Bitkilerde Kurşun Toksisitesi ve Kurşun Toleransı

Yıl 2020, Cilt: 3 Sayı: 4, 329 - 339, 01.10.2020

Ali Doğru

Öz

Doğada kalıcı ve toksik bir kirletici olarak kurşunun canlı organizmalar için bilinen biyolojik bir fonksiyonu olmadığı gibi yüksek kurşun konsantrasyonları bitkiler için zararlıdır. Bitkiler tarafından kök yoluyla alınan kurşunun büyük kısmı köklerde tutulurken çok az bir kısmı bitkinin toprak üstü organlarına taşınır. Böylece kurşunun besin zincirine katılması kısıtlanmış olur. Kurşun bitkilerde aktif oksijen türlerinin birikim hızını artırarak oksidatif strese neden olmaktadır. Sonuçta tohum çimlenmesi, fide büyümesi, proteinler, fotosentez, solunum, mineral madde beslenmesi ve su ilişkileri üzerinde olumsuz etkilere neden olur. Bitkiler kurşunun dokularındaki dağılımını engelleyerek, özellikle vakuollerde depo ederek ve antioksidant sistemin çeşitli bileşenleri ile kurşun toksisitesine karşı tolerans göstermeye çalışır. Bu çalışmada kurşun toksisitesinin bitkilerde neden olduğu metabolik bozukluklar ve tolerans mekanizmaları tartışılmıştır.

Anahtar Kelimeler

Antioxidant, Kurşun, Pb, Toksisite, Tolerans

Destekleyen Kurum

Sakarya Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi

Proje Numarası

2011-50-01-026

Lead Toxicity and Lead Tolerance in Plants

Öz

As a persistant and toxic pollutant in nature, lead does not have any known biological importance for living things and higher lead concentrations are harmful for plants. Lead enters plants mainly through the roots. A considerable amount of lead is sequestered in the roots while small amount is translocated to the leaves. Thus contamination of the food chain by lead is restricted. Lead causes oxidative stress in plants by accelerating the formation rate of active oxygen species. As a result, it leads to some noxious effects on plants such as germination, seedling growth, proteins, photosynthesis, respiration, mineral nutrition and water relations. Plants try to acquire tolerance by preventing translocation of lead, sequestering it in vacuoles and antioxidant system. In this study, metabolic anomalies caused by lead toxicity and tolerance mechanisms in plants are discussed.

Anahtar Kelimeler

Antioksidant, Lead, Pb, Toxicity, Tolerance

Proje Numarası

2011-50-01-026

Kaynakça

• Afify DG, Abdel-Satar AM. 2020. Risk assessment of heavy metal pollution in water, sediment and plants in the Nile River in the Cairo region, Egypt. Hydrobiol Studies, 49: 1-12.
• Alamri SA, Siddiqui MH, Al-Khaishany MYY, Khan MN, Ali HM, Alaraidh IA, Alsahli AA, Al-Rabiah H, Mateen M. 2018. Ascorbic acid improves the tolerance of wheat plants to lead toxicity. J. Plant Int, 13(1): 409-419.
• Alexander PD, Alloway BJ, Dourado AM. 2006. Genotypic variations in the accumulation of Cd, Cu, Pb and Zn exhibited by six commonly grown vegetables. Environ Pollut, 144: 736–745.
• Andra SS, Datta R, Sarkar D, Sarkar D, Saminathan SK, Mullens CP, Bach SB. 2009. Analysis of phytochelatin complexes in the lead tolerant vetiver grass [Vetiveria zizanioides (L.)] using liquid chromatography and mass spectrometry. Environ Pollut, 157(7): 2173–2183.
• Arazi T, Sunkar R, Kaplan B, Fromm H. 1999. A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J, 20: 171–182.
• Arias JA, Peralta-Videa JR, Ellzey JT, Ren M, Viveros MN, Gardea-Torresdey JL. 2010. Effects of Glomus deserticola inoculation on Prosopis: enhancing chromium and lead uptake and translocation as confirmed by X-ray mapping, ICP-OES and TEM techniques. Environ Exp Bot, 68(2): 139–148.
• Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid M, Guiresse M, Pradere P, Dumat C. 2008. A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere, 71(11): 2187–2192.
• Assche F, Clijsters H. 1990. Effects of metals on enzyme activity in plants. Plant Cell Environ, 13(3): 195–206.
• Atici Ö, Agar G, Battal P. 2005. Changes in phytohormone contents in chickpea seeds germinating under lead or zinc stress. Biol Plantarum, 49(2): 215–222.
• Barbosa J, Cabral T, Ferreira D, Agnez-Lima L, Batistuzzo de Medeiros S. 2010. Genotoxicity assessment in aquatic environment impacted by the presence of heavy metals. Ecotoxicol Environ Saf, 73(3): 320–325.
• Barceló J, Poschenrieder C. 1990. Plant water relations as affected by heavy metal stress: a review. J Plant Nutr, 13(1): 1–37.
• Barrutia O, Garbisu C, Hernández-Allica J, García-Plazaola JI, Becerril JM. 2010. Differences in EDTA-assisted metal phytoextraction between metallicolous and non-metallicolous accessions of Rumex acetosa L. Environ Pollut, 158(5): 1710–1715.
• Bi X, Ren L, Gong M, He Y, Wang L, Ma Z. 2010. Transfer of cadmium and lead from soil to mangoes in an uncontaminated area, Hainan Island, China. Geoderma, 155(1–2): 115–120.
• Bressler JP, Olivi L, Cheong JH, Kim Y, Bannona D. 2004. Divalent metal transporter 1 in lead and cadmium transport. Ann N Y Acad Sci, 1012: 142–152.
• Brunet J, Varrault G, Zuily-Fodil Y, Repellin A. 2009. Accumulation of lead in the roots of grass pea (Lathyrus sativus L.) plants triggers systemic variation in gene expression in the shoots. Chemosphere, 77(8): 1113–1120.
• Cao X, Ma LQ, Singh SP, Zhou Q. 2008. Phosphate-induced lead immobilization from different lead minerals in soils under varying pH conditions. Environ Pollut, 152(1): 184–192.
• Cecchi M, Dumat C, Alric A, Felix-Faure B, Pradere P, Guiresse M. 2008. Multi-metal contamination of a calcic cambisol by fallout from a lead-recycling plant. Geoderma, 144(1–2): 287–298.
• Chatterjee C, Dube BK, Sinha P, Srivastava P. 2004. Detrimental effects of lead phytotoxicity on growth, yield, and metabolism of rice. Commun Soil Sci Plant Anal, 35(1–2): 255–265.
• Chen C, Tian T, Wang MK, Wang G. 2016. Release of Pb in soils washed with various extractants. Geoderma, 275: 74-81.
• Dey SK, Dey J, Patra S, Pothal D. 2007. Changes in the antioxidative enzyme activities and lipid peroxidation in wheat seedlings exposed to cadmium and lead stress. Braz J Plant Physiol, 19(1): 53–60.
• Dias MC, Ponte NM, Santos C. 2019. Lead induces oxidative stress in Pisum sativum plants and changes the level of phytohormones with antioxidant activity. Plant Physiol Biochem, 137: 121-129.
• Doğru A. 2019. Bazı arpa genotiplerinde kurşun toleransının klorofil a floresansı ile değerlendirilmesi. JONAS, 2(2): 228-238.
• Doğru A. 2020. Antioxidant responses of barley (Hordeum vulgare L.) genotypes to lead toxicity. Biologia, https://doi.org/10.2478/s11756-020-00516-9
• Dumat C, Quenea K, Bermond A, Toinen S, Benedetti MF. 2006. Study of the trace metal ion influence on the turnover of soil organic matter in cultivated contaminated soils. Environ Pollut, 142(3): 521–529.
• Elzbieta W, Miroslawa C. 2005. Lead-induced histological and ultrastructural changes in the leaves of soybean (Glycine max (L.) Merr.). Soil Sci Plant Nutr, 51(2): 203–212.
• Garcia JS, Gratão PL, Azevedo RA, Arruda MAZ. 2006. Metal contamination effects on sunflower (Helianthus annuus L.) growth and protein expression in leaves during development. J Agric Food Chem, 54(22): 8623–8630.
• Ghani A, Hussain M, Ikram M, Hameed T. 2016. Toxic effect of lead on germination and seedling growth of Brassica campestris L. Int J Geol Earth Environ Sci, 6(2): 45-48.
• Gichner T, Znidar I, Száková J. 2008. Evaluation of DNA damage and mutagenicity induced by lead in tobacco plants. Mutat Res Genet Toxicol Environ Mutagen, 652(2): 186–190.
• Ginn BR, Szymanowski JS, Fein JB. 2008. Metal and proton binding onto the roots of Fescue rubra. Chem Geol, 253(3–4): 130–135.
• Gopal R, Rizvi AH. 2008. Excess lead alters growth, metabolism and translocation of certain nutrients in radish. Chemosphere 70(9): 1539–1544.
• Grover P, Rekhadevi P, Danadevi K, Vuyyuri S, Mahboob M, Rahman M. 2010. Genotoxicity evaluation in workers occupationally exposed to lead. Int J Hyg Environ Health, 213(2): 99–106.
• Gupta D, Huang H, Yang X, Razafindrabe B, Inouhe M. 2010. The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater, 177(1–3): 437–444.
• Gupta D, Nicoloso F, Schetinger M, Rossato L, Pereira L, Castro G, Srivastava S, Tripathi R. 2009. Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater, 172(1): 479–484.
• Hammett FS. 1928. Studies in the biology of metals. Protoplasma, 5(1): 535–542.
• Hirsch RE, Lewis BD, Spalding EP, Sussman MR. 1998. A role for the AKT1 potassium channel in plant nutrition. Science, 280(5365): 918–921.
• Hu J, Shi G, Xu Q, Wang X, Yuan Q, Du K. 2007. Effects of Pb2+ on the active oxygen scavenging enzyme activities and ultrastructure in Potamogeton crispus leaves. Russ J Plant Physiol, 54(3): 414–419.
• Huang JW, Cunningham SD. 1996. Lead phytoextraction: species variation in lead uptake and translocation. New Phytol, 134: 75–84.
• Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J. 2008. Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater, 154(1–3): 914–926.
• Islam E, Yang X, Li T, Liu D, Jin X, Meng F. 2007. Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater, 147(3): 806–816.
• Jiang W, Liu D. 2010. Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biol, 10: 40–40.
• Kim D, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y. 2006. AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physioli 140(3): 922–932.
• Kim YY, Yang YY, Lee Y. 2002. Pb and Cd uptake in rice roots. Physiol Plantarum, 116: 368–372.
• Kohler C, Merkle T, Neuhaus G. 1999. Characterisation of a novel gene family of putative cyclic nucleotide- and calmodulin-regulated ion channels in Arabidopsis thaliana. Plant J, 18(1): 97–104.
• Kohli SK, Handa N, Sharma A, Gautam V, Arora S, Bhardwaj R, Alyemeni MN, Wijaya L., Ahmad P. 2018. Combined effect of 24-epibrassinolide and salicylic acid mitigates lead (Pb) toxicity by modulating various metabolites in Brassica juncea L. seedlings. Protoplasma, 255, 11-24.
• Komjarova I, Blust R. 2009. Effect of Na, Ca and pH on simultaneous uptake of Cd, Cu, Ni, Pb, and Zn in the water flea Daphnia magna measured using stable isotopes. Aquat Toxicol, 94(2): 81–86.
• Kopittke PM, Asher CJ, Kopittke RA, Menzies NW. 2007. Toxic effects of Pb2+ on growth of cowpea (Vigna unguiculata). Environ Pollut, 150(2): 280–287.
• Kopittke PM, Asher CJ, Kopittke RA, Menzies NW. 2008. Prediction of Pb speciation in concentrated and dilute nutrient solutions. Environ Pollut, 153(3): 548–554.
• Kosobrukhov A, Knyazeva I, Mudrik V. 2004. Plantago major plants responses to increase content of lead in soil: growth and photosynthesis. Plant Growth Regul, 42(2): 145–151.
• Kovalchuk I, Titov V, Hohn B, Kovalchuk O. 2005. Transcriptome profiling reveals similarities and differences in plant responses to cadmium and lead. Mutat Res: Fundam Mol Mech Mutagen, 570(2): 149–161.
• Krzeslowska M, Lenartowska M, Mellerowicz EJ, Samardakiewicz S, Wozny A. 2009. Pectinous cell wall thickenings formation–a response of moss protonemata cells to lead. Environ Exp Bot, 65(1): 119–131.
• Krzesłowska M, Lenartowska M, Samardakiewicz S, Bilski H, Wozny A. 2010. Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable–a remobilization can occur. Environ Pollut, 158(1): 325–338.
• Lane SD, Martin ES. 1977. A histochemical investigation of lead uptake in Raphanus sativus. New Phytol, 79(2): 281–286.
• Lawal O, Sanni A, Ajayi I, Rabiu O. 2010. Equilibrium, thermodynamic and kinetic studies for the biosorption of aqueous lead(II) ions onto the seed husk of Calophyllum inophyllum. J Hazard Mater, 177(1–3): 829–835.
• Liao Y, Chien SC, Wang M, Shen Y, Hung P, Das B. 2006. Effect of transpiration on Pb uptake by lettuce and on water soluble low molecular weight organic acids in rhizosphere. Chemosphere, 65(2): 343–351.
• Liu D, Li T, Jin X, Yang X, Islam E, Mahmood Q. 2008. Lead induced changes in the growth and antioxidant metabolism of the lead accumulating and non-accumulating ecotypes of Sedum alfredii. J Integr Plant Biol, 50(2): 129–140.
• Liu T, Liu S, Guan H, Ma L, Chen Z, Gu H. 2009. Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead (Pb). Environ Exp Bot, 67(2): 377–386.
• Liu X, Peng K, Wang A, Lian C, Shen Z. 2010. Cadmium accumulation and distribution in populations of Phytolacca americana L. and the role of transpiration. Chemosphere, 78(9): 1136–1141.
• López ML, Peralta-Videa JR, Benitez T, Duarte-Gardea M, Gardea-Torresdey JL. 2007. Effects of lead, EDTA, and IAA on nutrient uptake by alfalfa plants. J Plant Nutr, 30(8): 1247–1261.
• Lyu G, Li D, Li S, Ning C, Qin R. 2020. Genotoxic effects and proteomic analysis on Allium cepa var. agrogarum L. root cells under Pb stress. Ecotoxicol, 29: 959-972.
• 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): 1–13.
• Małecka A, Piechalak A, Morkunas I, Tomaszewska B. 2008. Accumulation of lead in root cells of Pisum sativum. Acta Physiol Plant, 30(5): 629–637.
• Małkowski E, Kita A, Galas W, Karcz W, Kuperberg JM. 2002. Lead distribution in corn seedlings (Zea mays L.) and its effect on growth and the concentrations of potassium and calcium. Plant Growth Regul, 37(1): 69–76.
• Marcato-Romain C, Guiresse M, Cecchi M, Cotelle S, Pinelli E. 2009. New direct contact approach to evaluate soil genotoxicity using the Vicia faba micronucleus test. Chemosphere, 77(3): 345–350.
• Martinez MS, Galante PM, Plata IH, Cuevas LV, Morales AF, Hernandez LO, Trujillo KF, Quintana FR, Sanchez ET. 2020. Heavy metal bioaccumulation anf 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.
• Meyers DER, Auchterlonie GJ, Webb RI, Wood B. 2008. Uptake and localisation of lead in the root system of Brassica juncea. Environ Pollut, 153(2): 323–332.
• Mishra S, Srivastava S, Tripathi R, Kumar R, Seth C, Gupta D. 2006. Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere, 65(6): 1027–1039.
• Orenes AL, Dias MC, Ferrer MA, Calderon A, Pereira JM, Correia C, Santos C. 2018. Different mechanisms of metalliferous Zygophyllum fabago and roots to cope with Pb toxicity. Env Sci Pollut Res, 25: 1319-1330.
• Padmavathiamma PK, Li LY. 2010. Phytoavailability and fractionation of lead and manganese in a contaminated soil after application of three amendments. Bioresour Technol, 101(14): 5667–5676.
• Pais I, Jones JB. 2000. The handbook of trace elements. Saint Lucie Press, Boca Raton, FL, p 223.
• Parys E, Romanowska E, Siedlecka M, Poskuta J. 1998. The effect of lead on photosynthesis and respiration in detached leaves and in mesophyll protoplasts of Pisum sativum. Acta Physiol Plant, 20(3): 313–322.
• 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.
• Piechalak A, Tomaszewska B, Baralkiewicz D, Malecka A. 2002. Accumulation and detoxification of lead ions in legumes. Phytochem, 60(2): 153–162.
• Piotrowska A, Bajguz A, Godlewska-Zylkiewicz B, Czerpak R, Kaminska M. 2009. Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot, 66(3): 507–513.
• Pourrut B, Perchet G, Silvestre J, Cecchi M, Guiresse M, Pinelli E. 2008. Potential role of NADPH-oxidase in early steps of lead-induced oxidative burst in Vicia faba roots. J Plant Physiol, 165(6): 571–579.
• Punamiya P, Datta R, Sarkar D, Barber S, Patel M, Das P. 2010. Symbiotic role of glomus mosseae in phytoextraction of lead in vetiver grass [Chrysopogon zizanioides (L.)]. J Hazard Mater, 177(1–3): 465–474.
• Qureshi M, Abdin M, Qadir S, Iqbal M. 2007. Lead-induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. Biol Plantarum, 51(1): 121–128.
• Reddy AM, Kumar SG, Jyothsnakumari G, Thimmanaik S, Sudhakar C. 2005. Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum L.). Chemosphere, 60(1): 97–104.
• Roelfsema MRG, Hedrich R. 2005. In the light of stomatal opening: new insights into ‘the Watergate’. New Phytol, 167(3): 665–691.
• Romanowska E, Igamberdiev AU, Parys E, Gardeström P. 2002. Stimulation of respiration by Pb2+ in detached leaves and mitochondria of C3 and C4 plants. Physiol Plant, 116(2): 148–154.
• Romanowska E, Wróblewska B, Drozak A, Siedlecka M. 2006. High light intensity protects photosynthetic apparatus of pea plants against exposure to lead. Plant Physiol Biochem, 44(5–6): 387–394.
• Rucinska R, Sobkowiak R, Gwózdz EA. 2004. Genotoxicity of lead in lupin root cells as evaluated by the comet assay. Cell Mol Biol Lett, 9(3): 519–528.
• Sammut M, Noack Y, Rose J, Hazemann J, Proux O, Depoux Ziebel M, Fiani E. 2010. Speciation of Cd and Pb in dust emitted from sinter plant. Chemosphere, 78(4): 445–450.
• Sengar RS, Gautam M, Sengar RS, Sengar RS, Garg SK, Sengar K, Chaudhary R. 2009. Lead stress effects on physiobiochemical activities of higher plants. Rev Environ Contam Toxicol, 196: 1–21.
• Seregin IV, Ivanov VB. 2001. Physiological aspects of cadmium and lead toxic effects on higher plants. Russ J Plant Physiol, 48(4): 523–544.
• Seregin IV, Shpigun LK, Ivanov VB. 2004. Distribution and toxic effects of cadmium and lead on maize roots. Russ J Plant Physiol, 51(4): 525–533.
• 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(1): 78–84.
• Sharma P, Dubey RS. 2005. Lead toxicity in plants. Braz J Plant Physiol, 17(1): 35–52.
• 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.
• Sinha P, Dube B, Srivastava P, Chatterjee C. 2006. Alteration in uptake and translocation of essential nutrients in cabbage by excess lead. Chemosphere, 65(4): 651–656.
• Steffan JJ, Brevik EC, Burges LC, Cerda A. 2018. The effect of soil on human health: an overview. Eur J Soil Sci, 69: 159-171.
• Tabelin C, Igarashi T. 2009. Mechanisms of arsenic and lead release from hydrothermally altered rock. J Hazard Mater, 169(1–3): 980–990.
• Tomulescu IM, Radoviciu EM, Merca VV, Tuduce AD. 2004. Effect of copper, zinc and lead and their combinations on the germination capacity of two cereals. J Agric Sci, 15.
• Tung G, Temple PJ. 1996. Uptake and localization of lead in corn (Zea mays L.) seedlings, a study by histochemical and electron microscopy. Sci Total Environ, 188(2–3): 71–85.
• 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(4): 1178–1185.
• 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.
• Vadas TM, Ahner BA. 2009. Cysteine- and glutathione-mediated uptake of lead and cadmium into Zea mays and Brassica napus roots. Environ Pollut, 157(8–9): 2558–2563.
• Vega F, Andrade M, Covelo E. 2010. Influence of soil properties on the sorption and retention of cadmium, copper and lead, separately and together, by 20 soil horizons: comparison of linear regression and tree regression analyses. J Hazard Mater, 174(1–3): 522–533.
• Verbruggen N, Hermans C, Schat H. 2009. Molecular mechanisms of metal hyperaccumulation in plants. New Phytol, 181: 759–776.
• Wang H, Shan X, Wen B, Owens G, Fang J, Zhang S. 2007. Effect of indole-3-acetic acid on lead accumulation in maize (Zea mays L.) seedlings and the relevant antioxidant response. Environ Exp Bot, 61(3): 246–253.
• Wierzbicka MH, Przedpełska E, Ruzik R, Ouerdane L, Połec-Pawlak K, Jarosz M, Szpunar J, Szakiel A. 2007. Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma, 231(1): 99–111.
• Wojas S, Ruszczynska A, Bulska E, Wojciechowski M, Antosiewicz DM. 2007. Ca2+-dependent plant response to Pb2+ is regulated by LCT1. Environ Pollut, 147(3): 584–592.
• Xiong Z, Zhao F, Li M. 2006. Lead toxicity in Brassica pekinensis Rupr.: effect on nitrate assimilation and growth. Environ Toxicol, 21(2): 147–153.
• Yadav S. 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(2): 167–179.
• Yan ZZ, Ke L, Tam NFY. 2010. Lead stress in seedlings of Avicennia marina, a common mangrove species in South China, with and without cotyledons. Aquat Bot, 92(2): 112–118.
• Zaier H, Ghnaya T, Ben Rejeb K, Lakhdar A, Rejeb S, Jemal F. 2010. Effects of EDTA on phytoextraction of heavy metals (Zn, Mn and Pb) from sludge-amended soil with Brassica napus. Bioresour Technol, 101(11): 3978–3983.
• Zhang Y, Deng B, Li Z. 2018. Inhibition of NADPH oxidase increases defense enzyme activities and improves maize seed germination under Pb stress. Ecotoxicol Environ Safety, 158: 187-192.