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Morphological, physiological, and genotoxic effects of heavy metal bioaccumulation in Prosopis laevigata reveal its potential for phytoremediation

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Abstract

Mining industry generates large volumes of waste known as mine tailings, which contain heavy metals (HMs) that generate a risk to environmental health. Thus, remediation of HM pollution requires attention. In this study, HM bioaccumulation, genotoxic damage, and morphological and physiological changes in the tree species Prosopis laevigata were evaluated in order to assess its potential for remediation of mine tailings. P. laevigata plants were established in two treatments (reference substrate and tailing substrate) under greenhouse conditions. Every 2 months, six individuals were selected per treatment for 1 year. From each individual, macromorphological (height, stem diameter, and number of leaves), micromorphological (stomatal coverage and stomatal index), and physiological parameters (chlorophyll content) were evaluated, as well as the concentration of Pb, Cu, Cd, Cr, Fe, and Zn in root and foliar tissue. Genetic damage was assessed by the comet assay in foliar tissue. These parameters were evaluated in adult individuals established in mine tailings. Roots bioaccumulated significantly more HM compared to foliar tissue. However, the bioaccumulation pattern in both tissues was Fe > Pb > Zn > Cu. The plants in tailing substrate reduced significantly the morphological and physiological characters throughout the experiment. Only the bioaccumulation of Pb affected significantly the levels of genetic damage and the number of leaves, while Zn reduced plant height. The percentage of plants that have translocation factor values greater than 1 are Cu (92.9) > Fe (85.7) > Pb (75.0) > Zn (64.3). P. laevigata has potential to phytoremediate environments contaminated with metals, due to its dominance and establishment in abandoned mine tailings, and its ability to bioaccumulate HM unaffecting plant development, as well as their high levels of HM translocation.

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References

  • Aggarwal A, Sharma I, Tripathi B, Munjal A, Baunthiyal M, Sharma V (2012) Metal toxicity and photosynthesis. Photosynthesis: overviews on recent progress and future perspectives, 229–236

  • Alcalá Jáuregui J, Rodríguez Ortíz JC, Hernández Montoya A, Filippini MF, Martínez Carretero E, Díaz Flores PE (2018) Capacity of two vegetative species of heavy metal accumulation. Rev FCA UNCUYO 50(1):123–139

    Google Scholar 

  • Ali H, Khan E, Sjad 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 

  • Ali MR, Mehraj H, Jamal Uddin AFM (2015) Effects of foliar application of zinc and boron on growth and yield of summer tomato. Biosci Agric Res 06:512–517. https://doi.org/10.18801/jbar.060115.61

    Article  Google Scholar 

  • Ambler JE, Brown JC, Gauch HG (1971) Sites of Iron reduction in soybean plants. Agron J 63:9597

    Article  Google Scholar 

  • Arena C, Figlioli F, Sorrentino MC, Izzo LG, Capozzi F, Giordano S, Spagnuolo V (2017) Ultrastructural, protein and photosynthetic alterations induced by Pb and Cd in Cynara cardunculus L., and its potential for phytoremediation. Ecotox Environ Safe 145:83–89. https://doi.org/10.1016/j.ecoenv.2017.07.015

    Article  CAS  Google Scholar 

  • Ayeni O, Ndakidemi PA, Snyman RG, Odendaal JP (2010) Chemical, biological and physiological indicators of metal pollution in wetlands. Sci Res Essays 5:1938–1949. https://doi.org/10.5897/SER

    Article  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(6):801–806. https://doi.org/10.1093/aob/mcg205

    Article  CAS  Google Scholar 

  • Benimeli CS, Medina A, Navarro CM, Medina RB, Amoroso MJ, Gómez MI (2010) Bioaccumulation of copper by Zea mays: impact on root, shoot and leaf growth. Water Air Soil Pollut 210(1–4):365–370. https://doi.org/10.1007/s11270-009-0259-6

    Article  CAS  Google Scholar 

  • Bhatla SC (2018) Light perception and transduction. In: Bhatla SC, Lal MA (eds) Plant physiology. Development and Metabolism Springer, Singapore, pp 519–558

    Google Scholar 

  • Buendía-González L, Orozco-Villafuerte B, Cruz-Sosa F, Barrera-Díaz CE, Vernon-Carte EJ (2010) Prosopis laevigata, a potencial chromium (VI) and cadmium (II) hyperaccumulator desert plant. Bio/Technology 101:5862–5867. https://doi.org/10.1016/j.biortech.2010.03.027

    Article  CAS  Google Scholar 

  • Buendía González L, Cruz Sosa F, Rodríguez Huezo ME, Barrera Díaz CE, Hernández Jaimes C, Orozco Villafuerte J (2019) In vitro simultaneous acummulation of multiple heavy metals by Prosopis laevigata seedlings cultures. Rev Mex Ing Quím 18(3):1167–1177

    Article  Google Scholar 

  • Capozzi F, Sorrentino MC, Caporate AG, Fiorentino N, Giordano S, Spagnuolo V (2020) Exploring the phytoremediation potencial of Cynara cardunculus: a trial on an industrial soil highly cobtaminated by heavy metals. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-019-07575-9

  • Casana MM, Beltrán RA (2017) Bioacumulación de cobre, plomo, hierro y zinc en Lactuca sativa “lechuga”, Brassica oleracea “repollo”, Daucus carota “zanahoria” y Raphanus sativus “rabanito”. Conocimiento para el desarrollo 4(2) https://revista.usanpedro.edu.pe/index.php/CPD/article/view/167

  • Cenkci S, Cigerci IH, Yildiz M, Özay C, Bozdag A, Terzi H (2010) Lead contamination reduces chlorophyll biosynthesis and genomic template stability in Brassica rapa L. Environ Exp Bot 67:467–473. https://doi.org/10.1016/j.envexpbot.2009.10.001

    Article  CAS  Google Scholar 

  • Chaoui A, El Ferjani E (2005) Effects of cadmium and copper on antioxidant capacities, lignification and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. C R Biol 328(1):23–31. https://doi.org/10.1016/j.crvi.2004.10.001

    Article  CAS  Google Scholar 

  • Chaudhry H, Nisar N, Mehmood S, Iqbal M, Nazir A, Yasir M (2020) Indian mustard Brassica juncea efficiency for the accumulation, tolerance and traslocation of zinc from metal contaminated soil. Biocatal Agric Biotechnol 23. https://doi.org/10.1016/j.bcab.2019.101489

  • Covarrubias SA, Peña Cabriales JJ (2017) Contaminación por metales pesados en México: Problemática y estrategias de fitorremediación. Rev Int Cont Amb 7-21. https://doi.org/10.20937/RICA.2017.33.esp01.01

  • Cuypers A, Remans T, Weyens N, Colpaert J, Vassilev A, Vangronsveld J (2013) Soil-plant relationships of heavy metals and metalloids. In: Alloway BJ (ed) Heavy metals in soils: trace metals and metalloids in soils and their bioavailability. Dordrecht, the Netherlands: Springer, 161–193

  • DalCorso G (2012) Heavy metal toxicity in plants. In: Furini A (ed) Plants and heavy metals SpringerBriefs in Molecular Science. Springer, Dordrecht pp 1–25. https://doi.org/10.1007/978-94-007-4441-7_1

  • De la Cruz-Landero N, Hernández VE, Guevara E, López-López MA, Santos AT, Ojeda-Trejo E, Alderete Chavez A (2010) Lipinus versicolor response in soils contaminated with heavy metals from a petroleum extraction field. J Appl Sci 10(8):694–609

    Article  Google Scholar 

  • De la Rosa G, Cruz G, Cano I, Fuentes R, Gardea JL (2008) Efecto de la edad de la planta y presencia de SS-EDDS en la tolerancia y absorción de Cr (III) por Helianthus annuus. Rev Mex Ing Quim 7:243–251

    Google Scholar 

  • Delgadillo-López AE, González-Ramírez CA, Prieto-García F, Villagómez-Ibarra JR, Acevedo-Sandoval O (2011) Fitorremediación: Una alternativa para eliminar la contaminación. Tropic Subtropic Agroecosyst 14:597–612

    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

  • Dorado O, Arias D, Ramírez R, Sousa M (2005) Leguminosas de la Sierra de Huautla Universidad Autónoma del Estado de Morelos Centro de Educación Ambiental e Investigación Sierra de Huautla 176

  • Ercal N, Gurer Orhan H, Aykin Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem 1(6):529–539. https://doi.org/10.2174/1568026013394831

    Article  CAS  Google Scholar 

  • Eun SO, Youn HS, Lee Y (2000) Lead disturbs microtubule organization in the root meristem of Zea mays. Physiol Plant 110:357–365. https://doi.org/10.1111/j.1399-3054.2000.1100310.x

    Article  CAS  Google Scholar 

  • Frankenberger WT Jr, Arshad M (2020) Phytohormones in soils microbial production & function. CRC Press

  • García-Sánchez R, Camargo-Ricalde SL, García-Moya E, Luna-Cavazos M, Romero-Manzanarez A, Montaño M (2012) Prosopis laevigata and Mimosa biuncifera (Leguminosae), jointly influence plant diversity and soil fertility of a Mexican semiarid ecosystem. Rev Biol Trop 60:87–103

    Article  Google Scholar 

  • García V (2006) Efectos fisiológicos y compartametalización radicular en plantas de Zea mays L. expuestas a la toxicidad por plomo. Dissertation, Universidad Autónoma de Barcelona

  • Gichner T, Patková Z, Száková J, Demnerová K (2006) Toxicity and DNA damage in tobacco and potato plants growing on soil polluted with heavy metals. Ecotox Environ Safe 65:420–426. https://doi.org/10.1016/j.ecoenv.2005.08.006

    Article  CAS  Google Scholar 

  • Gold-Bouchot G, Zapata-Pérez O (2004) Contaminación, ecotoxicología y manejo costero. In: El Manejo Costero en México. Rivera Arriaga E, Villalobos GJ, Azuz Adeath I, Rosado May F. (eds) Universidad Autónoma de Campeche, SEMARNAT, CETYS-Universidad, Universidad de Quintana Roo, Campeche, Mexico. 654: 277–286

  • Golubov J, Mandujano MC, Eguiarte LE (2001) The paradox of mesquites (Prosopis spp.): invading species or biodiversity enhancers? Bot Sci 69:23–30. https://doi.org/10.17129/botsci.1644

    Article  Google Scholar 

  • Gonçalves AC Jr, Schwantes D, Braga de Sousa RF, Benetoli da Silva TR, Guimar VF, Campagnolo MA, Soares de Vasconcelos E, Zimmermann J (2020) Phytoremediation capacity, growth and physiological responses of Crambe abyssinica Hochst on soil contaminated with Cd and Pb. J Environ Manag 262:110432. https://doi.org/10.1016/j.jenvman.2020.110342

    Article  CAS  Google Scholar 

  • Guala SD, Vega FA, Covelo EF (2010) The dynamics of heavy metals in plant–soil interactions. Ecol Model 221:1148–1152

    Article  CAS  Google Scholar 

  • Guo Z, Miao X (2010) Growth changes and tissues anatomical characteristics of giant reed (Arundo donax L.) in soil contaminated with arsenic, cadmium and lead. J Cent South Univ T 17:770–777. https://doi.org/10.1007/s11771−010−0555−8

  • Guo J, Shi R, Cao Y, Luan Y, Zhou Y, Gao Y, Tian Y (2020) Genotoxic effects of imidacloprid in human lymphoblastoid TK6 cells. Drug Chem Toxicol 43:208–212. https://doi.org/10.1080/01480545.2018.1497048

    Article  CAS  Google Scholar 

  • Helmstädter A (2008) Is there a tonic in the toxin? The Arndt–Schulze law as an explanation for non-linear dose–response relationships, In: Balz V, Schwerin A.v, Stoff H, Wahrig B (eds) Precarious Matters. The History of Dangerous and Endangered Substances in the 19th and 20th Centuries, Max Planck Institut für Wissenschaftsgeschichte, Berlin, pp. 29–37

  • Hernández-Acosta E, Mondragón-Romero E, Cristobal-Acevedo D, Rubiños-Panta JE, Robledo-Santoyo E (2009) Vegetación, residuos de mina y elementos potencialmente tóxicos de un jal de Pachuca, Hidalgo, México. Rev Chapingo Ser Cie 15(2):109–114

    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. Universidad Autónoma del Estado de Morelos, Dissertation https://documentcloud.adobe.com/link/track?uri=urn:aaid:scds:US:f1e6be7a-3573-45ac-8d0f-bd0dd2f859d1

    Google Scholar 

  • Huihuia Z, Xina L, Zisonga X, Yueb W, Zhiyuanb T, Meijunc A, Yuehuic Z, Wenxud Z, Nanb X, Guangyub 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. Ecotox Environ Safe 195. https://doi.org/10.1016/j.ecoenv.2020.110469

  • Ibarra-García AR, Barceló-Quintal ID, García-Albortante J, López-Lafuente AL, González-Huecas C, Quintana-Nieto JR, Mugica-Alvarez V (2017) Phytoextraction of metals by native plants from mining wastes in Zacatecas, Mexico. Acta Hortic 1227:409–416. https://doi.org/10.17660/ActaHortic.2018.1227.51

  • INEGI (Instituto Nacional de Estadística y Geografía) (2016) Sistema de cuentas nacionales de México. http://www.inegi.org.mx/sistemas/bie

  • Kabata-Pendias A (2011) Trace elements in soil and plants, 4th edn. CRC Press, Boca Raton

    Google Scholar 

  • Kathpalia R, Bhatla SC (2018) Plant water relations. In: Bhatla SC, Lal MA (eds) Plant physiology. Development and Metabolism Springer, Singapore, pp 37–81

    Google Scholar 

  • Kaya C, Higgsb D, Ashrafc M, Alyemenid MN, Ahmadd P (2020) Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) plants to iron deficiency and salt stress alone or in combination. Physiol Plant 168:256–277. https://doi.org/10.1111/ppl.12976

    Article  CAS  Google Scholar 

  • Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13. https://doi.org/10.1016/j.envexpbot.2009.10.011

    Article  CAS  Google Scholar 

  • Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, Wang Q, Li R, Zhang Z (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotoxicol Environ Saf 126:111–121. https://doi.org/10.1016/j.ecoenv.2015.12.023

    Article  CAS  Google Scholar 

  • Manara A (2012) Plant responses to heavy metal toxicity. In: Furini A (ed) Plant and heavy metals. Springer Science & Business Media, Pisa, Italy, pp 27–53

    Chapter  Google Scholar 

  • Mei Y, Zhou H, Gao L, Zuo YM, Wei KH, Cui NQ (2020) Accumulation of Cu, Cd, Pb, Zn and total P fromsynthetic stormwater in 30 bioretention plants. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-020-07731-6

  • Mojiri A, Aziz HA, Zahed MA, Aziz SQ, Selamat MRB (2013) Phytoremediation of heavy metals from urban waste leachate by southern cattail (Typha domingensis). Int J Sci Res Environ Sci 1:63–70

    Google Scholar 

  • Mousavi Kouhi SM, Moudi M (2020) Assessment of phytoremediation potential of native plant species naturally growing in a heavy metal-polluted saline–sodic soil. Environ Sci Pollut Res 27:10027–10038. https://doi.org/10.1007/s11356-019-07578-6

    Article  CAS  Google Scholar 

  • Murillo-Herrera AI (2015) Detección de daño genotóxico en Prosopis laevigata de los jales de Sierra de Huautla, Morelos, México provocado por metales pesados. Universidad Nacional Autónoma de México, Dissertation https://documentcloud.adobe.com/link/track?uri=urn:aaid:scds:US:5d2461a0-1ec2-4d8a-96f3-1ea8ae5f5174

    Google Scholar 

  • Mussali-Galante P, Ávila Costa MR, Piñón Zarate G, Martínez Levy G, Rodríguez Lara V, Rojas Lemus M, Fortoul TI (2005) DNA damage as an early biomarker of effect in human health. Toxicol Ind Health 21(5–6):155–166. https://doi.org/10.1191/0748233705th224oa

    Article  CAS  Google Scholar 

  • Mussali-Galante P, Tovar Sánchez E, Valverde M, Rojas del Castillo E (2013) Biomarkers of exposure for assessing environmental metal pollution: from molecules to ecosystems. Rev Int Contam Ambie 29:117–140

    CAS  Google Scholar 

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216. https://doi.org/10.1007/s10311-010-0297-8

    Article  CAS  Google Scholar 

  • Navarrete Gutiérrez DM, Pons MN, Cuevas Sánchez JA, Echevarria G (2018) Is metal hyperaccumulation occurring in ultramafic vegetation of central and southern Mexico? Ecol Res 33:641–649. https://doi.org/10.1007/s11284-018-1574-4

    Article  CAS  Google Scholar 

  • Olguín E, 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 

  • Paniagua-Ibáñez M, López-Caamal A, Mussali-Galante P, Sánchez-Salinas E, Ortiz-Hernández LM, Ramírez-Rodríguez R, Tovar-Sánchez E (2015) Morphological variation of Cosmos bipinnatus (Asteraceae) and its relation to abiotic variables in Central Mexico. Rev Chil Hist Nat:2–13. https://doi.org/10.1186/s40693-015-0044-4

  • Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52(3):199–223. https://doi.org/10.1016/j.envexpbot.2004.02.009

    Article  CAS  Google Scholar 

  • Pedrosa-Gomes M, Lara Lanza T, Marques D, de Oliveira GM, de Castro E, Soares A (2011) Accumulation of heavy metal in Brachiaria decumbens. Sci Agrár 68:566–573. https://doi.org/10.1590/S0103-90162011000500009

    Article  Google Scholar 

  • Poschenrieder C, Cabot C, Martos S, Gallego B, Barceló J (2013) Do toxic ions induce hormesis in plants? Plant Sci 212:15–25. https://doi.org/10.1016/j.plantsci.2013.07.012

    Article  CAS  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. In: Whitacre D (ed) Reviews of Environmental Contamination and Toxicology Volume 213. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-9860-6_4

  • Pourrout B, Shahid M, Douay F, Dumat C, Pinelli E (2013) Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In: Gupta DK (ed) Heavy Metal Stress in Plants. Springer, Heidelberg, Berlin pp 121–147. https://doi.org/10.1007/978-3-642-38469-1_7

  • Prasad A, Kumar S, Khaliq A, Pandey A (2011) Heavy metals and arbuscular mycorrhizal (AM) fungi can alter the yield and chemical composition of volatile oil of sweet basil (Ocimum basilicum L.). Biol Fertil Soils 47:853–861

    Article  CAS  Google Scholar 

  • Prasad TNVKV, Sudhakar P, Sreenivasulu Y, Latha P, Munaswamy V, Reddy KR, Pradeep T (2012) Effect of nanoscale zinc oxide particles on the germination, growth and yield of peanut. J Plant Nutr 35(6):905–927. https://doi.org/10.1080/01904167.2012.663443

  • Rajakaruna N, Baker AJM (2006) Serpentine: a model hábitat for botanical research in Sri Lanka. Ceylon J Sci 32:1–19

    Google Scholar 

  • Ramírez V, Baez A, López P, Bustillos B, Villalobos MA, Carreño R, Contreras JL, Muñoz Rojas J, Fuentes LE, Martínez J, Munive JA (2019) Chromium hyper-tolerant Bacillus sp. MH778713 assists phytoremediation of heavy metals by mesquite trees (Prosopis laevigata). Front Microbiol 10:1833. https://doi.org/10.3389/fmicb.2019.01833

    Article  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(2):169–181. https://doi.org/10.1016/j.plantsci.2010.08.016

    Article  CAS  Google Scholar 

  • Rodríguez-Sauceda EN, Rojo Martínez GE, Valverde Ramírez B, Martínez Ruíz R, Cong Hermida MC, Medina Torres SM, Piña Ruíz HH (2014) Análisis técnico del árbol del Mezquite (Prosopis laevigata Humb. & Bonpl. ex Willd.) En México. Ra Ximhai 10(3):173–193

    Article  Google Scholar 

  • Rojas E, López MC, Valverde M (1999) Single cell gel electrophoresis assay: methodology and applications. J Chromatogr 722:225–254

  • Rosas-Ramírez ME (2018) Relación entre la bioacumulación de metales pesados y la concentración de clorofila en Sanvitalia procumbens. Universidad Autónoma del Estado de Morelos, Dissertation https://documentcloud.adobe.com/link/review?uri=urn:aaid:scds:US:b942e10e-6309-4556-bb54-1a8c395dd158

    Google Scholar 

  • Rout GR, Sahoo S (2015) Role of iron in plant growth and metabolism. Rev Agric Sci 3:1–24. https://doi.org/10.7831/ras.3.1

    Article  Google Scholar 

  • Ruiz HEA, Armienta HMA (2012) Acumulación de arsénico y metales pesados en maíz en suelos cercanos a jales o residuos mineros. Rev Int Contam Ambie:103–117

  • Sagardoy R, Vázquez S, Florez-Sarasa ID, Albacete A, Ribas-Carbó M, Flexas J, Abadıa J, Morales F (2010) Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytol 187:145–158. https://doi.org/10.1111/j.1469-8137.2010.03241.x

    Article  CAS  Google Scholar 

  • Salas-Luévano MA, Manzanares-Acuña E, Letechipía-de León C, Vega-Carrillo HR (2009) Tolerant and hyperaccumulators autochthonous plant species from mine tailing disposal sites. Asian J Exp Sci 23(1):27–32

    Google Scholar 

  • Salas Luévano MA, Mauricio-Castillo JA, González-Rivera ML, Vega-Carrillo HL, Salas-Muñoz S (2017) Accumulation and phytostabilization of As, Pb and Cd in plants growing inside mine tailings reforested in Zacatecas, Mexico. Environ Earth Sci 76: 806. https://doi.org/10.1007/s12665-017-7139-y

  • Salisbury FT (1968) Las plantas vasculares: forma y función. México: Herrero Hermanos Sucesores pp 598

  • Sánchez-Pinzón MS (2010) Contaminación por metales pesados en el Botadero de basuras de Moravia en Medellín: Transferencia a flora y fauna y evaluación del potencial fitorremediador de especies nativas producidas. Pontificia Universidad Javeriana, Colombia, Dissertation

    Google Scholar 

  • 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. https://doi.org/10.1007/s11356-020-07730-7

  • Secretaria de Economía (2011) Panorama Minero del estado de Morelos. Servicio Geológico Mexicano, serie panorama minero de los estados, Pachuca

  • SEMARNAT, Secretaria de Medio Ambiente y Recursos Naturales (2005) Dirección de Investigación en Residuos y Sitios Contaminados Subdirección de Investigación en Sitios Contaminados y Sustancias Tóxicas. Informe 42 anual de actividades. Evaluación de tecnologías de remediación para suelos contaminados con metales. Etapa II. [Fecha de consulta: 4 de noviembre de 2016]. http://www.inecc.gob.mx/descargas/dgcenica/metales_eii2005.pdf

  • Sharma P, Pandey S (2014) Status of phytoremediation in world scenario. Int J Environ Bioremediation & Biodegradation 2:178–191

    Google Scholar 

  • Sharma RK, Agrawal M (2005) Biological effects of heavy metals: an overview. J Environ Biol 26(2):301–313. https://doi.org/10.12691/ijebb-2-4-5

    Article  CAS  Google Scholar 

  • Shiqi L, Yang B, Kou Y, Zeng J, Wang R, Xiao Y, Li F, Lu Y, Mu Y, Zhao C (2018) Assessing the difference of tolerance and phytoremediation potential in mercury contaminated soil of a nonfood energy crop, Helianthus tuberosus L. (Jerusalem artichoke). Peer J 6:1–18. https://doi.org/10.7717/peerj.4325

    Article  CAS  Google Scholar 

  • Singh R, Tripathi RD, Dwivedi S, Kumar A, Trivedi PK, Chakrabarty D (2010) Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol 101:3025–3032. https://doi.org/10.1016/j.biortech.2009.12.031

    Article  CAS  Google Scholar 

  • Solís-Miranda BA (2016) Aislamiento de bacterias de jales mineros y análisis de su potencial para la remediación de sitios contaminados con metales pesados. Universidad Autónoma del Estado de Morelos, Dissertation https://documentcloud.adobe.com/link/track?uri=urn:aaid:scds:US:3a5f2873-da05-408d-b7d5-8b170013d30e

    Google Scholar 

  • StatSoft (2000) Correspondence analysis. Tulsa, StatSoft Inc 2000 http://www.statsoftinc.com/textbook/stcoran.html

  • Suman J, Uhlik O, Viktorova J, Macek T (2018) Phytoextraction of heavy metals: a promising tool for clean-up of polluted environment? Front Plant Sci 9:1476. https://doi.org/10.3389/fpls.2018.0147

    Article  Google Scholar 

  • Talavera O, Yta M, Moreno R, Dótor A, Flores N, Durante C (2005) Mineralogy and geochemistry of sulfide-bearing tailings from silver mines in the Taxco, Mexico area to evaluate their potential environmental impact. Geofis Int 44:49–64

    Google Scholar 

  • Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H et al (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206–221. https://doi.org/10.1002/(SICI)1098-2280(2000)35:3<206::AID-EM8>3.0.CO;2-J

    Article  CAS  Google Scholar 

  • Tovar-Sánchez E, Mussali Galante P, Martínez-Pacheco M, Ortiz Hernández ML, Sánchez-salinas E, Olvera-Verona A (2016) Relationship between genotoxic damage and arsenic blood concentrations in individuals residing in an arsenic contaminated area in Morelos, Mexico. Rev Int Contam Ambie 32:101–117

    Google Scholar 

  • Tovar-Sánchez E, Cervantes Ramírez T, Castañeda Bautista J, Gómez Arroyo S, Ortíz Hernández L, Sánchez Salinas E, Mussali Galante P (2018) Response of Zea mays to multimetal contaminated soils: a multibiomarker approach. Ecotoxicology 27:1161–1177. https://doi.org/10.1007/s10646-018-1974-9

    Article  CAS  Google Scholar 

  • Velasco J, De la Rosa D, Ramírez M, Volke T (2004) Evaluación de tecnologías de remediación para suelos contaminados con metales Etapa II. SEMARNAT-INE, México pp 46

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

    Google Scholar 

  • Wilson B, Pyatt FB (2007) Heavy metal bioaccumulation by the important food plant, Olea europaea L., in an ancient metalliferous polluted area of Cyprus. B Environ Contam Tox 78(5):390–394. https://doi.org/10.1007/s00128-007-9162-2

    Article  CAS  Google Scholar 

  • Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179. https://doi.org/10.1016/j.sajb.2009.10.007

    Article  CAS  Google Scholar 

  • Yang Z, Chen J, Dou R, Gao X, Mao C, Wang L (2015) Assessment of the phytotoxicity of metal oxide nanoparticles on two crop plants, maize (Zea mays L.) and rice (Oryza sativa L.). Int J Env Res Pub He 12:15100–15109

    Article  CAS  Google Scholar 

  • Yllanes P, Vélez A, Lozano S (2014) Efectos fitotóxicos del plomo en maíz híbrido Dekalb (Zea mays L.) en suelo arenoso y limoso. Biologist 12:337–248

    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 

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Acknowledgments

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: 429356). Also, we thank Rosalind Pearson Hedge for her comments and English edition that improved our manuscript.

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Authors and Affiliations

  1. Doctorado en Ciencias Naturales, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, Mexico

    Dalia A. Muro-González

  2. Laboratorio de Investigaciones Ambientales, Centro de Investigación en Biotecnología, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, Mexico

    Patricia Mussali-Galante & Karen Flores-Trujillo

  3. Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, Mexico

    Leticia Valencia-Cuevas & Efraín Tovar-Sánchez

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  1. Dalia A. Muro-González
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  2. Patricia Mussali-Galante
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  3. Leticia Valencia-Cuevas
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  4. Karen Flores-Trujillo
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  5. Efraín Tovar-Sánchez
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Correspondence to Efraín Tovar-Sánchez.

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

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