166. https://doi.org/10.1111/ppl.13285

    Article  CAS  Google Scholar 

  • Thakur P (1990) Different physiological responses of tomato (Lucopersicom esculetum Mill.) cultivars to drought. Acta Physiol Plant 12:175–182

    CAS  Google Scholar 

  • Tovar-Sánchez E, Hernández-Plata I, Martínez MS, Valencia-Cuevas L, Mussali-Galante P (2018) Heavy metal pollution as a biodiversity threat. In: Hosam El-Din M, Saleh Aglan R (eds) Heavy metals. IntechOpen, pp 384–399. https://doi.org/10.5772/intechopen.74052

  • Trumbore S, Brando P, Hartmann H (2015) Forest health and global change. Science 349:814–818. https://doi.org/10.1126/science.aac6759

    Article  CAS  Google Scholar 

  • Tyler G, Zohlen A (1998) Plant seeds as mineral nutrient resource for seedlings—a comparison of plants from calcareous and silicate soils. Ann Bot 81:455–459. https://doi.org/10.1006/anbo.1997.0581

    Article  Google Scholar 

  • Vázquez-Yanes C, Batis AI (1996) Adopción de árboles nativos valiosos para la restauración ecológica y la reforestación. Bot Sci 58:75–84

  • Velásquez JR, Schwartz M, Phipps LM, Restrepo-Baena OJ, Lucena J, Smits KM (2021) A review of the environmental and health implications of recycling mine tailings for construction purposes in artisanal and small-scale mining communities. Extr Ind Soc 9:101019. https://doi.org/10.1016/j.exis.2021.101019

    Article  Google Scholar 

  • Volke ST, Velasco TA, De la Rosa PA, Solórzano OG (2005) Evaluación de tecnologías de remediación para suelos contaminados con metales. Etapa II. Secretaría de Medio Ambiente y Recursos Naturales, Mexico

  • Wang L, Ji B, Hu Y, Liu R, Sun W (2017) A review on in situ phytoremediation of mine tailings. Chemosphere 184:594–600. https://doi.org/10.1016/j.chemosphere.2017.06.025

    Article  CAS  Google Scholar 

  • Wu D, Saleem M, He T, He G (2021) The mechanism of metal homeostasis in plants: a new view on the synergistic regulation pathway of membrane proteins, lipids and metal ions. Membranes (basel) 11:984. https://doi.org/10.3390/membranes11120984

    Article  CAS  Google Scholar 

  • Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S, Chen Z (2020) Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front Plant Sci 11:1–15. https://doi.org/10.3389/fpls.2020.00359

    Article  Google Scholar 

  • Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464. https://doi.org/10.1016/j.scitotenv.2006.01.016

    Article  CAS  Google Scholar 

  • Zar JH (2010) Biostatistical analysis. Prentice Hall, New Jersey

    Google Scholar 

  • Zimmermann M (2001) Adaptaciones de plantas a estrés abiótico que les permiten vivir y prosperar en diferentes condiciones ambientales. Rev Creces 25–43

Download references

Acknowledgements

We thank the “Doctorado en Ciencias Naturales,” Autonomous University of Morelos State (UAEM), for the facilities granted to carry out this project. This research was supported by a CONACyT scholarship grant to M.S.M. (Grant: 307350). Also, we thank Rosalind Pearson Hedge for her comments and English edition that improved our manuscript.

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Conceptualization: ET-S; methodology: ET-S, PM-G, MS-M; validation: ET-S, MLC-G, PM-G; formal analysis: ET-S, MS-M; writing—original draft preparation: ET-S, MLC-G, LB-D; writing—review and editing: ET-S, PM-G, LV-C, AR-S; supervision: ET-S. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Efraín Tovar-Sánchez.

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Mussali-Galante, P., Santoyo-Martínez, M., Castrejón-Godínez, M.L. et al. The bioaccumulation potential of heavy metals by Gliricidia sepium (Fabaceae) in mine tailings. Environ Sci Pollut Res 30, 38982–38999 (2023). https://doi.org/10.1007/s11356-022-24904-7

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