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Heavy metal-induced oxidative stress on seed germination and seedling development: a critical review

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A Correction to this article was published on 27 December 2017

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Abstract

Heavy metal contamination in soils can influence plants and animals, often leading to toxicosis. Heavy metals can impact various biochemical processes in plants, including enzyme and antioxidant production, protein mobilization and photosynthesis. Hydrolyzing enzymes play a major role in seed germination. Enzymes such as acid phosphatases, proteases and α-amylases are known to facilitate both seed germination and seedling growth via mobilizing nutrients in the endosperm. In the presence of heavy metals, starch is immobilized and nutrient sources become limited. Moreover, a reduction in proteolytic enzyme activity and an increase in protein and amino acid content can be observed under heavy metal stress. Proline, is an amino acid which is essential for cellular metabolism. Numerous studies have shown an increase in proline content under oxidative stress in higher plants. Furthermore, heat shock protein production has also been observed under heavy metal stress. The chloroplast small heat shock proteins (Hsp) reduce photosynthesis damage, rather than repair or help to recover from heavy metal-induced damage. Heavy metals are destructive substances for photosynthesis. They are involved in destabilizing enzymes, oxidizing photosystem II (PS II) and disrupting the electron transport chain and mineral metabolism. Although the physiological effects of Cd have been investigated thoroughly, other metals such as As, Cr, Hg, Cu and Pb have received relatively little attention. Among agricultural plants, rice has been studied extensively; additional studies are needed to characterize toxicities of different heavy metals on other crops. This review summarizes the current state of our understanding of the effects of heavy metal stress on seed germination and seedling development and highlights informational gaps and areas for future research.

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Change history

  • 27 December 2017

    Unfortunately, in the original publication of the article, Prof. Yong Sik Ok’s affiliation was incorrectly published. The author’s affiliation is as follows.

References

  • Abraham, K., Sridevi, R., Suresh, B., & Damodharam, T. (2013). Effect of heavy metals (Cd, Pb, Cu) on seed germination of Arachis hypogeae L. Asian Journal of Plant Science and Research, 3(1), 10–12.

    CAS  Google Scholar 

  • Adrees, M., Ali, S., Rizwan, M., Ibrahim, M., Abbas, F., Farid, M., et al. (2015). The effect of excess copper on growth and physiology of important food crops: A review. Environmental Science and Pollution Research, 22(11), 8148–8162.

    Article  CAS  Google Scholar 

  • Ahmad, I., Akhtar, M. J., Asghar, H. N., & Zahir, Z. A. (2013). Comparative efficacy of growth media in causing cadmium toxicity to wheat at seed germination stage. International Journal of Agriculture & Biology, 15, 517–522.

    CAS  Google Scholar 

  • Ahmad, I., Akhtar, M. J., Zahir, Z. A., & Jamil, A. (2012). Effect of cadmium on seed germination and seedling growth of four wheat (Triticum aestivum L.) cultivars. Pakistan Journal of Botany, 44(5), 1569–1574.

    Google Scholar 

  • Ahsan, N., Lee, D.-G., Lee, S.-H., Kang, K. Y., Lee, J. J., Kim, P. J., et al. (2007a). Excess copper induced physiological and proteomic changes in germinating rice seeds. Chemosphere, 67(6), 1182–1193.

    Article  CAS  Google Scholar 

  • Ahsan, N., Lee, S.-H., Lee, D.-G., Lee, H., Lee, S. W., Bahk, J. D., et al. (2007b). Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. Comptes Rendus Biologies, 330(10), 735–746.

    Article  CAS  Google Scholar 

  • Akinci, I. E., & Akinci, S. (2010). Effect of chromium toxicity on germination and early seedling growth in melon (Cucumis melo L.). African Journal of Biotechnology, 9(29), 4589–4594.

    CAS  Google Scholar 

  • Ali, M. B., Chun, H. S., Kim, B. K., & Lee, C. B. (2002). Cadmium-induced changes in antioxidant enzyme activities in rice (Oryza sativa L. cv. Dongjin). Journal of Plant Biology, 45(3), 134–140.

    Article  CAS  Google Scholar 

  • Arteca, R. N. (Ed.). (1996). Historical aspects and fundamental terms and concepts. In Plant growth substances (pp. 1–27). Berlin: Springer.

  • Ashraf, M., & Foolad, M. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59(2), 206–216.

    Article  CAS  Google Scholar 

  • Atici, Ö., Ağar, G., & Battal, P. (2005). Changes in phytohormone contents in chickpea seeds germinating under lead or zinc stress. Biologia Plantarum, 49(2), 215–222.

    Article  CAS  Google Scholar 

  • Aydinalp, C., & Marinova, S. (2009). The effects of heavy metals on seed germination and plant growth on alfalfa plant (Medicago sativa). Bulgarian Journal of Agricultural Science, 15(4), 347–350.

    Google Scholar 

  • Bakırdere, S., Bölücek, C., & Yaman, M. (2016). Determination of contamination levels of Pb, Cd, Cu, Ni, and Mn caused by former lead mining gallery. Environmental Monitoring and Assessment, 188(3), 1–7.

    Article  CAS  Google Scholar 

  • Bandara, T., Herath, I., Kumarathilaka, P., Hseu, Z.-Y., Ok, Y. S., & Vithanage, M. (2016). Efficacy of woody biomass and biochar for alleviating heavy metal bioavailability in serpentine soil. Environmental Geochemistry and Health. doi:10.1007/s10653-016-9842-0.

    Article  Google Scholar 

  • Bandara, T., Herath, I., Kumarathilaka, P., Seneviratne, M., Seneviratne, G., Rajakaruna, N., et al. (2017). Role of woody biochar and fungal–bacterial co-inoculation on enzyme activity and metal immobilization in serpentine soil. Journal of Soils and Sediments, 17(3), 665–673. doi:10.1007/s11368-015-1243-y.

    Article  CAS  Google Scholar 

  • Barceló, J., & Poschenrieder, C. (1990). Plant water relations as affected by heavy metal stress: A review. Journal of Plant Nutrition, 13(1), 1–37.

    Article  Google Scholar 

  • Barcelo, J., Poschenrieder, C., Andreu, I., & Gunse, B. (1986). Cadmium-induced decrease of water stress resistance in bush bean plants (Phaseolus vulgaris L. cv. Contender) I. Effects of Cd on water potential, relative water content, and cell wall elasticity. Journal of Plant Physiology, 125(1–2), 17–25.

    Article  CAS  Google Scholar 

  • Bashmakov, D. I., Lukatkin, A. S., Revin, V. V., Duchovskis, P., Brazaitytë, A., & Baranauskis, K. (2005). Growth of maize seedlings affected by different concentrations of heavy metals. Ekologija, 3, 22–27.

    Google Scholar 

  • Basile, A., Sorbo, S., Conte, B., Cardi, M., & Esposito, S. (2013). Ultrastructural changes and heat shock proteins 70 induced by atmospheric pollution are similar to the effects observed under in vitro heavy metals stress in Conocephalum conicum (Marchantiales–Bryophyta). Environmental Pollution, 182, 209–216.

    Article  CAS  Google Scholar 

  • Basta, N. T., Pantone, D., & Tabatabai, M. (1993). Path analysis of heavy metal adsorption by soil. Agronomy Journal, 85(5), 1054–1057.

    Article  CAS  Google Scholar 

  • Baszyński, T. (2014). Interference of Cd2+ in functioning of the photosynthetic apparatus of higher plants. Acta Societatis Botanicorum Poloniae, 55(2), 291–304.

    Article  Google Scholar 

  • Bénard, A., Rose, J., Hazemann, J.-L., Proux, O., Trotignon, L., Borschneck, D., et al. (2014). Modelling the Pb release during Portland cement alteration. arXiv:1402.2962.

  • Bewley, J. D. (1997). Seed germination and dormancy. The Plant Cell, 9(7), 1055.

    Article  CAS  Google Scholar 

  • Bolan, N. S., & Duraisamy, V. (2003). Role of inorganic and organic soil amendments on immobilisation and phytoavailability of heavy metals: A review involving specific case studies. Soil Research, 41(3), 533–555.

    Article  CAS  Google Scholar 

  • Boyd, R. S., & Rajakaruna, N. (2013). Heavy metal tolerance. In D. Gibson (Ed.), Oxford bibliographies in ecology. New York: Oxford University Press.

    Google Scholar 

  • Branzini, A., & Zubillaga, M. S. (2012). Comparative use of soil organic and inorganic amendments in heavy metals stabilization. Applied and Environmental Soil Science, 2012, 7. doi:10.1155/2012/721032.

    Article  CAS  Google Scholar 

  • Castaldi, P., Alberti, G., Merella, R., & Melis, P. (2005). Study of the organic matter evolution during municipal solid waste composting aimed at identifying suitable parameters for the evaluation of compost maturity. Waste Management, 25(2), 209–213. doi:10.1016/j.wasman.2004.12.011.

    Article  CAS  Google Scholar 

  • Charest, C., & Ton Phan, C. (1990). Cold acclimation of wheat (Triticum aestivum): Properties of enzymes involved in proline metabolism. Physiologia Plantarum, 80(2), 159–168.

    Article  CAS  Google Scholar 

  • Chen, C. T., Chen, L.-M., Lin, C. C., & Kao, C. H. (2001). Regulation of proline accumulation in detached rice leaves exposed to excess copper. Plant Science, 160(2), 283–290.

    Article  CAS  Google Scholar 

  • Choudhary, N., Sairam, R., & Tyagi, A. (2005). Expression of Δ1-pyrroline-5-carboxylate synthetase gene during drought in rice (Oryza sativa L.). Indian Journal of Biochemistry & Biophysics, 42, 366–370.

    CAS  Google Scholar 

  • Chugh, L., & Sawhney, S. (1996). Effect of cadmium on germination, amylases and rate of respiration of germinating pea seeds. Environmental Pollution, 92(1), 1–5.

    Article  CAS  Google Scholar 

  • Clemens, S. (2006). Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie, 88(11), 1707–1719.

    Article  CAS  Google Scholar 

  • Cokkizgin, A., & Cokkizgin, H. (2015). Effects of lead (PbCl2) stress on germination of lentil (Lens culinaris Medic.) lines. African Journal of Biotechnology, 9(50), 8608–8612.

    Google Scholar 

  • Dago, À., González, I., Ariño, C., Díaz-Cruz, J. M., & Esteban, M. (2014). Chemometrics applied to the analysis of induced phytochelatins in Hordeum vulgare plants stressed with various toxic non-essential metals and metalloids. Talanta, 118, 201–209.

    Article  CAS  Google Scholar 

  • Davies, K. J. (2001). Degradation of oxidized proteins by the 20S proteasome. Biochimie, 83(3), 301–310.

    Article  CAS  Google Scholar 

  • Davis, J. A. (1984). Complexation of trace metals by adsorbed natural organic matter. Geochimica et Cosmochimica Acta, 48(4), 679–691.

    Article  CAS  Google Scholar 

  • De Lacerda, L. D., & Salomons, W. (2012). Mercury from gold and silver mining: A chemical time bomb?. Berlin: Springer Science & Business Media.

    Google Scholar 

  • Debeaujon, I., & Koornneef, M. (2000). Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. Plant Physiology, 122(2), 415–424.

    Article  CAS  Google Scholar 

  • Dermont, G., Bergeron, M., Mercier, G., & Richer-Lafleche, M. (2008). Soil washing for metal removal: A review of physical/chemical technologies and field applications. Journal of Hazardous Materials, 152(1), 1–31.

    Article  CAS  Google Scholar 

  • Devi, R., Munjral, N., Gupta, A. K., & Kaur, N. (2013). Effect of exogenous lead on growth and carbon metabolism of pea (Pisum sativum L) seedlings. Physiology and Molecular Biology of Plants, 19(1), 81–89.

    Article  CAS  Google Scholar 

  • Diwan, H., Khan, I., Ahmad, A., & Iqbal, M. (2010). Induction of phytochelatins and antioxidant defence system in Brassica juncea and Vigna radiata in response to chromium treatments. Plant Growth Regulation, 61(1), 97–107.

    Article  CAS  Google Scholar 

  • Downs, C. A., Coleman, J. S., & Heckathorn, S. A. (1999). The chloroplast 22-Ku heat-shock protein: A lumenal protein that associates with the oxygen evolving complex and protects photosystem II during heat stress. Journal of Plant Physiology, 155(4), 477–487.

    Article  CAS  Google Scholar 

  • Dua, A., & Sawhney, S. K. (1991). Effect of chromium on activities of hydrolytic enzymes in germinating pea seeds. Environmental and Experimental Botany, 31(2), 133–139.

    Article  Google Scholar 

  • Dutta, P., Islam, M., & Mondal, S. (2014). Interactive effect of arsenic stress and seed phytate content on germination and seedling development of different vegetable crops. Journal of Plant Physiology & Pathology, 2(2), 2.

    Article  Google Scholar 

  • Fabro, G., Kovács, I., Pavet, V., Szabados, L., & Alvarez, M. E. (2004). Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. Molecular Plant–Microbe Interactions, 17(4), 343–350.

    Article  CAS  Google Scholar 

  • Falkowska, L., Reindl, A. R., Szumiło, E., Kwaśniak, J., Staniszewska, M., Bełdowska, M., et al. (2013). Mercury and chlorinated pesticides on the highest level of the food web as exemplified by herring from the Southern Baltic and African penguins from the zoo. Water, Air, and Soil Pollution, 224(5), 1–15.

    Article  CAS  Google Scholar 

  • Fariduddin, Q., Khalil, R. R., Mir, B. A., Yusuf, M., & Ahmad, A. (2013). 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environmental Monitoring and Assessment, 185(9), 7845–7856.

    Article  CAS  Google Scholar 

  • Fu, J., Zhao, C., Luo, Y., Liu, C., Kyzas, G. Z., Luo, Y., et al. (2014). Heavy metals in surface sediments of the Jialu River, China: Their relations to environmental factors. Journal of Hazardous Materials, 270, 102–109.

    Article  CAS  Google Scholar 

  • Fujii, H., Verslues, P. E., & Zhu, J.-K. (2007). Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. The Plant Cell, 19(2), 485–494.

    Article  CAS  Google Scholar 

  • Fulton, D. C., Stettler, M., Mettler, T., Vaughan, C. K., Li, J., Francisco, P., et al. (2008). β-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. The Plant Cell, 20(4), 1040–1058.

    Article  CAS  Google Scholar 

  • Gadepalle, V. P., Ouki, S. K., Herwijnen, R. V., & Hutchings, T. (2007). Immobilization of heavy metals in soil using natural and waste materials for vegetation establishment on contaminated sites. Soil and Sediment Contamination: An International Journal, 16(2), 233–251. doi:10.1080/15320380601169441.

    Article  CAS  Google Scholar 

  • Gajewska, E., & Skłodowska, M. (2008). Differential biochemical responses of wheat shoots and roots to nickel stress: Antioxidative reactions and proline accumulation. Plant Growth Regulation, 54(2), 179–188.

    Article  CAS  Google Scholar 

  • Gall, J. E., & Rajakaruna, N. (2013). The physiology, functional genomics, and applied ecology of heavy metal-tolerant Brassicaceae. In M. Lang (Ed.), Brassicaceae: Characterization, functional genomics and health benefits (pp. 121–148). New York: Nova.

  • Gallego, S. M., Benavides, M. P., & Tomaro, M. L. (1996). Effect of heavy metal ion excess on sunflower leaves: Evidence for involvement of oxidative stress. Plant Science, 121(2), 151–159.

    Article  CAS  Google Scholar 

  • Gianazza, E., Wait, R., Sozzi, A., Regondi, S., Saco, D., Labra, M., et al. (2007). Growth and protein profile changes in Lepidium sativum L. plantlets exposed to cadmium. Environmental and Experimental Botany, 59(2), 179–187.

    Article  CAS  Google Scholar 

  • Gratão, P. L., Polle, A., Lea, P. J., & Azevedo, R. A. (2005). Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology, 32(6), 481–494.

    Article  CAS  Google Scholar 

  • Groot, S., & Karssen, C. (1987). Gibberellins regulate seed germination in tomato by endosperm weakening: A study with gibberellin-deficient mutants. Planta, 171(4), 525–531.

    Article  CAS  Google Scholar 

  • Hadi, P., Gao, P., Barford, J. P., & McKay, G. (2013). Novel application of the nonmetallic fraction of the recycled printed circuit boards as a toxic heavy metal adsorbent. Journal of Hazardous Materials, 252, 166–170.

    Article  CAS  Google Scholar 

  • Hall, J. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany, 53(366), 1–11.

    Article  CAS  Google Scholar 

  • Han, D., Xiong, S., Tu, S., Liu, J., & Chen, C. (2015). Interactive effects of selenium and arsenic on growth, antioxidant system, arsenic and selenium species of Nicotiana tabacum L. Environmental and Experimental Botany, 117, 12–19.

    Article  CAS  Google Scholar 

  • Hasanuzzaman, M., & Fujita, M. (2013). Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology, 22(3), 584–596.

    Article  CAS  Google Scholar 

  • He, J., Ren, Y., Chen, X., & Chen, H. (2014). Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicology and Environmental Safety, 108, 114–119.

    Article  CAS  Google Scholar 

  • Heckathorn, S. A., Mueller, J. K., LaGuidice, S., Zhu, B., Barrett, T., Blair, B., et al. (2004). Chloroplast small heat-shock proteins protect photosynthesis during heavy metal stress. American Journal of Botany, 91(9), 1312–1318.

    Article  CAS  Google Scholar 

  • Herath, I., Iqbal, M. C. M., Al-Wabel, M. I., Abduljabbar, A., Ahmad, M., Usman, A. R. A., et al. (2017). Bioenergy-derived waste biochar for reducing mobility, bioavailability, and phytotoxicity of chromium in anthropized tannery soil. Journal of Soils and Sediments, 17(3), 731–740. doi:10.1007/s11368-015-1332-y.

    Article  CAS  Google Scholar 

  • Herath, I., Kumarathilaka, P., Navaratne, A., Rajakaruna, N., & Vithanage, M. (2015). Immobilization and phytotoxicity reduction of heavy metals in serpentine soil using biochar. Journal of Soils and Sediments, 15(1), 126–138. doi:10.1007/s11368-014-0967-4.

    Article  CAS  Google Scholar 

  • Hsu, Y., & Kao, C. (2003). Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant, Cell and Environment, 26(6), 867–874.

    Article  CAS  Google Scholar 

  • Hsu, Y. T., & Kao, C. H. (2005). Abscisic acid accumulation and cadmium tolerance in rice seedlings. Physiologia Plantarum, 124(1), 71–80.

    Article  CAS  Google Scholar 

  • Hu, Y., Liu, X., Bai, J., Shih, K., Zeng, E. Y., & Cheng, H. (2013). Assessing heavy metal pollution in the surface soils of a region that had undergone three decades of intense industrialization and urbanization. Environmental Science and Pollution Research, 20(9), 6150–6159.

    Article  CAS  Google Scholar 

  • Imran, M. A., Chaudhry, M., Khan, R., Ali, Z., & Mahmood, T. (2013). Toxicity of arsenic (As) on seed germination of sunflower (Helianthus annuus L.). International Journal of Physical Sciences, 8(17), 840–847.

    Article  CAS  Google Scholar 

  • Inyang, M., Gao, B., Yao, Y., Xue, Y., Zimmerman, A. R., Pullammanappallil, P., et al. (2012). Removal of heavy metals from aqueous solution by biochars derived from anaerobically digested biomass. Bioresource Technology, 110, 50–56.

    Article  CAS  Google Scholar 

  • Iqbal, N., Nazar, R., & Umar, S. (2016). Evaluating the importance of proline in cadmium tolerance and its interaction with phytohormones. In N. Iqbal, R. Nazar & N. A. Khan (Eds.), Osmolytes and plants acclimation to changing environment: Emerging omics technologies (pp. 129–153). Berlin: Springer.

  • Iqbal, M. Z., Shafiq, M., & Athar, M. (2014). Phytotoxic effects of mercury on seed germination and seedling growth of Albizia lebbeck (L.) Benth. (Leguminosae). Advances in Environmental Research, 3, 207–216.

    Article  Google Scholar 

  • Irfan, M., Ahmad, A., & Hayat, S. (2014). Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea. Saudi Journal of Biological Sciences, 21(2), 125–131.

    Article  CAS  Google Scholar 

  • Jackson, S. P., & Durocher, D. (2013). Regulation of DNA damage responses by ubiquitin and SUMO. Molecular Cell, 49(5), 795–807.

    Article  CAS  Google Scholar 

  • Jiang, M., & Zhang, J. (2002). Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. Journal of Experimental Botany, 53(379), 2401–2410.

    Article  CAS  Google Scholar 

  • Kalai, T., Khamassi, K., Teixeira da Silva, J. A., Gouia, H., & Bettaieb Ben-Kaab, L. (2014). Cadmium and copper stress affect seedling growth and enzymatic activities in germinating barley seeds. Archives of Agronomy and Soil Science, 60(6), 765–783.

    Article  CAS  Google Scholar 

  • Kang, J.-L., Zeng, Z.-J., & Liu, Y.-P. (2009). Effects of lead (Pb~(2+)) stress on seed germination and seedling growth of wheat. Guangxi Agricultural Sciences, 2, 009.

    Google Scholar 

  • Karmous, I., Bellani, L. M., Chaoui, A., El Ferjani, E., & Muccifora, S. (2015). Effects of copper on reserve mobilization in embryo of Phaseolus vulgaris L. Environmental Science and Pollution Research, 22(13), 10159–10165.

    Article  CAS  Google Scholar 

  • Karmous, I., Chaoui, A., Jaouani, K., Sheehan, D., El Ferjani, E., Scoccianti, V., et al. (2014a). Role of the ubiquitin-proteasome pathway and some peptidases during seed germination and copper stress in bean cotyledons. Plant Physiology and Biochemistry, 76, 77–85.

    Article  CAS  Google Scholar 

  • Karmous, I., Jaouani, K., El Ferjani, E., & Chaoui, A. (2014b). Responses of proteolytic enzymes in embryonic axes of germinating bean seeds under copper stress. Biological Trace Element Research, 160(1), 108–115.

    Article  CAS  Google Scholar 

  • Karmous, I., Khadija, J., Chaoui, A., & El Ferjani, E. (2012). Proteolytic activities in Phaseolus vulgaris cotyledons under copper stress. Physiology and Molecular Biology of Plants, 18(4), 337–343.

    Article  CAS  Google Scholar 

  • Kaul, S., Sharma, S., & Mehta, I. (2008). Free radical scavenging potential of l-proline: Evidence from in vitro assays. Amino Acids, 34(2), 315–320.

    Article  CAS  Google Scholar 

  • Khan, A. (1968). Inhibition of gibberellic acid-induced germination by abscisic acid and reversal by cytokinins. Plant Physiology, 43(9), 1463.

    Article  CAS  Google Scholar 

  • Khan, A., Kuek, C., Chaudhry, T., Khoo, C., & Hayes, W. (2000). Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere, 41(1), 197–207.

    Article  CAS  Google Scholar 

  • Kim, S., Lee, S., & Lee, I. (2012). Alteration of phytotoxicity and oxidant stress potential by metal oxide nanoparticles in Cucumis sativus. Water, Air, and Soil Pollution, 223(5), 2799–2806.

    Article  CAS  Google Scholar 

  • Komatsu, S., Abbasi, F., Kobori, E., Fujisawa, Y., Kato, H., & Iwasaki, Y. (2005). Proteomic analysis of rice embryo: An approach for investigating Gα protein-regulated proteins. Proteomics, 5(15), 3932–3941.

    Article  CAS  Google Scholar 

  • Koornneef, M., Reuling, G., & Karssen, C. (1984). The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiologia Plantarum, 61(3), 377–383.

    Article  CAS  Google Scholar 

  • Kranner, I., & Colville, L. (2011). Metals and seeds: Biochemical and molecular implications and their significance for seed germination. Environmental and Experimental Botany, 72(1), 93–105.

    Article  CAS  Google Scholar 

  • Kriz, A. L. (1989). Characterization of embryo globulins encoded by the maize Glb genes. Biochemical Genetics, 27(3–4), 239–251.

    Article  CAS  Google Scholar 

  • Kumar, P. N., Dushenkov, V., Motto, H., & Raskin, I. (1995). Phytoextraction: The use of plants to remove heavy metals from soils. Environmental Science and Technology, 29(5), 1232–1238.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Küpper, H., Küpper, F., & Spiller, M. (1996). Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. Journal of Experimental Botany, 47(2), 259–266.

    Article  Google Scholar 

  • Kuriakose, S. V., & Prasad, M. (2008). Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regulation, 54(2), 143–156.

    Article  CAS  Google Scholar 

  • Labra, M., Gianazza, E., Waitt, R., Eberini, I., Sozzi, A., Regondi, S., et al. (2006). Zea mays L. protein changes in response to potassium dichromate treatments. Chemosphere, 62(8), 1234–1244.

    Article  CAS  Google Scholar 

  • Lacerda, L. (1997). Global mercury emissions from gold and silver mining. Water, Air, and Soil Pollution, 97(3–4), 209–221.

    CAS  Google Scholar 

  • Li, C.-X., Feng, S.-L., Yun, S., Jiang, L.-N., Lu, X.-Y., & Hou, X.-L. (2007). Effects of arsenic on seed germination and physiological activities of wheat seedlings. Journal of Environmental Sciences, 19(6), 725–732.

    Article  CAS  Google Scholar 

  • Lin, T.-Y., Wei, C.-C., Huang, C.-W., Chang, C.-H., Hsu, F.-L., & Liao, V. H.-C. (2016). Both phosphorus fertilizers and indigenous bacteria enhance arsenic release into groundwater in the arsenic-contaminated aquifers. Journal of Agricultural and Food Chemistry, 64(11), 2214–2222.

  • Liu, J., Zhang, Y., Shi, P., & Chai, T. (2012). Effect of cadmium on seed germination and antioxidative enzymes activities in cotyledon of Solanum nigrum L. Journal of Agro-Environment Science, 31(5), 880–884.

    CAS  Google Scholar 

  • Mahdieh, S., Ghaderian, S. M., & Karimi, N. (2013). Effect of arsenic on germination, photosynthesis and growth parameters of two winter wheat varieties in Iran. Journal of Plant Nutrition, 36(4), 651–664.

    Article  CAS  Google Scholar 

  • Maheshwari, R., & Dubey, R. S. (2008). Inhibition of ribonuclease and protease activities in germinating rice seeds exposed to nickel. Acta Physiologiae Plantarum, 30(6), 863–872.

    Article  CAS  Google Scholar 

  • Maheshwari, R., & Dubey, R. (2009). Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regulation, 59(1), 37–49.

    Article  CAS  Google Scholar 

  • Mahmood, T., Islam, K., & Muhammad, S. (2007). Toxic effects of heavy metals on early growth and tolerance of cereal crops. Pakistan Journal of Botany, 39(2), 451.

    Google Scholar 

  • Malik, J. A., Goel, S., Kaur, N., Sharma, S., Singh, I., & Nayyar, H. (2012). Selenium antagonises the toxic effects of arsenic on mungbean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environmental and Experimental Botany, 77, 242–248.

    Article  CAS  Google Scholar 

  • Mazhoudi, S., Chaoui, A., Ghorbal, M. H., & El Ferjani, E. (1997). Response of antioxidant enzymes to excess copper in tomato (Lycopersicon esculentum, Mill.). Plant Science, 127(2), 129–137.

    Article  CAS  Google Scholar 

  • Mishra, S., & Dubey, R. S. (2005). Heavy metal toxicity induced alterations in photosynthetic metabolism in plants. In M. Pessarakli (Ed.), Handbook of phytosynthesis. Tucson: CRC Press.

    Google Scholar 

  • Mishra, S., & Dubey, R. S. (2006). Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: Role of proline as enzyme protectant. Journal of Plant Physiology, 163(9), 927–936.

    Article  CAS  Google Scholar 

  • Mishra, S., Jha, A., & Dubey, R. (2011). Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma, 248(3), 565–577.

    Article  CAS  Google Scholar 

  • Mohamed, A. A., Castagna, A., Ranieri, A., & di Toppi, L. S. (2012). Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiology and Biochemistry, 57, 15–22.

    Article  CAS  Google Scholar 

  • Muhammad, Z. I., Maria, K. S., Mohammad, A., Muhammad, S., Zia-Ur-Rehman, F., & Muhammad, K. (2015). Effect of mercury on seed germination and seedling growth of Mungbean (Vigna radiata (L.) Wilczek). Journal of Applied Sciences and Environmental Management, 19(2), 191–199.

    Article  CAS  Google Scholar 

  • Nagajyoti, P. C., Lee, K. D., & Sreekanth, T. V. M. (2010). Heavy metals, occurrence and toxicity for plants: A review. Environmental Chemistry Letters, 8(3), 199–216. doi:10.1007/s10311-010-0297-8.

    Article  CAS  Google Scholar 

  • Nambara, E., Akazawa, T., & McCourt, P. (1991). Effects of the gibberellin biosynthetic inhibitor uniconazol on mutants of Arabidopsis. Plant Physiology, 97(2), 736–738.

    Article  CAS  Google Scholar 

  • Nasr, N. (2013). Germination and seedling growth of maize (Zea mays L.) seeds in toxicity of aluminum and nickel. Merit Research Journal of Environmental Science and Toxicology, 1(5), 110–113.

    CAS  Google Scholar 

  • Neilson, S., & Rajakaruna, N. (2015). Phytoremediation of agricultural soils: Using plants to clean metal-contaminated arable land. In A. A. Ansari, S. S. Gill, R. Gill, G. R. Lanza & L. Newman (Eds.), Phytoremediation (pp. 159–168). Berlin: Springer.

  • Nicholson, F., Smith, S., Alloway, B., Carlton-Smith, C., & Chambers, B. (2003). An inventory of heavy metals inputs to agricultural soils in England and Wales. Science of the Total Environment, 311(1), 205–219.

    Article  CAS  Google Scholar 

  • Østergaard, O., Finnie, C., Laugesen, S., Roepstorff, P., & Svensson, B. (2004). Proteome analysis of barley seeds: Identification of major proteins from two-dimensional gels (pI 4–7). Proteomics, 4(8), 2437–2447.

    Article  CAS  Google Scholar 

  • Ouzounidou, G., Moustakas, M., & Eleftheriou, E. (1997). Physiological and ultrastructural effects of cadmium on wheat (Triticum aestivum L.) leaves. Archives of Environmental Contamination and Toxicology, 32(2), 154–160.

    Article  CAS  Google Scholar 

  • Park, J. H., Lamb, D., Paneerselvam, P., Choppala, G., Bolan, N., & Chung, J.-W. (2011). Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils. Journal of Hazardous Materials, 185(2–3), 549–574. doi:10.1016/j.jhazmat.2010.09.082.

    Article  CAS  Google Scholar 

  • Patnaik, A., & Mohanty, B. (2013). Toxic effect of mercury and cadmium on germination and seedling growth of Cajanus cajan L. (pigeon pea). Annals of Biological Research, 4(3), 123–126.

    CAS  Google Scholar 

  • Perfus-Barbeoch, L., Leonhardt, N., Vavasseur, A., & Forestier, C. (2002). Heavy metal toxicity: Cadmium permeates through calcium channels and disturbs the plant water status. The Plant Journal, 32(4), 539–548.

    Article  CAS  Google Scholar 

  • Prasad, M., & Strzałka, K. (1999). Impact of heavy metals on photosynthesis. In M. N. V. Prasad & J. Hagemeyer (Eds.), Heavy metal stress in plants (pp. 117–138). Berlin: Springer.

  • Prodanovic, O., Prodanovic, R., Pristov, J. B., Mitrovic, A., & Radotic, K. (2016). Effect of cadmium stress on antioxidative enzymes during the germination of Serbian spruce [Picea omorika (Pan.) Purkynĕ]. African Journal of Biotechnology, 11(52), 11377–11385.

    Google Scholar 

  • Prost, R., & Yaron, B. (2001). Use of modified clays for controlling soil environmental quality. Soil Science, 166(12), 880–895.

    Article  CAS  Google Scholar 

  • Rai, A., Tripathi, P., Dwivedi, S., Dubey, S., Shri, M., Kumar, S., et al. (2011). Arsenic tolerances in rice (Oryza sativa) have a predominant role in transcriptional regulation of a set of genes including sulphur assimilation pathway and antioxidant system. Chemosphere, 82(7), 986–995.

    Article  CAS  Google Scholar 

  • Ranki, H., Sopanen, T., & Voutilainen, R. (1990). Localization of carboxypeptidase I in germinating barley grain. Plant Physiology, 93(4), 1449–1452.

    Article  CAS  Google Scholar 

  • Rao, K. M., & Sresty, T. (2000). Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Science, 157(1), 113–128.

    Article  Google Scholar 

  • Rezaei, M., Sedghi, M., & Parmoon, G. (2013). Effect of HgCl2 on the germination of hardened rapeseed. Technical Journal of Engineering and Applied Sciences, 3(13), 1162–1166.

  • Rubio, M., Escrig, I., Martinez-Cortina, C., Lopez-Benet, F., & Sanz, A. (1994). Cadmium and nickel accumulation in rice plants. Effects on mineral nutrition and possible interactions of abscisic and gibberellic acids. Plant Growth Regulation, 14(2), 151–157.

    Article  CAS  Google Scholar 

  • Salt, D. E., Prince, R. C., Pickering, I. J., & Raskin, I. (1995). Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiology, 109(4), 1427–1433.

    Article  CAS  Google Scholar 

  • Sanal, F., Şeren, G., & Güner, U. (2014). Effects of arsenate and arsenite on germination and some physiological attributes of barley Hordeum vulgare L. Bulletin of Environmental Contamination and Toxicology, 92(4), 483–489.

    Article  CAS  Google Scholar 

  • Sánchez-Virosta, P., Espín, S., García-Fernández, A., & Eeva, T. (2015). A review on exposure and effects of arsenic in passerine birds. Science of the Total Environment, 512, 506–525.

    Article  CAS  Google Scholar 

  • Sankarganesh, K., Selvaraj, M., Baskaran, L., & Chidambaram, A. A. (2015). Chromium induced changes in Soybean (Glycine max L.) metabolism. World Scientific News, 16, 145–178.

    Google Scholar 

  • Saradhi, P. P. (1991). Proline accumulation under heavy metal stress. Journal of Plant Physiology, 138(5), 554–558.

    Article  Google Scholar 

  • Saradhi, P. P., AliaArora, S., & Prasad, K. (1995). Proline accumulates in plants exposed to UV radiation and protects them against UV-induced peroxidation. Biochemical and Biophysical Research Communications, 209(1), 1–5.

    Article  CAS  Google Scholar 

  • Saueia, C. H. R., Le Bourlegat, F. M., Mazzilli, B. P., & Fávaro, D. I. T. (2013). Availability of metals and radionuclides present in phosphogypsum and phosphate fertilizers used in Brazil. Journal of Radioanalytical and Nuclear Chemistry, 297(2), 189–195.

    Article  CAS  Google Scholar 

  • Schat, H., Sharma, S. S., & Vooijs, R. (1997). Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiologia Plantarum, 101(3), 477–482.

    Article  CAS  Google Scholar 

  • Schützendübel, A., & Polle, A. (2002). Plant responses to abiotic stresses: Heavy metal-induced oxidative stress and protection by mycorrhization. Journal of Experimental Botany, 53(372), 1351–1365.

    Google Scholar 

  • Shah, K., & Dubey, K. (1995). Effect of cadmium on RNA level as well as activity and molecular forms of ribonuclease in growing rice seedlings. Plant Physiology and Biochemistry, 33(5), 577–584.

    CAS  Google Scholar 

  • Shah, K., & Dubey, R. (1998). Cadmium elevates level of protein, amino acids and alters activity of proteolytic enzymes in germinating rice seeds. Acta Physiologiae Plantarum, 20(2), 189–196.

    Article  CAS  Google Scholar 

  • Shah, K., Kumar, R. G., Verma, S., & Dubey, R. (2001). Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Science, 161(6), 1135–1144.

    Article  CAS  Google Scholar 

  • Shakeel, S. N., Haq, N. U., Heckathorn, S., & Luthe, D. (2012). Analysis of gene sequences indicates that quantity not quality of chloroplast small HSPs improves thermotolerance in C4 and CAM plants. Plant Cell Reports, 31(10), 1943–1957.

    Article  CAS  Google Scholar 

  • Sharma, R. K., & Agrawal, M. (2005). Biological effects of heavy metals: An overview. Journal of Environmental Biology, 26(2), 301–313.

    CAS  Google Scholar 

  • Shen, G., Zhu, C., & Du, Q. Z. (2010). Genome-wide identification of PHYTOCHELATIN and PHYTOCH_SYNTH domain-containing phytochelatin family from rice. Electronic Journal of Biology, 6(3), 73–79.

    Google Scholar 

  • Sheoran, I., Singal, H., & Singh, R. (1990). Effect of cadmium and nickel on photosynthesis and the enzymes of the photosynthetic carbon reduction cycle in pigeonpea (Cajanus cajan L.). Photosynthesis Research, 23(3), 345–351.

    Article  CAS  Google Scholar 

  • Shri, M., Kumar, S., Chakrabarty, D., Trivedi, P. K., Mallick, S., Misra, P., et al. (2009). Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicology and Environmental Safety, 72(4), 1102–1110.

    Article  CAS  Google Scholar 

  • Singh, H. P., Kaur, G., Batish, D. R., & Kohli, R. K. (2011). Lead (Pb)-inhibited radicle emergence in Brassica campestris involves alterations in starch-metabolizing enzymes. Biological Trace Element Research, 144(1–3), 1295–1301.

    Article  CAS  Google Scholar 

  • Singh, D., Nath, K., & Sharma, Y. K. (2007). Response of wheat seed germination and seedling growth under copper stress. Journal of Environmental Biology, 28(2), 409.

    CAS  Google Scholar 

  • Singh, N., Singh, J., Kaur, L., Sodhi, N. S., & Gill, B. S. (2003). Morphological, thermal and rheological properties of starches from different botanical sources. Food Chemistry, 81(2), 219–231.

    Article  CAS  Google Scholar 

  • Somashekaraiah, B., Padmaja, K., & Prasad, A. (1992). Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): Involvement of lipid peroxides in chlorophyll degradation. Physiologia Plantarum, 85(1), 85–89.

    Article  CAS  Google Scholar 

  • Spurgeon, D., & Hopkin, S. (1996). Effects of variations of the organic matter content and pH of soils on the availability and toxicity of zinc to the earthworm Eisenia fetida. Pedobiologia, 40(1), 80–96.

    CAS  Google Scholar 

  • Srivastava, S., Akkarakaran, J. J., Suprasanna, P., & D’Souza, S. F. (2013). Response of adenine and pyridine metabolism during germination and early seedling growth under arsenic stress in Brassica juncea. Acta Physiologiae Plantarum, 35(4), 1081–1091.

    Article  CAS  Google Scholar 

  • Srivastava, S., & Dubey, R. (2011). Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regulation, 64(1), 1–16.

    Article  CAS  Google Scholar 

  • Srivastava, R. K., Pandey, P., Rajpoot, R., Rani, A., & Dubey, R. (2014). Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. Protoplasma, 251(5), 1047–1065.

    Article  CAS  Google Scholar 

  • Szabados, L., & Savouré, A. (2010). Proline: A multifunctional amino acid. Trends in Plant Science, 15(2), 89–97.

    Article  CAS  Google Scholar 

  • Taiz, L., & Honigman, W. A. (1976). Production of cell wall hydrolyzing enzymes by barley aleurone layers in response to gibberellic acid. Plant Physiology, 58(3), 380–386.

    Article  CAS  Google Scholar 

  • Uchimiya, M., Lima, I. M., Thomas Klasson, K., Chang, S., Wartelle, L. H., & Rodgers, J. E. (2010). Immobilization of heavy metal ions (CuII, CdII, NiII, and PbII) by broiler litter-derived biochars in water and soil. Journal of Agricultural and Food Chemistry, 58(9), 5538–5544.

    Article  CAS  Google Scholar 

  • Usman, A., Kuzyakov, Y., & Stahr, K. (2005). Effect of clay minerals on immobilization of heavy metals and microbial activity in a sewage sludge-contaminated soil (8 pp). Journal of Soils and Sediments, 5(4), 245–252.

    Article  CAS  Google Scholar 

  • Vázquez de Aldana, B., Gundel, P., Garcia Criado, B., García Ciudad, A., García Sánchez, A., & Zabalgogeazcoa, I. (2014). Germination response of endophytic Festuca rubra seeds in the presence of arsenic. Grass & Forage Science, 69(3), 462–469.

    Article  CAS  Google Scholar 

  • Waalkes, M. P. (2003). Cadmium carcinogenesis. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 533(1), 107–120.

    Article  CAS  Google Scholar 

  • Wan, M., Wang, M., Zhou, F., & Yang, L. (2013). Effects of arsenic on seed germination of mung bean and black soybean. Journal of Hubei University (Natural Science), 3, 006.

    Google Scholar 

  • Wang, J., Zhao, F.-J., Meharg, A. A., Raab, A., Feldmann, J., & McGrath, S. P. (2002). Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiology, 130(3), 1552–1561.

    Article  CAS  Google Scholar 

  • Waters, E. R., Lee, G. J., & Vierling, E. (1996). Evolution, structure and function of the small heat shock proteins in plants. Journal of Experimental Botany, 47(3), 325–338.

    Article  CAS  Google Scholar 

  • Wu, G., Kang, H., Zhang, X., Shao, H., Chu, L., & Ruan, C. (2010). A critical review on the bio-removal of hazardous heavy metals from contaminated soils: Issues, progress, eco-environmental concerns and opportunities. Journal of Hazardous Materials, 174(1), 1–8.

    Article  CAS  Google Scholar 

  • Wuana, R. A., & Okieimen, F. E. (2011). Heavy metals in contaminated soils: A review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology. doi:10.5402/2011/402647.

  • Xiang, L., Etxeberria, E., & den Ende, W. (2013). Vacuolar protein sorting mechanisms in plants. FEBS Journal, 280(4), 979–993.

    Article  CAS  Google Scholar 

  • Yan, D., Duermeyer, L., Leoveanu, C., & Nambara, E. (2014). The functions of the endosperm during seed germination. Plant and Cell Physiology, 55(9), 1521–1533.

  • Yan, H., Filardo, F., Hu, X., Zhao, X., & Fu, D. (2015). Cadmium stress alters the redox reaction and hormone balance in oilseed rape (Brassica napus L.) leaves. Environmental Science and Pollution Research, 23(4), 1–12.

  • Yang, S.-L., Lan, S.-S., & Gong, M. (2009). Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. Journal of Plant Physiology, 166(15), 1694–1699.

    Article  CAS  Google Scholar 

  • Yasur, J., & Rani, P. U. (2013). Environmental effects of nanosilver: Impact on castor seed germination, seedling growth, and plant physiology. Environmental Science and Pollution Research, 20(12), 8636–8648.

    Article  CAS  Google Scholar 

  • Yin, L., Colman, B. P., McGill, B. M., Wright, J. P., & Bernhardt, E. S. (2012). Effects of silver nanoparticle exposure on germination and early growth of eleven wetland plants. PLoS ONE, 7(10), e47674.

    Article  CAS  Google Scholar 

  • Yoshiba, Y., Kiyosue, T., Katagiri, T., Ueda, H., Mizoguchi, T., Yamaguchi-Shinozaki, K., et al. (1995). Correlation between the induction of a gene for Δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. The Plant Journal, 7(5), 751–760.

    Article  CAS  Google Scholar 

  • Zayneb, C., Bassem, K., Zeineb, K., Grubb, C. D., Noureddine, D., Hafedh, M., et al. (2015). Physiological responses of fenugreek seedlings and plants treated with cadmium. Environmental Science and Pollution Research, 22(14), 10679–10689.

    Article  CAS  Google Scholar 

  • Zeid, I. (2001). Responses of Phaseolus vulgaris chromium and cobalt treatments. Biologia Plantarum, 44(1), 111–115.

    Article  CAS  Google Scholar 

  • Zeng, F., Ali, S., Zhang, H., Ouyang, Y., Qiu, B., Wu, F., et al. (2011). The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environmental Pollution, 159(1), 84–91.

    Article  CAS  Google Scholar 

  • Zhang, Q., & Riechers, D. E. (2004). Proteomic characterization of herbicide safener-induced proteins in the coleoptile of Triticum tauschii seedlings. Proteomics, 4(7), 2058–2071.

    Article  CAS  Google Scholar 

  • Zhang, S., Zhang, H., Qin, R., Jiang, W., & Liu, D. (2009). Cadmium induction of lipid peroxidation and effects on root tip cells and antioxidant enzyme activities in Vicia faba L. Ecotoxicology, 18(7), 814–823.

    Article  CAS  Google Scholar 

  • Zhi, Y., Deng, Z., Luo, M., Ding, W., Hu, Y., Deng, J., et al. (2015). Influence of heavy metals on seed germination and early seedling growth in Eruca sativa Mill. American Journal of Plant Sciences, 6(05), 582.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Botany, Faculty of Natural Sciences, Open University of Sri Lanka, Nawala, Nugegoda, Sri Lanka

    Mihiri Seneviratne

  2. Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa

    Nishanta Rajakaruna

  3. Biological Sciences Department, California Polytechnic State University, San Luis Obispo, CA, 93407, USA

    Nishanta Rajakaruna

  4. Department of Environmental Sciences and Engineering, Government College University, Allama Iqbal Road, Faisalabad, 38000, Pakistan

    Muhammad Rizwan

  5. Department of Botany, University of Peradeniya, Peradeniya, Sri Lanka

    H. M. S. P. Madawala

  6. Korea Biochar Research Center & School of Natural Resources and Environmental Science, Kangwon National University, Chuncheon, 24341, Korea

    Yong Sik Ok

  7. Environmental Chemodynamics Project, National Institute of Fundamental Studies, Kandy, Sri Lanka

    Meththika Vithanage

  8. Office of the Dean, Faculty of Applied Sciences, University of Sri Jayewardenepura, Nugegoda, Sri Lanka

    Meththika Vithanage

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  1. Mihiri Seneviratne
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Seneviratne, M., Rajakaruna, N., Rizwan, M. et al. Heavy metal-induced oxidative stress on seed germination and seedling development: a critical review. Environ Geochem Health 41, 1813–1831 (2019). https://doi.org/10.1007/s10653-017-0005-8

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