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Foliar application of lead and arsenic solutions to Spinacia oleracea: biophysiochemical analysis and risk assessment

  • Environmental Toxicology and Risks Associated with Human Health
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Abstract

Atmospheric contamination by heavy metal(loid)s is a widespread global issue. Recent studies have shown foliar pathway of heavy metal(loid) uptake by plants, thus menacing plant productivity and threatening health risks. In contrast to root uptake of heavy metal(loid)s, there is scarce data available on heavy metal(loid) foliar uptake, accumulation in different plant parts, changes in growth and other biophysiochemical processes/reactions, detoxification mechanisms and associated health risks due to the consumption of contaminated vegetables. This study evaluated the effect of foliar application of two potentially toxic metal(loid)s (arsenic (As) and lead (Pb)) on their uptake by Spinacia oleracea, plant growth, pigment contents, physiological changes, and activation of antioxidative enzymes. Results revealed that S. oleracea seedlings can accumulate both the metal(loid)s in their leaves via foliar pathway. Arsenic was transferred from the leaves towards the roots, while Pb was mainly sequestered in S. oleracea leaves. Both the metal(loid)s significantly decreased plant growth and pigment contents, As being more toxic than Pb. Foliar application of As and Pb did not cause lipid peroxidation and overproduction of reactive oxygen species (ROS). However, both the metal(loid)s enhanced the activities of antioxidative enzymes. We also calculated possible health risks (both non-carcinogenic and carcinogenic) due to As and Pb accumulation in the edible parts for both the adults and children. It was observed that As can induce non-carcinogenic effects (HQ > 1) in children only, while both As and Pb can cause carcinogenic hazards in both adults and children under their all applied foliar levels. Therefore, it is proposed that As and Pb contents in the atmosphere must be monitored continuously for their possible foliar uptake and accumulation in edible plant parts to avoid cancer risks. Moreover, multivariate analysis traced weak-strong correlations between metal(loid) treatments and plant response variables.

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References

  • Abbas G, Murtaza B, Bibi I, Shahid M, Niazi N, Khan M, Amjad M, Hussain M, Natasha (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59

    Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    CAS  Google Scholar 

  • Antoniadis V, Shaheen SM, Levizou E, Shahid M, Niazi NK, Vithanage M, Ok YS, Bolan N, Rinklebe J (2019) A critical prospective analysis of the potential toxicity of trace element regulation limits in soils worldwide: are they protective concerning health risk assessment?-a review. Environ Int 127:819–847

    CAS  Google Scholar 

  • ATSDR (2007) Toxicological profile for arsenic. Agency for Toxic Substances and Disease Registry

  • Bakhat HF, Zia Z, Fahad S, Abbas S, Hammad HM, Shahzad AN, Abbas F, Alharby H, Shahid M (2017) Arsenic uptake, accumulation and toxicity in rice plants: possible remedies for its detoxification: a review. Environ Sci Pollut Res 24:9142–9158

    CAS  Google Scholar 

  • Bondada BR, Tu S, Ma LQ (2004) Absorption of foliar-applied arsenic by the arsenic hyperaccumulating fern (Pteris vittata L.). Sci Total Environ 332:61–70

    CAS  Google Scholar 

  • Chowdhury NR, Das R, Joardar M, Ghosh S, Bhowmick S, Roychowdhury T (2018) Arsenic accumulation in paddy plants at different phases of pre-monsoon cultivation. Chemosphere 210:987–997

    CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    CAS  Google Scholar 

  • Dumat C, Xiong T, Shahid M (2016) Agriculture urbaine durable: Opportunité pour la transition écologique. OmniScriptum, Germany, Germany, pp 1–80

    Google Scholar 

  • El Hayek E, El Samrani A, Lartiges B, Kazpard V, Aigouy T (2017) Lead bioaccumulation in Opuntia ficus-indica following foliar or root exposure to lead-bearing apatite. Environ Pollut 220:779–787

    Google Scholar 

  • Gajbhiye T, Pandey SK, Kim K-H, Szulejko JE, Prasad S (2016) Airborne foliar transfer of PM bound heavy metals in Cassia siamea: a less common route of heavy metal accumulation. Sci Total Environ 573:123–130

    CAS  Google Scholar 

  • Gunawardena J, Egodawatta P, Ayoko GA, Goonetilleke A (2013) Atmospheric deposition as a source of heavy metals in urban stormwater. Atmos Environ 68:235–242

    CAS  Google Scholar 

  • Hariram M, Sahu R, Elumalai SP (2018) Impact assessment of atmospheric dust on foliage pigments and pollution resistances of plants grown nearby coal based thermal power plants. Arch Environ Contam Toxicol 74:56–70

    CAS  Google Scholar 

  • Hemeda HM, Klein B (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–185

    CAS  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    CAS  Google Scholar 

  • Huang H, Jiang Y, Xu X, Cao X (2018) In vitro bioaccessibility and health risk assessment of heavy metals in atmospheric particulate matters from three different functional areas of Shanghai, China. Sci Total Environ 610:546–554

    Google Scholar 

  • Jadoon WA, Khpalwak W, Chidya RCG, Abdel-Dayem SMMA, Takeda K, Makhdoom MA, Sakugawa H (2018) Evaluation of levels, sources and health hazards of road-dust associated toxic metals in Jalalabad and Kabul cities, Afghanistan. Arch Environ Contam Toxicol 74:32–45

    CAS  Google Scholar 

  • Khalid S, Shahid M, Dumat C, Niazi NK, Bibi I, Gul Bakhat HFS, Abbas G, Murtaza B, Javeed HMR (2017) Influence of groundwater and wastewater irrigation on lead accumulation in soil and vegetables: implications for health risk assessment and phytoremediation. Int J Phytoremediation:0–0

  • Kim HS, Kim K-R, Kim W-I, Owens G, Kim K-H (2017) Influence of road proximity on the concentrations of heavy metals in Korean urban agricultural soils and crops. Arch Environ Contam Toxicol 72:260–268

    CAS  Google Scholar 

  • Klink A, Polechońska L, Dambiec M, Białas K (2018) A comparative study on macro-and microelement bioaccumulation properties of leaves and bark of Quercus petraea and Pinus sylvestris. Arch Environ Contam Toxicol 74:71–79

    CAS  Google Scholar 

  • Kováčik J, Dresler S, Peterková V, Babula P (2018) Metal-induced oxidative stress in terrestrial macrolichens. Chemosphere 203:402–409

    Google Scholar 

  • Li X, Li Z, Lin C-J, Bi X, Liu J, Feng X, Zhang H, Chen J, Wu T (2018) Health risks of heavy metal exposure through vegetable consumption near a large-scale Pb/Zn smelter in Central China. Ecotoxicol Environ Saf 161:99–110

    CAS  Google Scholar 

  • Lichtenthaler HK (1987): [34] chlorophylls and carotenoids: pigments of photosynthetic biomembranes, Plant Cell Membranes Academic Press, pp. 350–382

  • Liu Y, Xing J, Wang S, Fu X, Zheng H (2018) Source-specific speciation profiles of PM 2.5 for heavy metals and their anthropogenic emissions in China. Environ Pollut 239:544–553

    CAS  Google Scholar 

  • Mombo S, Foucault Y, Deola F, Gaillard I, Goix S, Shahid M, Schreck E, Pierart A, Dumat C (2016) Management of human health risk in the context of kitchen gardens polluted by lead and cadmium near a lead recycling company. J Soils Sediments 16:1214–1224

    CAS  Google Scholar 

  • Natasha SM, Dumat C, Khalid S, Rabbani F, Farooq ABU, Amjad M, Abbas G, Niazi NK (2018a) Foliar uptake of arsenic nanoparticles by spinach: an assessment of physiological and human health risk implications. Environ Sci Pollut Res Int 26:20121–20131

    Google Scholar 

  • Natasha SM, Niazi NK, Khalid S, Murtaza B, Bibi I, Rashid MI (2018b) A critical review of selenium biogeochemical behavior in soil-plant system with an inference to human health. Environ Pollut 234:915–934

    CAS  Google Scholar 

  • Natasha, Shahid M, Khalid S, Dumat C, Pierart A, Niazi NK (2019) Biogeochemistry of antimony in soil-plant system: ecotoxicology and human health. Applied Geochemistry

  • Phi TH, Chinh PM, Cuong DD, Ly LTM, Van Thinh N, Thai PK (2018) Elemental concentrations in roadside dust along two National Highways in Northern Vietnam and the health-risk implication. Arch Environ Contam Toxicol 74:46–55

    CAS  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136

    CAS  Google Scholar 

  • Raessler M (2018) The arsenic contamination of drinking and groundwaters in Bangladesh: featuring biogeochemical aspects and implications on public health. Arch Environ Contam Toxicol 75:1–7

    CAS  Google Scholar 

  • Rizvi A, Khan MS (2018) Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicol Environ Saf 157:9–20

    CAS  Google Scholar 

  • Sawut R, Kasim N, Maihemuti B, Hu L, Abliz A, Abdujappar A, Kurban M (2018) Pollution characteristics and health risk assessment of heavy metals in the vegetable bases of northwest China. Sci Total Environ 642:864–878

    CAS  Google Scholar 

  • Schreck E, Foucault Y, Sarret G, Sobanska S, Cécillon L, Castrec-Rouelle M, Uzu G, Dumat C (2012) Metal and metalloid foliar uptake by various plant species exposed to atmospheric industrial fallout: mechanisms involved for lead. Sci Total Environ 427:253–262

    Google Scholar 

  • Schreck E, Laplanche C, Le Guédard M, Bessoule J-J, Austruy A, Xiong T, Foucault Y, Dumat C (2013) Influence of fine process particles enriched with metals and metalloids on Lactuca sativa L. leaf fatty acid composition following air and/or soil-plant field exposure. Environ Pollut 179:242–249

    CAS  Google Scholar 

  • Schreck E, Dappe V, Sarret G, Sobanska S, Nowak D, Nowak J, Stefaniak EA, Magnin V, Ranieri V, Dumat C (2014) Foliar or root exposures to smelter particles: consequences for lead compartmentalization and speciation in plant leaves. Sci Total Environ 476-477:667–676

    CAS  Google Scholar 

  • Shahid M, Pinelli E, Pourrut B, Silvestre J, Dumat C (2011) Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. Ecotoxicol Environ Saf 74:78–84

    CAS  Google Scholar 

  • Shahid M, Pinelli E, Dumat C (2012) Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands. J Hazard Mater 219:1–12

    Google Scholar 

  • Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014): Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants, reviews of environmental contamination and toxicology volume 232. Springer, pp. 1-44

  • Shahid M, Dumat C, Khalid S, Schreck E, Xiong T, Niazi NK (2017a) Foliar heavy metal uptake, toxicity and detoxification in plants: a comparison of foliar and root metal uptake. J Hazard Mater 325:36–58

    CAS  Google Scholar 

  • Shahid M, Rafiq M, Niazi NK, Dumat C, Shamshad S, Khalid S, Bibi I (2017c) Arsenic accumulation and physiological attributes of spinach in the presence of amendments: an implication to reduce health risk. Environ Sci Pollut Res 24:16097–16106

    CAS  Google Scholar 

  • Shahid M, Pinelli E, Dumat C (2018) Tracing trends in plant physiology and biochemistry: need of databases from genetic to kingdom level. Plant Physiol Biochem 127:630–635

    CAS  Google Scholar 

  • Shahid M, Shamshad S, Farooq ABU, Rafiq M, Khalid S, Dumat C, Zhang Y, Hussain I, Niazi NK (2019) Comparative effect of organic amendments on physio-biochemical traits of young and old bean leaves grown under cadmium stress: a multivariate analysis. Environ Sci Pollut Res 26:11579–11590

    CAS  Google Scholar 

  • Song J, Zhang H, Duan C, Cui X (2018) Exogenous application of succinic acid enhances tolerance of Larix olgensis seedling to lead stress. J For Res 29:1497–1505

    CAS  Google Scholar 

  • Uzu G, Sobanska S, Aliouane Y, Pradere P, Dumat C (2009) Study of lead phytoavailability for atmospheric industrial micronic and sub-micronic particles in relation with lead speciation. Environ Pollut 157:1178–1185

    CAS  Google Scholar 

  • Uzu G, Sobanska S, Sarret G, Munoz M, Dumat C (2010) Foliar lead uptake by lettuce exposed to atmospheric fallouts. Environ Sci Technol 44:1036–1042

    CAS  Google Scholar 

  • Uzu G, Sauvain JJ, Baeza-Squiban A, Riediker M, Hohl MS, Val S, Tack K, Denys S, Pradere P, Dumat C (2011) In vitro assessment of the pulmonary toxicity and gastric availability of lead-rich particles from a lead recycling plant. Environ Sci Technol 45:7888–7895

    CAS  Google Scholar 

  • Uzu G, Schreck E, Xiong T, Macouin M, Lévêque T, Fayomi B, Dumat C (2014) Urban market gardening in Africa: foliar uptake of metal (loid) s and their bioaccessibility in vegetables; implications in terms of health risks. Water Air Soil Pollut 225:2185

    Google Scholar 

  • Wang Z, Watanabe I, Ozaki H, Zhang J (2018) Enrichment and bioavailability of trace elements in soil in vicinity of railways in Japan. Arch Environ Contam Toxicol 74:16–31

    CAS  Google Scholar 

  • Xiong T-T, Leveque T, Austruy A, Goix S, Schreck E, Dappe V, Sobanska S, Foucault Y, Dumat C (2014a) Foliar uptake and metal (loid) bioaccessibility in vegetables exposed to particulate matter. Environ Geochem Health 36:897–909

    CAS  Google Scholar 

  • Xiong T, Leveque T, Shahid M, Foucault Y, Mombo S, Dumat C (2014b) Lead and cadmium phytoavailability and human bioaccessibility for vegetables exposed to soil or atmospheric pollution by process ultrafine particles. J Environ Qual 43:1593–1600

    Google Scholar 

  • Xiong T, Austruy A, Pierart A, Shahid M, Schreck E, Mombo S, Dumat C (2016) Kinetic study of phytotoxicity induced by foliar lead uptake for vegetables exposed to fine particles and implications for sustainable urban agriculture. J Environ Sci 46:16–27

    CAS  Google Scholar 

  • Xiong T, Dumat C, Dappe V, Vezin H, Schreck E, Shahid M, Pierart A, Sobanska S (2017) Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture. Environ Sci Technol 51:5242–5251

    CAS  Google Scholar 

  • Xiong T, Zhang T, Dumat C, Sobanska S, Dappe V, Shahid M, Xian Y, Li X, Li S (2018) Airborne foliar transfer of particular metals in Lactuca sativa L.: translocation, phytotoxicity, and bioaccessibility. Environ Sci Pollut Res 26:20064–20078. https://doi.org/10.1007/s11356-018-3084-x

    Article  CAS  Google Scholar 

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Correspondence to Muhammad Shahid.

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Natasha, Shahid, M. & Khalid, S. Foliar application of lead and arsenic solutions to Spinacia oleracea: biophysiochemical analysis and risk assessment. Environ Sci Pollut Res 27, 39763–39773 (2020). https://doi.org/10.1007/s11356-019-06519-7

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