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Bioaccumulation of heavy metals and As in maize (Zea mays L) grown close to mine tailings strongly impacts plant development

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Abstract

Potentially toxic metals and metalloids present in mining residues can affect ecosystems, particularly plant growth and development. In this study we evaluated heavy metal (Fe, Zn, Cu, Cd, Pb) and As contents in maize (Zea mays L) plants grown in soils collected near (40 m), at intermediate (400 m) and remote (3000 m) distances from mine tailings near Taxco City, Mexico. Soils sampled near and at intermediate sites from the tailings contained high levels of heavy metals which were 3- to 55-fold higher compared to the control samples. Heavy metal and As content in plants reflected the soil contamination being the greatest for most studied elements in root samples followed by stems, leaves, and kernels. Though plants were capable of completing their life cycle and producing the seeds, high bioaccumulation levels had a strong impact negatively on plant development. Abnormalities in the organs like malformations in reproductive structures (tassel and ear), reduction in the phytomer number and the plant height were present. Microscopic studies and morphometric analyses suggest that strongly affected plant growth result from negative and synergistic action of heavy metals and As in soils on cell growth and cell production. This study showed that maize grown near mine tailings accumulated high levels of heavy metals and As which decrease significantly plant yield and could be dangerous if it is consumed by animals and humans.

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References

  • Ager FJ, Ynsa MD, Domınguez-Solıs JR, Gotor C, Respaldiza MA, Romero LC (2002) Cadmium localization and quantification in the plant Arabidopsis thaliana using micro-PIXE. Nucl Instrum Methods Phys Res B 189(1–4):494–498. https://doi.org/10.1016/S0168-583X(01)01130-2

    Article  CAS  Google Scholar 

  • Aladesanmi OT, Oroboade JG, Osisiogu CP, Osewole AO (2019) Bioaccumulation factor of selected heavy metals in Zea mays. J Health Pollut 9:1–19

    Article  Google Scholar 

  • Alamgir A, Khan MA, Shaukat SS, Shahab S, Mahmood K (2016) Estimation of environmental pollutants in vegetables. Int J Veg Sci 22(2):161–169. https://doi.org/10.1080/19315260.2014.984263

    Article  Google Scholar 

  • Alharbi NS, Hu B, Hayat T, Rabah SO, Alsaedi A, Zhuang L, Wang X (2020) Efficient elimination of environmental pollutants through sorption-reduction and photocatalytic degradation using nanomaterials. Front Chem Sci Eng 14:1124–1135. https://doi.org/10.1007/s11705-020-1923-z

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals concepts and applications. Chemosphere 91(7):869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075

    Article  CAS  Google Scholar 

  • Ali NA, Bernal MP, Ater M (2002) Tolerance and bioaccumulation of copper in Phragmites australis and Zea mays. Plant Soil 239:103–111. https://doi.org/10.1023/A:1014995321560

    Article  CAS  Google Scholar 

  • Alloway BJ (1995) Heavy metals in soils. Springer. Netherlands. https://doi.org/10.1007/978-94-007-4470-7

  • Alvarez E, Marcos MF, Vaamonde C, Fernández-Sanjurjo MJ (2003) Heavy metals in the dump of an abandoned mine in Galicia (NW Spain) and in the spontaneously occurring vegetation. Sci Total Environ 313(1-3):185–197. https://doi.org/10.1016/S0048-9697(03)00261-4

    Article  CAS  Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Ashraf U, Khan I, Wang L (2017) Alteration in growth, leaf gas exchange, and photosynthetic pigments of maize plants under combined cadmium and arsenic stress. Water Air Soil Pollut 228(1):13. https://doi.org/10.1007/s11270-016-3187-2

    Article  CAS  Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Ullah E, Wang L, Khan I, Samad RA, Tung SA, Anam M, Shahzad B (2016) Morphophysiological growth and yield responses of two contrasting maize cultivars to cadmium exposure. CLEAN–Soil, Air, Water 44:29–36

  • Armienta MA, Talavera O, Morton O, Barrera M (2003) Geochemistry of metals from mine tailings in Taxco, Mexico. Bull Environ Contam Toxicol 71:0387–0393. 10.loo7/soo128-oo3-0176-0

    Article  CAS  Google Scholar 

  • Armienta Hernández MA, Talavera O, Barrera M, Morton O, Villaseñor G, Cruz O, Ceniceros N, Aguayo A (2001) Movilidad de metales pesados a partir de jales en Taxco Gro. Actas INAGED

  • Armienta Hernández MA, Talavera O, Ceniceros N, Aguayo A, Cruz O (2000) Caracterización geoquímica de cuerpos de agua en la zona Taxco – Taxco El Viejo Gro. Actas INAGEQ

  • Bai YC, Zuo WG, Zhao HT, Mei LJ, Gu CH, Guan YX, Wang XK, Gu MJ, Zang KY, Shan YH, Feng K (2017) Distribution of heavy metals in maize and mudflat saline soil amended by sewage sludge. J Soils Sediments 17(6):1565–1578. https://doi.org/10.1007/s11368-016-1630-z

    Article  CAS  Google Scholar 

  • Barać N, Škrivanj S, Mutić J, Manojlović D, Bukumirić Z, Živojinović D, Petrović R, Ćorac A (2016) Heavy metals fractionation in agricultural soils of Pb/Zn mining region and their transfer to selected vegetables. Water Air Soil Pollut 227(12):481. https://doi.org/10.1007/s11270-016-3177-4

    Article  CAS  Google Scholar 

  • Barceló J, Vázquez MD, Poschenrieder C (1988) Cadmium-induced structural and ultrastructural changes in the vascular system of bush bean stems. Bot Acta 101:254–261. https://doi.org/10.1111/j.1438-8677.1988.tb00041.x

    Article  Google Scholar 

  • Beiyuan J, Awad YM, Beckers F, Wang J, Tsang DC, Ok YS, Rinklebe J (2020) (Im) mobilization and speciation of lead under dynamic redox conditions in a contaminated soil amended with pine sawdust biochar. Environment international 135:105376

  • Bi X, Feng X, Yang Y, Li X, Shin GP, Li F, Qiu G, Li G, Liu T, Fu Z (2009) Allocation and source attribution of lead and cadmium in maize (Zea mays L.) impacted by smelting emissions. Environ Pollut 157:834–839

    Article  CAS  Google Scholar 

  • Bostick BC, Sun J, Landis JD, Clausen JL (2018) Tungsten speciation and solubility in munitions-impacted soils. Environ Sci Technol 52(3):1045–1053. https://doi.org/10.1021/acs.est.7b05406

    Article  CAS  Google Scholar 

  • Boulet MP, Larocque ACL (1998) A comparative mineralogical and geochemical study of sulfide mine tailings at two sites in New Mexico, USA. Environ Geol 33:130–142. https://doi.org/10.1007/s002540050233

    Article  CAS  Google Scholar 

  • Bozzola JJ, Russell LD (1999) Electron microscopy: principles and techniques for biologists. Jones & Bartlett Learning

  • Bradshaw AD, Humphreys MO, Johnson MS (1978) The value of heavy metal tolerance in the revegetation of metalliferous mine wastes. Environmental management of mineral wastes. Sijthoff & Noordhoff, Alphen aan den Rijn, Netherlands, p. 311–314

  • Castellanos JZ, Uvalle-Bueno JX, Aguilar-Santelises A (2000) Manual de interpretación de análisis de suelos y aguas. Instituto de Capacitación para la Productividad Agrícola

  • Chardonnens AN, Ten Bookum WM, Kuijper LDJ, Verkleij JAC, Ernst WHO (1998) Distribution of cadmium in leaves of cadmium tolerant and sensitive ecotypes of Silene vulgaris. Physiol Plant 104:75–80. https://doi.org/10.1034/j.1399-3054.1998.1040110.x

    Article  CAS  Google Scholar 

  • Chen R, Chen H, Song L, Yao Z, Meng F, Teng Y (2019) Characterization and source apportionment of heavy metals in the sediments of Lake Tai (China) and its surrounding soils. Sci Total Environ 694:133819. https://doi.org/10.1016/j.scitotenv.2019.133819

    Article  CAS  Google Scholar 

  • Choi YE, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H (2001) Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213(1):45–50. https://doi.org/10.1007/s004250000487

    Article  CAS  Google Scholar 

  • Clemente R, Almela C, Bernal MP (2006) A remediation strategy based on active phytoremediation followed by natural attenuation in a soil contaminated by pyrite waste. Environ Pollut 143:397–406. https://doi.org/10.1016/j.envpol.2005.12.011

    Article  CAS  Google Scholar 

  • CONABIO (Comisión Nacional para el Conocimiento y uso de la Biodiversidad), 2006. Natural capital and social welfare. CONABIO, Mexico

  • COREMI, 2013. Monografía Geológico Minera del Estado de Guerrero. Servicio Geológico Mexicano

  • Dahmani-Muller H, van Oort F, Gélie B, Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ Pollut 109:231–238. https://doi.org/10.1016/S0269-7491(99)00262-6

    Article  CAS  Google Scholar 

  • De-Jesús-García R, Rosas U, Dubrovsky JG (2020) The barrier function of plant roots: biological bases for selective uptake and avoidance of soil compounds. Funct Plant Biol 47(5):383–397. https://doi.org/10.1071/FP19144

    Article  Google Scholar 

  • Drličková G, Vaculík M, Matejkovič P, Lux A (2013) Bioavailability and toxicity of arsenic in maize (Zea mays L.) grown in contaminated soils. Bull. Environ. Contam. Toxicol. 91:235–239

  • Du L, Xia X, Lan X, Liu M, Zhao L, Zhang P, Wu Y (2017) Influence of arsenic stress on physiological, biochemical, and morphological characteristics in seedlings of two cultivars of maize (Zea mays L.). Water Air Soil Pollut 228(2):55. https://doi.org/10.1007/s11270-016-3231-2

    Article  CAS  Google Scholar 

  • Dudka S, Adriano DC (1997) Environmental impacts of metal ore mining and processing: a review. J Env Qual 26:590–602. https://doi.org/10.2134/jeq1997.00472425002600030003x

    Article  CAS  Google Scholar 

  • FAO (1977) Guía para la descripción de perfiles de suelo. Food Agric. Organ. U.N. http://www.fao.org/publications/card/es/c/0f070cdd-1b6d-53fa-add1-5c972fb299d2. Accessed 19 April 2015

  • Figlioli F, Sorrentino MC, Memoli V, Arena C, Maisto G, Giordano S, Capozzi F, Spagnuolo V (2019) Overall plant responses to Cd and Pb metal stress in maize: Growth pattern, ultrastructure, and photosynthetic activity. Environ. Sci. Pollut. Res. 26:1781–1790

  • Gómez-Bernal JM, Morton-Bermea O, Ruiz-Huerta EA, Armienta-Hernández MA, Dávila González O (2014) Microscopic evidences of heavy metals distribution and anatomic alterations in breaching-leaves of Cupressus lindleyi growing around mining wastes. Microsc Res Tech 77:714–726. https://doi.org/10.1002/jemt.22392

    Article  Google Scholar 

  • Gopal R, Rizvi AH (2008) Excess lead alters growth, metabolism and translocation of certain nutrients in radish. Chemosphere 70:1539–1544

  • Gupta VK, Yola ML, Atar N, Ustundağ Z, Solak AO (2013) A novel sensitive Cu (II) and Cd (II) nanosensor platform: graphene oxide terminated p-aminophenyl modified glassy carbon surface. Electrochim Acta 112:541–548

    Article  CAS  Google Scholar 

  • Hochholdinger F, Park WJ, Sauer M, Woll K (2004) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci 9(1):42–48. https://doi.org/10.1016/j.tplants.2003.11.003

    Article  CAS  Google Scholar 

  • Hu B, Ai Y, Jin J, Hayat T, Alsaedi A, Zhuang L, Wang X (2020) Efficient elimination of organic and inorganic pollutants by biochar and biochar-based materials. Biochar 3:255–281. https://doi.org/10.1007/s42773-020-00044-4

  • Hu YN, Cheng HF (2013) Application of stochastic models in identification and apportionment of heavy metal pollution sources in the surface soils of a large-scale region. Environ Sci Technol 47:3752–3760

  • Hund A, Ruta N, Liedgens M (2009) Rooting depth and water use efficiency of tropical maize inbred lines, differing in drought tolerance. Plant and Soil 318:311–325. https://doi.org/10.1007/s11104-008-9843-6

    Article  CAS  Google Scholar 

  • IHOBE SP de GA (2003) Manual práctico para la investigación de la contaminación del suelo. Propues. Plan Dir. Para Protección Suelo Dep. Urban. Vivienda Medio Ambiente Gob. Vasco 1

  • IMMSA (1973) Yacimientos minerales metálicos del Distrito Minero de Taxco (Reporte Interno, Taxco, Guerrero-México). Industrial Minera México S.A

  • INEGI (1999) Síntesis geográfica del Estado de Guerrero. Instituto Nacional de Estadística, Geografía e Informática, Aguascalientes, México

  • INEGI (2005) Prontuario de información geográfica municipal de los Estados Unidos Mexicanos. Taxco de Alarcón, Guerrero. Instituto Nacional de Estadística y Geografía de México

  • Kabata-Pendias A (2000) Trace Elements in Soils and Plants, Third Edition. CRC Press

  • Lagriffoul A, Mocquot B, Mench M, Vangronsveld J (1998) Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant Soil 200:241–250. https://doi.org/10.1023/A:1004346905592

    Article  CAS  Google Scholar 

  • Lavid N, Barkay Z, Tel-Or E (2001a) Accumulation of heavy metals in epidermal glands of the waterlily (Nymphaeaceae). Planta 212:313–322. https://doi.org/10.1007/s004250000399

    Article  CAS  Google Scholar 

  • Lavid N, Schwartz A, Lewinsohn E, Tel-Or E (2001b) Phenols and phenol oxidases are involved in cadmium accumulation in the water plants Nymphoides peltata (Menyanthaceae) and Nymphaeae (Nymphaeaceae). Planta 214:189–195. https://doi.org/10.1007/s004250100610

    Article  CAS  Google Scholar 

  • Li S, Zhao B, Jin M, Hu L, Zhong H, He Z (2020) A comprehensive survey on the horizontal and vertical distribution of heavy metals and microorganisms in soils of a Pb/Zn smelter. J. Hazard. Mater. 400:123255

  • Liang S, Jin Y, Liu W, Li X, Shen S, Ding L (2017) Feasibility of Pb phytoextraction using nano-materials assisted ryegrass: results of a one-year field-scale experiment. J. Environ. Manag 190:170–175

    Article  CAS  Google Scholar 

  • Lin W, Xiao T, Wu Y, Ao Z, Ning Z (2012) Hyperaccumulation of zinc by Corydalis davidii in Zn-polluted soils. Chemosphere 86:837–842. https://doi.org/10.1016/j.chemosphere.2011.10.060

    Article  CAS  Google Scholar 

  • Ling T, Gao Q, Du H, Zhao Q, Ren J (2017) Growing, physiological responses and Cd uptake of Corn (Zea mays L.) under different Cd supply. Chem Speciat Bioavailab, 29(1):216–221

    Article  CAS  Google Scholar 

  • Liu WT, Zhou QX, Sun YB, Liu R (2009) Variety difference of lead accumulation and translocation in Chinese cabbage (Brassica peckinensis L.). J Environ Sci (China) 29(1):63–67

    Google Scholar 

  • Liu J, Li N, Zhang W, Wei X, Tsang DC, Sun Y, Feng Y (2019) Thallium contamination in farmlands and common vegetables in a pyrite mining city and potential health risks. Environ. Pollut. 248:906–915

  • Liu J, Wei X, Zhou Y, Tsang DC, Yin M, Lippold H, Yuana W, Wang J, Feng Y, Chen D (2020a) Thallium contamination, health risk assessment and source apportionment in common vegetables Sci Total Environ 703:135547. https://doi.org/10.1016/j.scitotenv.2019.135547

  • Liu WR, Zeng D, She L, Su WX, He DC, Wu GY, Ying GG (2020b) Comparisons of pollution characteristics, emission situations, and mass loads for heavy metals in the manures of different livestock and poultry in China. Sci. Total Environ. 734:139023

  • Lv J (2019) Multivariate receptor models and robust geostatistics to estimate source apportionment of heavy metals in soils. Environ Pollut 244:72–83. https://doi.org/10.1016/j.envpol.2018.09.147

    Article  CAS  Google Scholar 

  • Maksimović I, Kastori R, Krstić L, Luković J (2007) Steady presence of cadmium and nickel affects root anatomy, accumulation and distribution of essential ions in maize seedlings. Biol Plant 51:589–592. https://doi.org/10.1007/s10535-007-0129-2

    Article  Google Scholar 

  • Mantovi P, Baldoni G, Toderi G (2005) Reuse of liquid, dewatered, and composted sewage sludge on agricultural land: effects of long-term application on soil and crop. Water Res 39:289–296

    Article  CAS  Google Scholar 

  • Máthé-Gáspár G, Anton A (2005) Phytoremediation study: factors influencing heavy metal uptake of plants. Acta Biologica Szegediensis 49(1–2):69–70

    Google Scholar 

  • Mertens J, Vervaeke P, Schrijver AD, Luyssaert S (2004) Metal uptake by young trees from dredged brackish sediment: limitations and possibilities for phytoextraction and phytostabilisation. Sci Total Environ 326:209–215. https://doi.org/10.1016/j.scitotenv.2003.12.010

    Article  CAS  Google Scholar 

  • Moldovan L, Moldovan NI (2004) Oxygen free radicals and redox biology of organelles. Histochem Cell Biol 122:395–412

    Article  CAS  Google Scholar 

  • Müller G (1969) Index of geoaccumulation in sediments of the Rhine River. Geo Journal 2:108–118

    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. Ambient 29:117–140

  • 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 

  • Nan Z, Li J, Zhang J, Cheng G (2002) Cadmium and zinc interactions and their transfer in soil-crop system under actual field conditions. Sci Total Environ 285:187–195

    Article  CAS  Google Scholar 

  • Navarro-Pedreño J, Almendro-Candel MB, Jordán-Vidal MM, Mataix-Solera J, García-Sánchez E (2003) Mobility of cadmium, chromium, and nickel through the profile of a calcisol treated with sewage sludge in the southeast of Spain. Environ Geol 44(5):545–553. https://doi.org/10.1007/s00254-003-0790-5

    Article  CAS  Google Scholar 

  • NOM-021-SEMARNAT-2000 (2000) Norma Oficial Mexicana que establece las especificaciones de fertilidad, salinidad y clasificación de suelos, estudio, muestreo y análisis

  • Norland MR, Veith DL (1995) Revegetation of coarse taconite iron ore tailing using municipal solid waste compost. J Hazard Matter 41:123–134

    Article  CAS  Google Scholar 

  • Norma Oficial Mexicana NOM-147-SEMARNAT/SSA1-2004 (2007) Que establece criterios para determinar las concentraciones de remediación de suelos contaminados por arsénico, berilio, cadmio, cromo hexavalente, mercurio, níquel, plomo, selenio, talio y vanadio. México

  • Oladipo OG, Olayinka A, Awotoye OO (2016) Maize (Zea mays L.) performance in organically amended mine site soils. J Environ Manage 181:435–442. https://doi.org/10.1016/j.jenvman.2016.07.009

    Article  CAS  Google Scholar 

  • Pál M, Horváth E, Janda T, Páldi E, Szalai G (2006) Physiological changes and defense mechanisms induced by cadmium stress in maize. J Plant Nutr Soil Sci 169:239–246. https://doi.org/10.1002/jpln.200520573

    Article  CAS  Google Scholar 

  • Prommer H, Sun J, Helm L, Rathi B, Siade AJ, Morris R (2018) Deoxygenation prevents arsenic mobilization during deep well injection into sulfide-bearing aquifers. Environ Sci Technol 52(23):13801–13810. https://doi.org/10.1021/acs.est.8b05015

    Article  CAS  Google Scholar 

  • Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29:529–540. https://doi.org/10.1016/S0160-4120(02)00152-6

    Article  CAS  Google Scholar 

  • Romero FM, Armienta MA, González-Hernández G (2007) Solid-phase control on the mobility of potentially toxic elements in an abandoned lead/zinc mine tailings impoundment, Taxco, Mexico. Appl Geochem 22:109–127. https://doi.org/10.1016/j.apgeochem.2006.07.017

    Article  CAS  Google Scholar 

  • Romero FM, Armienta MA, Gutiérrez ME, Villaseñor G (2008) Factores geológicos y climáticos que determinan la peligrosidad y el impacto ambiental de jales mineros. Rev Int Contam Ambient 24:43–54

    CAS  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 Ambient 28:103–117

    Google Scholar 

  • Ruíz-Huerta EA, De la Garza Varela A, Gómez-Bernal JM, Castillo F, Avalos-Borja M, SenGupta B, Martínez-Villegas N (2017) Arsenic contamination in irrigation water, agricultural soil and maize crop from an abandoned smelter site in Matehuala, Mexico. J. Hazard. Mater. 339:330–339

  • Salcedo ERS, Morales MM, Martínez JME, Mendoza OT (2021) Heavy metal contamination and ecological risk assessment in fluvial sediment of San Juan–Taxco river system in mining region of Taxco Guerrero, Mexico. https://doi.org/10.21203/rs.3.rs-785264/v1

  • Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109(4):1427–1433. https://doi.org/10.1104/pp.109.4.1427

  • Seregin IV, Shpigun LK, Ivanov VB (2004) Distribution and toxic effects of cadmium and lead on maize roots. Russ J Plant Physiol 51:525–533. https://doi.org/10.1023/B:RUPP.0000035747.42399.84

    Article  CAS  Google Scholar 

  • Seregin IV, Kozhevnikova AD (2005) Distribution of cadmium, lead, nickel, and strontium in imbibing maize caryopses. Russ J Plant Physiol 52:565–569. https://doi.org/10.1007/s11183-005-0084-8

    Article  CAS  Google Scholar 

  • Sharma DC, Sharma CP, Tripathi RD (2003) Phytotoxic lesions of chromium in maize. Chemosphere 51(1):63–68

  • Shen H, Christie P, Li X (2006) Uptake of zinc, cadmium and phosphorus by arbuscular mycorrhizal maize (Zea mays L.) from a low available phosphorus calcareous soil spiked with zinc and cadmium. Environ Geochem Health 28:111–119. https://doi.org/10.1007/s10653-005-9020-2

    Article  CAS  Google Scholar 

  • Shi Y, Huang Z, Liu X, Imran S, Peng L, Dai R, Deng Y (2016) Environmental materials for remediation of soils contaminated with lead and cadmium using maize (Zea mays L.) growth as a bioindicator. Environ Sci Pollut Res 23(7):6168–6178. https://doi.org/10.1007/s11356-015-5778-7

    Article  CAS  Google Scholar 

  • Shinmachi F, Kumanda Y, Noguchi A, Hasegawa I (2003) Stem-specific cadmium accumulation in cadmium-tolerant Polygonum thunbergii. Soil Sci Plant Nutr 49:363–368. https://doi.org/10.1080/00380768.2003.10410021

    Article  CAS  Google Scholar 

  • Shubenko EM (1996) Morphological investigations of maize (Zea mays L.) root systems. Acta Phytogeogr. Suec. 81, Uppsala. p 116–118. ISBN 91-7210-081-8

  • Souza JF, Rauser WE (2003) Maize and radish sequester excess cadmium and zinc in different ways. Plant Sci 165:1009–1022. https://doi.org/10.1016/S0168-9452(03)00289-9

    Article  CAS  Google Scholar 

  • Souza JF, Dolder H, Cortelazzo AL (2005) Effect of excess cadmium and zinc ions on roots and shoots of maize seedlings. J Plant Nutr 28:1923–1931. https://doi.org/10.1080/01904160500310435

    Article  CAS  Google Scholar 

  • Talavera-Mendoza O, Yta M, Moreno-Tovar R, Dótor-Almazán A, Flores-Mundo N, Duarte-Gutiérrez 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 44:46–64

    Google Scholar 

  • Tovar-Sánchez E, Cervantes LT, Martínez C, Rojas E, Valverde M, Ortiz-Hernández ML, Mussali-Galante P (2012) Comparison of two wild rodent species as sentinels of environmental contamination by mine tailings. Environ Sci Pollut Res 19(5):1677–1686. https://doi.org/10.1007/s11356-011-0680-4

    Article  CAS  Google Scholar 

  • Tovar-Sánchez E, Cervantes-Ramírez T, Castañeda-Bautista J, Gómez-Arroyo S, Ortiz-Hernández L, Sánchez-Salinas E, Mussali-Galante P (2018) Response of Zea mays to multimetal contaminated soils: a multibiomarker approach. Ecotoxicol 27(8):1161–1177. https://doi.org/10.1007/s10646-018-1974-9

    Article  CAS  Google Scholar 

  • Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2011) Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant Soil 341:75–87. https://doi.org/10.1007/s11104-010-0623-8

    Article  CAS  Google Scholar 

  • Unterbrunner R, Puschenreiter M, Sommer P, Wieshammer G, Tlustoš P, Zupan M, Wenzel WW (2007) Heavy metal accumulation in trees growing on contaminated sites in Central Europe. Environ Pollut 148:107–114. https://doi.org/10.1016/j.envpol.2006.10.035

    Article  CAS  Google Scholar 

  • USDOE (US Department of Energy) (2011) The Risk Assessment Information System (RAIS). US Department of Energy’s Oak Ridge Operations Office (ORO), Oak Ridge, TN, USA

  • USEPA (1992) Framework for ecological risk assessment. In Risk Assessment Forum. US Environmental Protection Agency, Washington, DC

  • USEPA (US Environmental Protection Agency) (1989) Risk Assessment Guidance for Superfund. Volume I: Human Health Evaluation Manual (Part A). EPA/540/1-89/002. Office of Emergency and Remedial Response, Washington, DC, USA

  • USEPA. (1997) Exposure Factors Handbook. EPA/600/P-95/002Fa. Office of Research and Development, Washington, DC, USA

  • USEPA. (2001) Risk Assessment Guidance for Superfund: Volume III-part A, Process for Conducting Probabilistic Risk Assessment, 20460. EPA 540-R-02-002. Office of Emergency and Remedial Response, Washington, DC, USA

  • Vázquez S, Agha R, Granado A, Sarro MJ, Esteban E, Peñalosa JM, Carpena RO (2006) Use of white lupin plant for phytostabilization of Cd and As polluted acid soil. Water Air Soil Pollut 177:349–365. https://doi.org/10.1007/s11270-006-9178-y

    Article  CAS  Google Scholar 

  • Vielle-Calzada JP, de la Vega OM, Hernández-Guzmán G, Ibarra-Laclette E, Alvarez-Mejía C, Vega-Arreguín JC, Jiménez-Moraila B, Fernández-Cortés A, Corona-Armenta G, Herrera-Estrella L, Herrera-Estrella A (2009) The Palomero genome suggests metal effects on domestication. Science 326(5956):1078–1078. https://doi.org/10.1126/science.1178437

    Article  CAS  Google Scholar 

  • Walder IF, Chavez WX (1995) Mineralogical and geochemical behavior of mill tailing material produced from lead-zinc skarn mineralization, Hanover, Grant County, New Mexico, USA. Environ Geol 26:1–18. https://doi.org/10.1007/BF00776027

    Article  CAS  Google Scholar 

  • Wang J, Liu J, Li H, Chen Y, Xiao T, Song G, Chen D, Wang C (2017) Uranium and thorium leachability in contaminated stream sediments from a uranium mine site. J Geochem Exp 176:85–90. https://doi.org/10.1016/j.gexplo.2016.01.008

    Article  CAS  Google Scholar 

  • Wang J, Zhou Y, Dong X, Yin M, Tsang D, Sun J, Liu J, Song G, Liu Y (2020b) Temporal sedimentary record of thallium pollution in an urban lake: an emerging thallium pollution source from copper metallurgy. Chemosphere 242:125172. https://doi.org/10.1016/j.chemosphere.2019.125172

    Article  CAS  Google Scholar 

  • Wang J, Jiang Y, Sun J, She J, Yin M, Fang F, Xiao T, Song G, Liu J (2020a) Geochemical transfer of cadmium in river sediments near a lead-zinc smelter. Ecotoxicol Environ Saf 196:110529. https://doi.org/10.1016/j.ecoenv.2020.110529

    Article  CAS  Google Scholar 

  • Wang J, She J, Zhou Y, Tsang DCW, Beiyuan J, Xiao T, Dong X, Chen Y, Liu J, Yin M, Wang L (2020c) Microbial insights into the biogeochemical features of thallium occurrence: a case study from polluted river sediments. Sci Total Environ 739:139957. https://doi.org/10.1016/j.scitotenv.2020.139957

    Article  CAS  Google Scholar 

  • Wang X, Yu S, Jin J, Wang H, Alharbi NS, Alsaedi A, Hayat T, Wang X (2016) Application of graphene oxides and graphene oxide-based nanomaterials in radionuclide removal from aqueous solutions. Sci Bull 061:1583–1593. https://doi.org/10.1007/s11434-016-1168-x

    Article  CAS  Google Scholar 

  • Wei X, Zhou Y, Jiang Y, Tsang DC, Zhang C, Liu J, Zhou Y, Yin M, Wang J, Shen N, Xiao T, Xiao T (2020) Health risks of metal (loid)s in maize (Zea mays L.) in an artisanal zinc smelting zone and source fingerprinting by lead isotope. Sci Total Environ 742:140321. https://doi.org/10.1016/j.scitotenv.2020.140321

    Article  CAS  Google Scholar 

  • Wenger K, Gupta SK, Furrer G, Schulin R (2002) Zinc Extraction potential of two common crop plants, Nicotiana tabacum and Zea mays. Plant Soil 242:217–225. https://doi.org/10.1023/A:1016253821174

    Article  CAS  Google Scholar 

  • Weryszko-Chmielewska E, Chwil M (2005) Lead-induced histological and ultrastructural changes in the leaves of soybean (Glycine max (L.) Merr.). Soil Sci Plant Nutr 51:203–212. https://doi.org/10.1111/j.1747-0765.2005.tb00024.x

    Article  CAS  Google Scholar 

  • Wójcik M, Tukiendorf A (2005) Cadmium uptake, localization and detoxification in Zea mays. Biol Plant 49:237–245. https://doi.org/10.1007/s10535-005-7245-7

    Article  Google Scholar 

  • Wójicik M, Tukendorf A (1999) Cd-tolerance of maize, rye and wheat seedlings. Acta Physiol Plant 21:99–107. https://doi.org/10.1007/s11738-999-0063-3

    Article  Google Scholar 

  • Wong JWC, Ip CM, Wong MH (1998) Acid-forming capacity of lead–zinc mine tailings and its implications for mine rehabilitation. Environ Geochem Health 20:149–155. https://doi.org/10.1023/A:1006589124204

    Article  CAS  Google Scholar 

  • Wu Q, Pagès L, Wu J (2016) Relationships between root diameter, root length and root branching along lateral roots in adult, field-grown maize. Ann Bot 117(3):379–390. https://doi.org/10.1093/aob/mcv185

    Article  Google Scholar 

  • Wuana RA, Okieimen FE (2010) Phytoremediation potential of maize (Zea mays L.). A review. Afri J General Agric 6:275–287

    Google Scholar 

  • Xu Q, Shi G (2000) The toxic effects of single Cd and interaction of Cd with Zn on some physiological index of [Oenanthe javanica (Blume) DC]. J Nanjing Norm Univ Nat Sci 23(4):97–100

    CAS  Google Scholar 

  • Yin K, Chan WP, Dou X, Lisak G, Chang VWC (2019) Vertical distribution of heavy metals in seawater column during IBA construction in land reclamation–Re-exploration of a large-scale field trial experiment. Sci. Total Environ. 654:356–364

  • Zhao FJ, Lombi E, Breedon T, SPMC (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514. https://doi.org/10.1046/j.1365-3040.2000.00569.x

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Nora Ceniceros, Alejandra Aguayo, and Olivia Cruz for their skillful collaboration in analytical determinations and Guillermina González Mancera for help with scanning electron microscopy.

Funding

The authors appreciate the doctoral fellowship of Consejo Nacional de Ciencia y Tecnología (CONACyT) and the Posgrado en Ciencias de la Tierra, Universidad Nacional Autónoma de México (UNAM) for EAR-H. The work in JGD laboratory is supported by CONACyT (grant A1-S-9236) and Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica-UNAM (grants IN200818 and IN204221).

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Conceptualization: EAR-H, JMG-B, and MAA-H; formal data analysis: EAR-H, MAA-H, JMG-B, and JGD; project administration: EAR-H and MAA-H; writing—original draft: EAR-H, JMG-B, and JGD; writing—review and editing: EAR-H, JMG-B, MAA-H, and JGD.

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Correspondence to Esther Aurora Ruiz-Huerta.

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Ruiz-Huerta, E.A., Armienta-Hernández, M.A., Dubrovsky, J.G. et al. Bioaccumulation of heavy metals and As in maize (Zea mays L) grown close to mine tailings strongly impacts plant development. Ecotoxicology 31, 447–467 (2022). https://doi.org/10.1007/s10646-022-02522-w

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