Reactive Oxygen Species Metabolism and Antioxidant Defense in Plants Under Metal/Metalloid Stress

  • Jubayer Al Mahmud
  • M. H. M. Borhannuddin Bhuyan
  • Taufika Islam Anee
  • Kamrun Nahar
  • Masayuki Fujita
  • Mirza HasanuzzamanEmail author


Toxic metals/metalloids are considered leading environmental contaminants for world agriculture. Metal/metalloid pollution in the crop growing area increases their accumulation in plant as well as facilitates entry of them into the human food cycle. Recently it is gaining enormous research interest as it limits crop production by harshly altering the physiology and biochemistry of plant. Metal/metalloid-induced stress reduces rate of photosynthesis, enhances generation of reactive oxygen species (ROS), increases methylglyoxal (MG) content and consequently causes oxidative stress, which is also accountable for overall growth reduction of plant. Plants have well-structured antioxidant defense and glyoxalase system at the cellular level to minimize the metal/metalloid toxicity. Beside these, different osmolytes and chelating agents were synthesized in plant cell to work against stress. So, effective function of antioxidant defense and glyoxalase systems against ROS and MG, improvement of osmolytes synthesis and production of different chelating agents under stress condition determines the tolerance capability of plants. However, the efficiency of this system varies greatly with plant genotypes and stress intensity. In this chapter, we reviewed the recent reports on different molecular approaches of metal/metalloid-induced stress tolerance strategies.


ROS metabolism Antioxidant defense Metal chelation Phytoremediation Arsenic Cadmium 


  1. Achary VM, Jena S, Panda KK, Panda BB (2008) Aluminium induced oxidative stress and DNA damage in root cells of Allium cepa L. Ecotoxicol Environ Saf 70:300–310PubMedCrossRefGoogle Scholar
  2. Aftab T, Khan MMA, Naeem M, Idrees M, da Silva JAT, Ram M (2012) Exogenous nitric oxide donor protects Artemisia annua from oxidative stress generated by boron and aluminium toxicity. Ecotoxicol Environ Saf 80:60–68PubMedCrossRefGoogle Scholar
  3. Agami RA, Mohamed GF (2013) Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotoxicol Environ Saf 94:164–171PubMedCrossRefGoogle Scholar
  4. Ahn YO, Kim SH, Lee J, Kim HR, Lee H-S, Kwak S-S (2012) Three Brassica rapa metallothionein genes are differentially regulated under various stress conditions. Mol Biol Rep 39:2059–2067PubMedCrossRefGoogle Scholar
  5. Ali B (2017) Salicylic acid induced antioxidant system enhances the tolerence to aluminium in mung bean (Vigna radiata L. Wilczek) plants. Indian J Plant Physiol 22:178–189CrossRefGoogle Scholar
  6. Ali B, Hasan SA, Hayat S, Hayat Q, Yadav S, Fariduddin Q, Ahmad A (2008) A role for brassinosteroids in the amelioration of aluminum stress through antioxidant system in mung bean (Vigna radiate L. Wilczek). Environ Exp Bot 62:153–159CrossRefGoogle Scholar
  7. Ali B, Xu X, Gill RA, Yang S, Ali S, Tahir M, Zhou W (2014) Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind Crop Prod 52:617–626CrossRefGoogle Scholar
  8. Ali S, Bharwana SA, Rizwan M, Farid M, Kanwal S, Ali Q, Ibrahim M, Gill RA, Khan MD (2015a) Fulvic acid mediates chromium (Cr) tolerance in wheat (Triticum aestivum L.) through lowering of Cr uptake and improved antioxidant defense system. Environ Sci Pollut Res 22:10601–10609. Scholar
  9. Ali B, Gill RA, Yang S, Gill MB, Farooq MA, Liu D, Daud MK, Ali S, Zhou W (2015b) Regulation of cadmium-induced proteomic and metabolic changes by 5-aminolevulinic acid in leaves of Brassica napus L. PLoS One 10:e0123328. Scholar
  10. Amooaghaie R, Zangene-Madar F, Enteshari S (2017) Role of two-sided crosstalk between NO and H2S on improvement of mineral homeostasis and antioxidative defense in Sesamum indicum under lead stress. Ecotoxicol Environ Saf 139:210–218PubMedCrossRefGoogle Scholar
  11. Anjum NA, Hasanuzzaman M, Hossain MA, Thangavel P, Roychoudhury A, Gill SS, Rodrigo MAM, Adam V, Fujita M, Kizek R, Duarte AC, Pereira E, Ahmad I (2015) Jacks of metal/metalloid chelation trade in plants—an overview. Front Plant Sci 6:192. Scholar
  12. Anwaar SA, Ali S, Ali S, Ishaque W, Farid M, Farooq MA, Najeeb U, Abbas F, Sharif M (2015) Silicon (Si) alleviates cotton (Gossypium hirsutum L.) from zinc (Zn) toxicity stress by limiting Zn uptake and oxidative damage. Environ Sci Pollut Res 22(5):3441–3450. Scholar
  13. Asgher M, Khan MIR, Iqbal N, Masood A, Khan NA (2013) Cadmium tolerance in mustard cultivars: dependence on proline accumulation and nitrogen assimilation. J Funct Environ Bot 3:30–42CrossRefGoogle Scholar
  14. Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  15. Ashraf U, Tang X (2017) Yield and quality responses, plant metabolism and metal distribution pattern in aromatic rice under lead (Pb) toxicity. Chemosphere 176:141–155PubMedCrossRefGoogle Scholar
  16. Ashraf U, Kanu AS, Mo Z, Hussain S, Anjum SA, Khan I, Abbas RN, Tang X (2015) Lead toxicity in rice; effects, mechanisms and mitigation strategies—a mini review. Environ Sci Pollut Res 22:18318–18332CrossRefGoogle Scholar
  17. Awasthi JP, Saha B, Regon P, Sahoo S, Chowra U, Pradhan A, Roy A, Panda SK (2017) Morpho-physiological analysis of tolerance to aluminum toxicity in rice varieties of North East India. PLoS One 12:e0176357. Scholar
  18. Baruah KK, Bharali A (2015) Physiological basis of iron toxicity and its management in crops: recent advances in crop physiology. Daya Publishing House, New DelhiGoogle Scholar
  19. Becker M, Asch F (2005) Iron toxicity in rice—conditions and management concepts. J Plant Nutr Soil Sci 168:558–573CrossRefGoogle Scholar
  20. Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34. Scholar
  21. Biswas S, Mano J (2015) Lipid peroxide-derived short-chain carbonyls mediate hydrogen peroxide-induced and salt-induced programmed cell death in plants. Plant Physiol 168:885–898PubMedPubMedCentralCrossRefGoogle Scholar
  22. Boojar MM, Goodarzi F (2008) Comparative evaluation of oxidative stress status and manganese availability in plants growing on manganese mine. Ecotoxicol Environ Saf 71:692–699PubMedCrossRefGoogle Scholar
  23. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702PubMedCrossRefGoogle Scholar
  24. Cargnelutti D, Tabaldi LA, Spanevello RM, Jucoski GO, Battisti V, Redin M, Linares CEB, Dressler VL, Flores ÉMM, Nicoloso FT, Morsch VM, Schetinger MRC (2006) Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere 65:999–1006PubMedCrossRefGoogle Scholar
  25. Cervilla LM, Blasco B, Ríos JJ, Romero L, Ruiz JM (2007) Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Ann Bot 100:747–756PubMedPubMedCentralCrossRefGoogle Scholar
  26. Chandrakar V, Yadu B, Meena RK, Dubey A, Keshavkant S (2017) Arsenic-induced genotoxic responses and their amelioration by diphenylene iodonium, 24-epibrassinolide and proline in Glycine max L. Plant Physiol Biochem 112:74–86. Scholar
  27. Chen L, Wang L, Chen F, Korpelainen H, Li C (2013) The effects of exogenous putrescine on sex-specific responses of Populus cathayana to copper stress. Ecotoxicol Environ Saf 97:94–102PubMedCrossRefGoogle Scholar
  28. Chen Y, Mo HZ, Hu LB, Li YQ, Chen J, Yang LF (2014) The endogenous nitric oxide mediates selenium-induced phytotoxicity by promoting ROS generation in Brassica rapa. PLoS One 9:e110901PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chen J, Shaf M, Li S, Wang Y, Wu J, Ye Z, Peng D, Yan W, Liu D (2015) Copper induced oxidative stresses, antioxidant responses and phytoremediation potential of Moso bamboo (Phyllostachys pubescens). Sci Rep 5:13554. Scholar
  30. Chen Q, Zhang X, Liu Y, Wei J, Shen W, Shen Z, Cui J (2017) Hemin-mediated alleviation of zinc, lead and chromium toxicity is associated with elevated photosynthesis, antioxidative capacity; suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regul 81:253–264. Scholar
  31. Cherif J, Mediouni C, Ammar WB, Jemal F (2011) Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solanum lycopersicum). J Environ Sci 23:837–844CrossRefGoogle Scholar
  32. Chou T-S, Chao Y-Y, Huang W-D, Hong C-Y, Kao CH (2011) Metal/metalloid-induced oxidative stress in plants. J Plant Physiol 168:1021–1030PubMedCrossRefGoogle Scholar
  33. Choudhary SP, Kanwar M, Bhardwaj R, Yu J-Q, Tran L-SP (2012) Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS One 7:e33210. Scholar
  34. Choudhury S, Panda SK (2004) Toxic effects, oxidative stress and ultrastructural changes in moss Taxithelium nepalense (Schwaegr.) Broth. under chromium and lead phytotoxicity. Water Air Soil Pollut 167:73–90. Scholar
  35. Chowra U, Yanase E, Koyama H, Panda SK (2017) Aluminium-induced excessive ROS causes cellular damage and metabolic shifts in black gram Vigna mungo (L.) Hepper. Protoplasma 254:293–302PubMedCrossRefGoogle Scholar
  36. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182PubMedCrossRefGoogle Scholar
  37. Cui Y, Zhao N (2011) Oxidative stress and change in plant metabolism of maize (Zea mays L.) growing in contaminated soil with elemental sulfur and toxic effect of zinc. Plant Soil Environ 57:34–39CrossRefGoogle Scholar
  38. Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, Opdenakker K, Nair AR, Munters E, Artois TJ, Nawrot T, Vangronsveld J, Smeets K (2010) Cadmium stress: an oxidative challenge. Biometals 23:927–940. Scholar
  39. Dai M, Lu H, Liu W, Jia H, Hong H, Liu J, Yan C (2017) Phosphorus mediation of cadmium stress in two mangrove seedlings Avicennia marina and Kandelia obovata differing in cadmium accumulation. Ecotoxicol Environ Saf 139:272–279. Scholar
  40. de Sousa A, AbdElgawad H, Han A, Teixeira J, Matos M, Fidalgo F (2016) Oxidative metabolism of rye (Secale cereale L.) after short term exposure to aluminum, uncovering the glutathione-ascorbate redox network. Front Plant Sci 7:685. Scholar
  41. Deng C, Zhang D, Pan X, Chang F, Wang S (2013) Toxic effects of mercury on PSI and PSII activities, membrane potential and transthylakoid proton gradient in Microsorium pteropus. J Photochem Photobiol B 127:1–7PubMedCrossRefGoogle Scholar
  42. Dixon DP, Edwards R (2010) Glutathione transferases. In: The Arabidopsis book, vol 8. The American Society of Plant Biologists, AustinGoogle Scholar
  43. Dong Y, Xu L, Wang Q, Fan Z, Kong J, Bai X (2014) Effects of exogenous nitric oxide on photosynthesis, antioxidative ability, and mineral element contents of perennial ryegrass under copper stress. J Plant Interact 9:402–411CrossRefGoogle Scholar
  44. Dordas C, Chrispeels MJ, Brown PH (2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124:1349–1362PubMedPubMedCentralCrossRefGoogle Scholar
  45. Duan X, Li X, Ding F, Zhao J, Guo A, Zhang L, Yao J, Yang Y (2015) Interaction of nitric oxide and reactive oxygen species and associated regulation of root growth in wheat seedlings under zinc stress. Ecotoxicol Environ Saf 113:95–102PubMedCrossRefGoogle Scholar
  46. Dubey D, Pandey A (2011) Effect of nickel (Ni) on chlorophyll, lipid peroxidation and antioxidant enzymes activities in black gram (Vigna mungo) leaves. Int J Sci Nat 2:395–401Google Scholar
  47. Elbaz A, Wei YY, Meng Q, Zheng Q, Yang ZM (2010) Mercury-induced oxidative stress and impact on antioxidant enzymes in Chlamydomonas reinhardtii. Ecotoxicology 19:1285–1293PubMedCrossRefGoogle Scholar
  48. El-Ramady HR, Domokos-Szabolcsy E, Abdalla NA, Alshaal TA, Shalaby TA, Sztrik A, Prokisch J, Fari M (2014) Selenium and nano-selenium in agroecosystems. Environ Chem Lett 12:495–510CrossRefGoogle Scholar
  49. Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:756120. Scholar
  50. Eraslan F, Inal A, Savasturk O, Gunes A (2007) Changes in antioxidative system and membrane damage of lettuce in response to salinity and boron toxicity. Sci Hortic 114:5–10CrossRefGoogle Scholar
  51. Eser A, Aydemir T (2016) The effect of kinetin on wheat seedlings exposed to boron. Plant Physiol Biochem 108:158–164PubMedCrossRefGoogle Scholar
  52. Faize M, Burqos L, Piqueras A, Nicolas E, Barba-Espin G, Clement-Moreno MJ, Alcobendas R, Artlip T, Hernandez JA (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J Exp Bot 62:2599–2613PubMedCrossRefGoogle Scholar
  53. Farid M, Ali S, Rizwan M, Saeed R, Tauqeer HM, Sallah-Ud-Din R, Azam A, Raza N (2017) Microwave irradiation and citric acid assisted seed germination and phytoextraction of nickel (Ni) by Brassica napus L.: morpho-physiological and biochemical alterations under Ni stress. Environ Sci Pollut Res 24(26):21050–21064. Scholar
  54. Farooq MA, Islam F, Ali B, Najeeb U, Mao B, Gill RA, Yan G, Siddique KHM, Zhou W (2016) Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism. Environ Exp Bot 132:42–52CrossRefGoogle Scholar
  55. Feigl G, Lehotai N, Molnár Á, Ördög A, Rodríguez-Ruiz M, Palma JM, Corpas FJ, Erdei L, Kolbert Z (2015) Zinc induces distinct changes in the metabolism of reactive oxygen and nitrogen species (ROS and RNS) in the roots of two Brassica species with different sensitivity to zinc stress. Ann Bot 116:613–625PubMedCrossRefGoogle Scholar
  56. Fernando DR, Lynch JP (2015) Manganese phytotoxicity: new light on an old problem. Ann Bot 116:313–319PubMedPubMedCentralCrossRefGoogle Scholar
  57. Fernando DR, Marshall AT, Forster PI, Hoebee SE, Siegele R (2013) Multiple metal accumulation within a manganese-specific genus. Am J Bot 100:690–700PubMedCrossRefGoogle Scholar
  58. Fischel JS, Fischel MH, Sparks DL (2015) Advances in understanding reactivity of manganese oxides with arsenic and chromium in environmental systems. In: Feng X, Li W, Zhu M, Sparks DL (eds) Advances in the environmental biogeochemistry of manganese oxides. American Chemical Society, pp 1–27Google Scholar
  59. Flora SJS, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res 128:501–523PubMedGoogle Scholar
  60. Flora G, Gupta D, Tiwari A (2012) Toxicity of lead: a review with recent updates. Interdiscip Toxicol 5(2):47–58PubMedPubMedCentralCrossRefGoogle Scholar
  61. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100PubMedCrossRefGoogle Scholar
  62. Gajewska E, Drobik D, Wielanek M, Nalewajko JS, Gocławski J, Mazur J, Skłodowska M (2013) Alleviation of nickel toxicity in wheat (Triticum aestivum L.) seedlings by selenium supplementation. Biol Lett 50:63–76CrossRefGoogle Scholar
  63. Gao X, Wang X, Lu Y, Zhang L, Shen Y, Liang Z, Zhang D (2004) Jasmonic acid is involved in the water stress induced betaine accumulation in pear leaves. Plant Cell Environ 27:497–507. Scholar
  64. Ghasemi F, Heidari R, Jameii R, Purakbar L (2013) Responses of growth and antioxidative enzymes to various concentrations of nickel in Zea mays leaves and roots. Rom J Biol Plant Biol 58:37–49Google Scholar
  65. Giannakoula A, Moustakas M, Mylona P, Papadakis I, Yupsanis T (2008) Aluminium tolerance in maize is correlated with increased levels of mineral nutrients, carbohydrates and proline and decreased levels of lipid peroxidation and Al accumulation. J Plant Physiol 165:385–396PubMedCrossRefGoogle Scholar
  66. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedCrossRefGoogle Scholar
  67. Gill RA, Zang L, Ali B, Farooq MA, Cui P, Yang S, Ali S, Zhou W (2015) Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere 120:154–164. Scholar
  68. Gjorgieva D, Panovska TK, Ruskovska T, Bačeva T, Stafilov T (2013) Mineral nutrient imbalance, total antioxidants level and DNA damage in common bean (Phaseolus vulgaris L.) exposed to heavy metals. Physiol Mol Biol Plants 19:499–507PubMedPubMedCentralCrossRefGoogle Scholar
  69. Gomes-Junior RA, Gratão PL, Gaziola SA, Mazzafera P, Lea PJ, Azevedo RA (2007) Selenium-induced oxidative stress in coffee cell suspension cultures. Funct Plant Biol 34:449–456CrossRefGoogle Scholar
  70. González A, Lynch J (1999) Tolerance of tropical common bean genotypes to manganese toxicity: performance under different growing conditions. J Plant Nutr 22:511–525CrossRefGoogle Scholar
  71. González A, Steffen KL, Lynch JP (1998) Light and excess manganese. Implications for oxidative stress in common bean. Plant Physiol 118:493–504PubMedPubMedCentralCrossRefGoogle Scholar
  72. Gorny J, Billon G, Noiriel C, Dumoulin D, Lesven L, Madé B (2016) Chromium behavior in aquatic environments: a review. Environ Rev 24:503–516. Scholar
  73. Gunes A, Inal A, Bagci EG, Coban S, Pilbeam DJ (2007) Silicon mediates changes to some physiological and enzymatic parameters symptomatic for oxidative stress in spinach (Spinacia oleracea L.) grown under B toxicity. Sci Hortic 113:113–119CrossRefGoogle Scholar
  74. Gupta B, Pathak GC, Pandey N (2011) Induction of oxidative stress and antioxidant responses in Vigna mungo by zinc stress. Russ J Plant Physiol 58:85–91CrossRefGoogle Scholar
  75. Gururani MA, Venkatesh J, Tran LSP (2015) Regulation of photosynthesis during abiotic stress induced photoinhibition. Mol Plant 8:1304–1320PubMedCrossRefGoogle Scholar
  76. Habiba U, Ali S, Farid M, Shakoor MB, Rizwan M, Ibrahim M, Abbasi GH, Hayat T, Ali B (2015) EDTA enhanced plant growth, antioxidant defense system, and phytoextraction of copper by Brassica napus L. Environ Sci Pollut Res 22(2):1534–1544. Scholar
  77. Hamed SM, Zinta G, Klöck G, Asard H, Selim S, AbdElgawad H (2017a) Zinc-induced differential oxidative stress and antioxidant responses in Chlorella sorokiniana and Scenedesmus acuminatus. Ecotoxicol Environ Saf 140:256–263PubMedCrossRefGoogle Scholar
  78. Hamed SM, Selim S, Klöck G, AbdElgawad H (2017b) Sensitivity of two green microalgae to copper stress: growth, oxidative and antioxidants analyses. Ecotoxicol Environ Saf 144:19–25PubMedCrossRefGoogle Scholar
  79. Hasanuzzaman M, Fujita M (2012) Heavy metals in the environment: current status, toxic effects on plants and possible phytoremediation. In: Anjum NA, Pereira MA, Ahmad I, Duarte AC, Umar S, Khan NA (eds) Phytotechnologies: remediation of environmental contaminants. CRC Press, Boca Raton, pp 7–73CrossRefGoogle Scholar
  80. 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 23:584–596CrossRefGoogle Scholar
  81. Hasanuzzaman M, Anwar Hossain M, Masayuki F (2011) Selenium-induced up regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings. Biol Trace Elem Res 143:1704–1721PubMedCrossRefGoogle Scholar
  82. Hasanuzzaman M, Hossain MA, Fujita M (2012a) Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biol Trace Elem Res 149:248–261PubMedCrossRefGoogle Scholar
  83. Hasanuzzaman M, Hossain MA, Teixeira da Silva JA, Fujita M (2012b) Plant responses and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Bandi V, Shanker AK, Shanker C, Mandapaka M (eds) Crop stress and its management: perspectives and strategies. Springer, Berlin, pp 261–316CrossRefGoogle Scholar
  84. Hasanuzzaman M, Nahar K, Hossain MS, Mahmud JA, Rahman A, Inafuku M, Oku H, Fujita M (2017a) Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants. Int J Mol Sci 18:200. Scholar
  85. Hasanuzzaman M, Nahar K, Gill SS, Alharby HF, Razafindrabe BH, Fujita M (2017b) Hydrogen peroxide pretreatment mitigates cadmium-induced oxidative stress in Brassica napus L.: an intrinsic study on antioxidant defense and glyoxalase systems. Front Plant Sci 8:115. Scholar
  86. Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017c) Exogenous silicon attenuates cadmium-induced oxidative stress in Brassica napus L. by modulating AsA-GSH pathway and glyoxalase system. Front Plant Sci 8:1061. Scholar
  87. Hasanuzzaman M, Nahar K, Rahman A, Mahmud JA, Alharby HF, Fujita M (2018) Exogenous glutathione attenuates lead-induced oxidative stress in wheat by improving antioxidant defense and physiological mechanisms. J Plant Interact 13:203–212CrossRefGoogle Scholar
  88. Hattab S, Hattab S, Flores-Casseres ML, Boussetta H, Doumas P, Hernandez LE, Banni M (2016) Characterisation of lead-induced stress molecular biomarkers in Medicago sativa plants. Environ Exp Bot 123:1–12CrossRefGoogle Scholar
  89. Hauck M, Hesse V, Runge M (2002) Correlations between the Mn/Ca ratio in stem flow and epiphytic lichen abundance in a dieback-affected spruce forest of the Harz Mountains Flora. Funct Ecol Plants 197:361–369CrossRefGoogle Scholar
  90. Hauck M, Paul A, Gross S, Raubuch M (2003) Manganese toxicity in epiphytic lichens: chlorophyll degradation and interaction with iron and phosphorus. Environ Exp Bot 49:181–191CrossRefGoogle Scholar
  91. Hayat S, Khalique G, Wani AS, Alyemeni MN, Ahmad A (2014) Protection of growth in response to 28-homobrassinolide under the stress of cadmium and salinity in wheat. Int J Biol Macromol 64:130–136PubMedCrossRefGoogle Scholar
  92. He J, Wang Y, Ding H, Ge C (2016) Epibrassinolide confers zinc stress tolerance by regulating antioxidant enzyme responses, osmolytes, and hormonal balance in Solanum melongena seedlings. Braz J Bot 39(1):295–303. Scholar
  93. Hoang TH, Ju-Yong K, Sunbaek B, Kyoung-Woong K (2010) Source and fate of As in the environment. Geosyst Eng 13:35–42CrossRefGoogle Scholar
  94. Homa D, Haile E, Washe AP (2016) Determination of spatial chromium contamination of the environment around industrial zones. Int J Anal Chem 7214932.
  95. Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:872875. Scholar
  96. Houtz RL, Nable RO, Cheniae GM (1988) Evidence for effects on the in vivo activity of ribulose-biphosphate carboxylase/oxygenase during development of Mn toxicity in tobacco. Plant Physiol 86:1143–1149PubMedPubMedCentralCrossRefGoogle Scholar
  97. Inal A, Pilbeam DJ, Gunes A (2009) Silicon increases tolerance to boron toxicity and reduces oxidative damage in barley. J Plant Nutr 32:112–128CrossRefGoogle Scholar
  98. Islam F, Yasmeen T, Riaz M, Arif MS, Ali S, Raza SH (2014) Proteus mirabilis alleviates zinc toxicity by preventing oxidative stress in maize (Zea mays) plants. Ecotoxicol Environ Saf 110:143–152PubMedCrossRefGoogle Scholar
  99. Israr M, Sahi S, Datta R, Sarkar D (2006) Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere 65:591–598PubMedCrossRefGoogle Scholar
  100. Jadid N, Maziyah R, Nurcahyani DD, Mubarokah NR (2017) Growth and physiological responses of some Capsicum frutescens varieties to copper stress. AIP Conf Proc 1854:020018. Scholar
  101. Kagi JHR (1991) Overview of metallothionein. Methods Enzymol 205:613–626PubMedCrossRefGoogle Scholar
  102. Kamran MA, Musstjab SA, Eqani AS, Bibi S, Xu R-K, Amna, Monis MFH, Katsoyiannis A, Bokhari H, Chaudhary HJ (2016) Bioaccumulation of nickel by E. sativa and role of plant growth promoting rhizobacteria (PGPRs) under nickel stress. Ecotoxicol Environ Saf 26:256–263CrossRefGoogle Scholar
  103. Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plant 59:609–619CrossRefGoogle Scholar
  104. Kaur G, Kumar S, Thakur P, Malik JA, Bhandhari K, Sharma KD, Nayyar H (2011) Involvement of proline in response of chickpea (Cicer arietinum L.) to chilling stress at reproductive stage. Sci Hortic 128:174–118CrossRefGoogle Scholar
  105. Kaya C, Ashraf M (2015) Exogenous application of nitric oxide promotes growth and oxidative defense system in highly boron stressed tomato plants bearing fruit. Sci Hortic 185:43–47CrossRefGoogle Scholar
  106. Kaya C, Tuna AL, Okant AM (2010) Effect of foliar applied kinetin and indole acetic acid on maize plants grown under saline conditions. Turk J Agric For 34:529–538Google Scholar
  107. Khaliq A, Ali S, Hameed A, Farooq MA, Farid M, Shakoor MB, Mahmood K, Ishaque W, Rizwan M (2015) Silicon alleviates nickel toxicity in cotton seedlings through enhancing growth, photosynthesis and suppressing Ni uptake and oxidative stress Silicon alleviates nickel toxicity in cotton. Arch Agron Soil Sci.
  108. Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18PubMedCrossRefGoogle Scholar
  109. Kochian L, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598PubMedCrossRefGoogle Scholar
  110. Kong Z, Glick BR, Duan J, Ding S, Tian J, McConkey BJ, Wei G (2015) Effects of 1-aminocyclopropane-1-carboxylate (ACC) deaminase-overproducing Sinorhizobium meliloti on plant growth and copper tolerance of Medicago lupulina. Plant Soil 391(1–2):383–398CrossRefGoogle Scholar
  111. Kováčik J, Babula P, Klejdus B, Hedbavny J (2013) Chromium uptake and consequences for metabolism and oxidative stress in chamomile plants. J Agric Food Chem 61:7864–7873. Scholar
  112. Kumar A, Prasad MNV, Sytar O (2012a) Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere 89:1056–1065PubMedCrossRefGoogle Scholar
  113. Kumar H, Sharma D, Kumar V (2012b) Nickel-induced oxidative stress and role of antioxidant defence in Barley roots and leaves. Int J Environ Biol 2:121–128Google Scholar
  114. Kumar S, Dubey RS, Tripathi RD, Chakrabarty D, Trivedi PK (2015) Omics and biotechnology of arsenic stress and detoxification in plants: current updates and prospective. Environ Int 74:221–230PubMedCrossRefGoogle Scholar
  115. Kumar B, Smita K, Flores LC (2017) Plant mediated detoxification of mercury and lead. Arab J Chem 10:S2335–S2342CrossRefGoogle Scholar
  116. Lamhamdi M, Lafont R, Rharrabe K, Sayah F, Aarab A, Bakrim A (2016) 20-Hydroxyecdysone protects wheat seedlings (Triticum aestivum L.) against lead stress. Plant Physiol Biochem 98:64–71PubMedCrossRefGoogle Scholar
  117. Landi M, Pardossi A, Remorini D, Guidi L (2013) Antioxidant and photosynthetic response of a purple-leaved and a green-leaved cultivar of sweet basil (Ocimum basilicum) to boron excess. Environ Exp Bot 85:64–75CrossRefGoogle Scholar
  118. Lidon FC, Teixeira MG (2000) Rice tolerance to excess Mn: implications in the chloroplast lamellae and synthesis of a novel Mn protein. Plant Physiol Biochem 38:969–978CrossRefGoogle Scholar
  119. Lidon FC, Barreiro M, Ramalho J (2004) Manganese accumulation in rice: implications for photosynthetic functioning. J Plant Physiol 161:1235–1244PubMedCrossRefGoogle Scholar
  120. Mahmood Q, Ahmad R, Kwak SS, Rashid A, Anjum NA (2010) Ascorbate and glutathione: protectors of plants in oxidative stress. In: Anjum NA, Chan MT, Umar S (eds) Ascorbate glutathione pathway and stress tolerance in plants. Springer, Dordrecht, pp 209–229. Scholar
  121. Mahmud JA, Hasanuzzaman M, Nahar K, Rahman A, Fujita M (2017a) Relative tolerance of different species of Brassica to cadmium toxicity: coordinated role of antioxidant defense and glyoxalase systems. Plant Omics 10:107–117. Scholar
  122. Mahmud JA, Hasanuzzaman M, Nahar K, Rahman A, Hossain MS, Fujita M (2017b) γ-aminobutyric acid (GABA) confers chromium stress tolerance in Brassica juncea L. by modulating the antioxidant defense and glyoxalase systems. Ecotoxicology 26:675–690. Scholar
  123. Mahmud JA, Hasanuzzaman M, Nahar K, Rahman A, Hossain SM, Fujita M (2017c) Maleic acid assisted improvement of metal chelation and antioxidant metabolism confers chromium tolerance in Brassica juncea L. Ecotoxicol Environ Saf 144:216–226. Scholar
  124. Mahmud JA, Hasanuzzaman M, Nahar K, Bhuyan MHMB, Fujita M (2018) Insights into citric acid-induced cadmium tolerance and phytoremediation in Brassica juncea L.: coordinated functions of metal chelation, antioxidant defense and glyoxalase systems. Ecotoxicol Environ Saf 147:990–1001PubMedCrossRefGoogle Scholar
  125. Majerus V, Bertin P, Swenden V, Fortemps A, Lobréaux S, Lutts S (2007) Organ-dependent responses of the African rice to short-term iron toxicity: ferritin regulation and antioxidative responses. Biol Plant 51:303–312CrossRefGoogle Scholar
  126. Malar S, Sahi SV, Favas PJC, Venkatachalam P (2015) Mercury heavy-metalinduced physiochemical changes and genotoxic alterations in water hyacinths [Eichhornia crassipes (Mart.)]. Environ Sci Pollut Res 22:4597–4608CrossRefGoogle Scholar
  127. Mano J (2012) Reactive carbonyl species, their production from lipid peroxides, action in environmental stress, and the detoxification mechanism. Plant Physiol Biochem 59:90–97PubMedCrossRefGoogle Scholar
  128. Marschner H (1995) Mineral nutrition of higher plants. Academic, London, pp 411–430Google Scholar
  129. Martínez-Ruiz EB, Martínez-Jerónimo F (2016) How do toxic metals affect harmful cyanobacteria? An integrative study with a toxigenic strain of Microcystis aeruginosa exposed to nickel stress. Ecotoxicol Environ Saf 133:36–46PubMedCrossRefGoogle Scholar
  130. Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46PubMedCrossRefGoogle Scholar
  131. Mei L, Daud MK, Ullah N, Ali S, Khan M, Malik Z, Zhu SJ (2015) Pretreatment with salicylic acid and ascorbic acid significantly mitigate oxidative stress induced by copper in cotton genotypes. Environ Sci Pollut Res 22(13):9922–9931. Scholar
  132. Meriga B, Reddy BK, Rao KR, Reddy LA, Kishor PB (2004) Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 161:63–68PubMedCrossRefGoogle Scholar
  133. Michael PI, Krishnaswamy M (2011) The effect of zinc stress combined with high irradiance stress on membrane damage and antioxidative response in bean seedling. Environ Exp Bot 74:171–177CrossRefGoogle Scholar
  134. Millaleo R, Reyes-Diaz M, Alberdi M, Ivanov AG, Krol M, Huner NP (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Exp Bot 64:343–354PubMedCrossRefGoogle Scholar
  135. Miller G, Shulaev V, Mitter R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489. Scholar
  136. Min S, Wen-jing X, Xiang-yong P, Fan-hua K (2013) Effects of exogenous proline on the growth of wheat seedlings under cadmium stress. Chin J Appl Ecol 24:129–134Google Scholar
  137. Moenne A, Gonzáleza A, Sáez CA (2016) Mechanisms of metal tolerance in marine macroalgae, with emphasis on copper tolerance in Chlorophyta and Rhodophyta. Aquat Toxicol 176:30–37PubMedCrossRefGoogle Scholar
  138. Molas J (2001) Comparison of nickel toxicity and resistance strategies of cabbage plants grown in soil with addition of inorganic and organic Ni (II) complexes. Dev Plant Soil Sci 92:464–465Google Scholar
  139. Molassiotis A, Sotiropoulos T, Tanou G, Diamantidis G, Therios I (2006) Boron-induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM 9 (Malus domestica Borkh). Environ Exp Bot 56:54–62CrossRefGoogle Scholar
  140. Morina F, Jovanovic L, Mojovic M, Vidovic M, Pankovic D, Veljovic Jovanovic S (2010) Zinc-induced oxidative stress in Verbascum thapsus is caused by an accumulation of reactive oxygen species and quinhydrone in the cell wall. Physiol Plant 140(3):209–224PubMedGoogle Scholar
  141. Mostofa MG, Fujita M (2013) Salicylic acid alleviates copper toxicity in rice (Oryza sativa L.) seedlings by up-regulating antioxidative and glyoxalase systems. Ecotoxicology 22(6):959–973. Scholar
  142. Mostofa MG, Seraj ZI, Fujita M (2014) Exogenous sodium nitroprusside and glutathione alleviate copper toxicity by reducing copper uptake and oxidative damage in rice (Oryza sativa L.) seedlings. Protoplasma 251(6):1373–1386. Scholar
  143. Mostofa MG, Hossain MA, Fujita M, Tran L-SP (2015) Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep 5:11433. Scholar
  144. Mostofa MG, Hossain MA, Siddiqui MN, Fujita M, Tran LSP (2017) Phenotypical, physiological and biochemical analyses provide insight into selenium-induced phytotoxicity in rice plants. Chemosphere 178:212–223PubMedCrossRefGoogle Scholar
  145. Moulick D, Ghosh D, Santra SC (2016) Evaluation of effectiveness of seed priming with selenium in rice during germination under arsenic stress. Plant Physiol Biochem 109:571–578PubMedCrossRefGoogle Scholar
  146. Mukhopadhyay M, Das A, Subba P, Bantawal P, Sarkar B, Ghosh P, Mondal TK (2013) Structural, physiological, and biochemical profiling of tea plants under zinc stress. Biol Plant 57:474–480. Scholar
  147. Nable RO, Banuelos GS, Paull JG (1997) Boron toxicity. Plant Soil 193:181–198CrossRefGoogle Scholar
  148. Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016a) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense, and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255. Scholar
  149. Nahar K, Rahman M, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016b) Physiological and biochemical mechanisms of spermine-induced cadmium stress tolerance in mung bean (Vigna radiata L.) seedlings. Environ Sci Pollut Res 23:21206–21218. Scholar
  150. Nahar K, Hasanuzzaman M, Suzuki T, Fujita M (2017) Polyamines-induced aluminum tolerance in mung bean: a study on antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology 26:58–73PubMedCrossRefGoogle Scholar
  151. Najeeb U, Ahmad W, Zia MH, Malik Z, Zhou W (2017) Enhancing the lead phytostabilization in wetland plant Juncus effusus L. through somaclonal manipulation and EDTA enrichment. Arab J Chem 10:3310–3317CrossRefGoogle Scholar
  152. Nanda R, Agrawal V (2016) Elucidation of zinc and copper induced oxidative stress, DNA damage and activation of defence system during seed germination in Cassia angustifolia Vahl. Environ Exp Bot 125:31–41. Scholar
  153. Nasibi F, Heidari T, Asrar Z, Mansoori H (2013) Effect of arginine pre-treatment on nickel accumulation and alleviation of the oxidative stress in Hyoscyamus niger. J Soil Sci Plant Nutr 13:680–689Google Scholar
  154. Nath S, Panda P, Mishra S (2014) Arsenic stress in rice: redox consequences and regulation by iron. Plant Physiol Biochem 80:203–210PubMedCrossRefGoogle Scholar
  155. Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304. Scholar
  156. Olaleye AO, Ogunkunle AO, Singh BN, Akinbola GE, Tabi FO, Fayinminu OO, Iji ME (2009) Ratios of nutrients in lowland rice grown on two iron toxic soils in Nigeria. J Plant Nutr 32:1–17CrossRefGoogle Scholar
  157. Panda SK, Choudhury S (2005) Chromium stress in plants. Braz J Plant Physiol 17:95–102CrossRefGoogle Scholar
  158. Panda SK, Baluška F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signal Behav 4:592–597PubMedPubMedCentralCrossRefGoogle Scholar
  159. Panda SK, Choudhury S, Patra HK (2016) Heavy metal induced oxidative stress in plants: physiological and molecular perspectives. In: Tuteja N, Gill SS (eds) Abiotic stress response in plants. Wiley Online Library.
  160. Pandey C, Khan E, Panthri M, Tripathi RD, Gupta M (2016) Impact of silicon on Indian mustard (Brassica juncea L.) root traits by regulating growth parameters, cellular antioxidants and stress modulators under arsenic stress. Plant Physiol Biochem 104:216–225. Scholar
  161. Papadakis IE, Dimassi KN, Bosabadilis AM, Therios IN, Pataks A, Giannakoula A (2004) Boron toxicity in ‘Clementine’ mandarin plants grafted on two rootstocks. Plant Sci 166:539–547CrossRefGoogle Scholar
  162. Patel A, Pandey V, Patra DD (2016) Metal absorption properties of Mentha spicata grown under tannery sludge amended soil-its effect on antioxidant system and oil quality. Chemosphere 147:67–73PubMedCrossRefGoogle Scholar
  163. Pontigo S, Godoy K, Jiménez H, Gutiérrez-Moraga A, Mora ML, Cartes P (2017) Silicon-mediated alleviation of aluminum toxicity by modulation of Al/Si uptake and antioxidant performance in ryegrass plants. Front Plant Sci 8:642PubMedPubMedCentralCrossRefGoogle Scholar
  164. Poonam S, Kaur H, Geetika S (2013) Effect of jasmonic acid on photosynthetic pigments and stress markers in Cajanus cajan (L.) Millsp. seedlings under copper stress. Am J Plant Sci 4:817CrossRefGoogle Scholar
  165. Pramanick P, Chakraborty A, Raychaudhuri SS (2017) Phenotypic and biochemical alterations in relation to MT2 gene expression in Plantago ovata forsk under zinc stress. Biometals 30(2):171–184. Scholar
  166. Rahman A, Mostofa MG, Alam MM, Nahar K, Hasanuzzaman M, Fujita M (2015) Calcium mitigates arsenic toxicity in rice seedlings by reducing arsenic uptake and modulating the antioxidant defense and glyoxalase systems and stress markers. BioMed Res Int 2015:340812. Scholar
  167. Rahman A, Mostofa MG, Nahar K, Hasanuzzaman M, Fujita M (2016) Exogenous calcium alleviates cadmium-induced oxidative stress in rice (Oryza sativa L.) seedlings by regulating the antioxidant defense and glyoxalase systems. Braz J Bot 39:393–407. Scholar
  168. Rajpoot R, Rani A, Srivastava RK, Pandey P, Dubey RS (2015) Terminalia arjuna bark extract alleviates nickel toxicity by suppressing its uptake and modulating antioxidative defence in rice seedlings. Protoplasma 253(6):1449–1462. Scholar
  169. Ramakrishna B, Rao SSR (2015) Foliar application of brassinosteroids alleviates adverse effects of zinc toxicity in radish (Raphanus sativus L.) plants. Protoplasma 252(2):665–677. Scholar
  170. Ramírez-Duarte WF, Kurobe T, Teh SJ (2017) Impairment of antioxidant mechanisms in Japanese Medaka (Oryzias latipes) by acute exposure to aluminum. Comp Biochem Physiol Toxicol Pharmacol 198:37–44CrossRefGoogle Scholar
  171. Reddy PS, Jogeswar G, Rasineni GK, Maheswari M, Reddy AR, Varshney RK, Kishor PK (2015) Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol Biochem 94:104–113PubMedCrossRefGoogle Scholar
  172. Regier N, Larras F, Bravo AG, Ungureanu VG, Amouroux D, Cosio C (2013) Mercury bioaccumulation in the aquatic plant Elodea nuttallii in the field and in microcosm: accumulation in shoots from the water might involve copper transporters. Chemosphere 90:595–602PubMedCrossRefGoogle Scholar
  173. Rehman MZU, Rizwan M, Ali S, Ok YS, Ishaque W, Saifullah, Nawaz MF, Akmal F, Waqar M (2017) Remediation of heavy metal contaminated soils by using Solanum nigrum: a review. Ecotoxicol Environ Saf 143:236–248PubMedCrossRefGoogle Scholar
  174. Reid R (2010) Can we really increase yields by making crop plants tolerant to boron toxicity? Plant Sci 178:9–11CrossRefGoogle Scholar
  175. Ren J-H, Sun H-J, Wang S-F, Luo J, Ma LQ (2014) Interactive effects of mercury and arsenic on their uptake, speciation and toxicity in rice seedling. Chemosphere 117:737–744PubMedCrossRefGoogle Scholar
  176. Rizwan M, Ali S, Abbas T, Rehman MZ, Hannan F, Keller C, Al-Wabel MI, Ok YS (2016) Cadmium minimization in wheat: a critical review. Ecotoxicol Environ Saf 130:43–53PubMedCrossRefGoogle Scholar
  177. Rizwan M, Imtiaz M, Dai Z, Mehmood S, Adeel M, Liu J, Tu S (2017) Nickel stressed responses of rice in Ni subcellular distribution, antioxidant production, and osmolyte accumulation. Environ Sci Pollut Res 24(25):20587–20598. Scholar
  178. Rojas-Lillo Y, Alberdi M, Acevedo P, Inostroza-Blancheteau C, Rengel Z, de la Luz Mora M, Reyes-Díaz M (2014) Manganese toxicity and UV-B radiation differentially influence the physiology and biochemistry of highbush blueberry (Vaccinium corymbosum) cultivars. Funct Plant Biol 41:156–167CrossRefGoogle Scholar
  179. Sáez CA, Roncarati F, Moenne A, Moody AJ, Brown MT (2015) Copper-induced intra-specific oxidative damage and antioxidant responses in strains of the brown alga Ectocarpus siliculosus with different pollution histories Claudio. Aquat Toxicol 159:81–89PubMedCrossRefGoogle Scholar
  180. Sahrawat KL (2003) Iron toxicity in wetland rice: occurrence and management through integration of genetic tolerance with plant nutrition. J Indian Soc Soil Sci 51:409–417Google Scholar
  181. Sahrawat KL (2004) Iron toxicity in wetland rice and the role of other nutrients. J Plant Nutr 27:1471–1504CrossRefGoogle Scholar
  182. Santos E, Santini JM, Paixao A, Júnior E, Lavres J, Campos M, Reis A (2017) Physiological highlights of manganese toxicity symptoms in soybean plants: Mn toxicity responses. Plant Physiol Biochem 113:6–19PubMedCrossRefGoogle Scholar
  183. Sarwar N, Imran M, Shaheen MR, Ishaque W, Kamran MA, Matloob A, Rehim A, Hussain S (2017) Phytoremediation strategies for soils contaminated with heavy metal: modifications and future perspectives. Chemosphere 171:710–721PubMedCrossRefGoogle Scholar
  184. Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144CrossRefGoogle Scholar
  185. Shahid M, Dumat C, Pourrut B, Sabir M, Pinelli E (2014a) Assessing the effect of metal speciation on lead toxicity to Vicia faba pigment contents. J Geochem Explor 144:290–297CrossRefGoogle Scholar
  186. Shahid M, Pinelli E, Pourrut B, Dumat C (2014b) Effect of organic ligands on lead-induced oxidative damage and enhanced antioxidant defense in the leaves of Vicia faba plants. J Geochem Explor 144:282–289CrossRefGoogle Scholar
  187. Shahid M, Dumat C, Pourrut B, Abbas G, Shahid N, Pinelli E (2015) Role of metal speciation in lead induced oxidative stress to Vicia faba roots. Russ J Plant Physiol 6:448–454CrossRefGoogle Scholar
  188. Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753. Scholar
  189. Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50PubMedCrossRefGoogle Scholar
  190. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:217037. Scholar
  191. Sharma P, Kumar A, Bhardwaj R (2016) Plant steroidal hormone epibrassinolide regulate—heavy metal stress tolerance in Oryza sativa L. by modulating antioxidant defense expression. Environ Exp Bot 122:1–9CrossRefGoogle Scholar
  192. Sigfridsson KGV, Bernát G, Mamedov F, Styring S (2004) Molecular interference of Cd2+ with photosystem II. Biochim Biophys Acta 1659:19–31PubMedCrossRefGoogle Scholar
  193. Singh K, Pandey SN (2011) Effect of nickel-stresses on uptake, pigments and antioxidative responses of water lettuce, Pistia stratiotes L. J Environ Biol 32:391–394PubMedGoogle Scholar
  194. Singh AL, Jat RS, Chaudhari V, Bariya H, Sharma SJ (2010) Toxicities and tolerance of mineral elements boron, cobalt, molybdenum and nickel in crop plants. Plant Stress 4:31–56Google Scholar
  195. Singh VP, Srivastava PK, Prasad SM (2013) Nitric oxide alleviates arsenic-induced toxic effects in ridged Luffa seedlings. Plant Physiol Biochem 71:155–163PubMedCrossRefGoogle Scholar
  196. Singh M, Singh VP, Dubey G, Prasad SM (2015) Exogenous proline application ameliorates toxic effects of arsenate in Solanum melongena L. seedlings. Ecotoxicol Environ Saf 117:164–173PubMedCrossRefGoogle Scholar
  197. Singh N, Marwa N, Mishra SK, Mishra J, Verma PC, Rathaur S, Singh N (2016) Brevundimonas diminuta mediated alleviation of arsenic toxicity and plant growth promotion in Oryza sativa L. Ecotoxicol Environ Saf 125:25–34PubMedCrossRefGoogle Scholar
  198. Sinh S, Saxena R (2006) Effect of iron on lipid peroxidation, and enzymatic and non-enzymatic antioxidants and bacoside-A content in medicinal plant Bacopa monnieri L. Chemosphere 62:1340–1350CrossRefGoogle Scholar
  199. Soltani E, Radjabian T, Abrishamchi P, Talei D (2016) Physiological and biochemical responses of Melissa officinalis L. to nickel stress and the protective role of salicylic acid. Arch Agron Soil Sci.
  200. Soylemezoglu G, Demir K, Inal A, Gunes A (2009) Effect of silicon on antioxidant and stomatal response of two grapevine (Vitis vinifera L.) rootstocks grown in boron toxic, saline and boron toxic-saline soil. Sci Hortic 123:240–246CrossRefGoogle Scholar
  201. Srivastava S, Dubey RS (2011) Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul 64:1–16CrossRefGoogle Scholar
  202. Srivastava S, Tripathi RD, Dwivedi UN (2004) Synthesis of phytochelatins and modulation of antioxidants in response to cadmium stress in Cuscuta reflexa—an angiospermic parasite. J Plant Physiol 161:665–674PubMedCrossRefGoogle Scholar
  203. Stoeva N, Berova M, Zlatev ZL (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Plant 49:293–296CrossRefGoogle Scholar
  204. Štolfa I, Pfeiffer TŽ, Špoljarić D, Teklić T, Lončarić Z (2015) Heavy metal-induced oxidative stress in plants: response of the antioxidative system. In: Gupta D, Palma J, Corpas F (eds) Reactive oxygen species and oxidative damage in plants under stress. Springer, Cham. Scholar
  205. Sun CL, Lu LL, Liu LJ, Liu WJ, Yu Y, Liu XX, Hu Y, Jin CW, Lin XY (2014) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol 201:1240–1250PubMedCrossRefGoogle Scholar
  206. Sundaramoorthy P, Chidambaram A, Ganesh KS, Unnikannan P, Baskaran L (2010) Chromium stress in paddy: (i) Nutrient status of paddy under chromium stress; (ii) Phytoremediation of chromium by aquatic and terrestrial weeds. C R Biol 333:597–607. Scholar
  207. Szollosi R, Varga IS, Erdei L, Mihalik E (2009) Cadmium-induced oxidative stress and antioxidative mechanisms in germinating Indian mustard (Brassica juncea L.) seeds. Ecotoxicol Environ Saf 72:1337–1342PubMedCrossRefGoogle Scholar
  208. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182PubMedCrossRefGoogle Scholar
  209. Tangahu BV, Abdullah SRS, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 2011:939161CrossRefGoogle Scholar
  210. Tewari RK, Kumar P, Sharma PN (2008) Morphology and physiology of zinc-stressed mulberry plants. J Plant Nutr Soil Sci 171:286–294CrossRefGoogle Scholar
  211. Theriault G, Michael P, Nkongolo K (2016) Comprehensive transcriptome analysis of response to nickel stress in White Birch (Betula papyrifera). PLoS One 11:e0153762. Scholar
  212. Thounaojam TC, Panda P, Choudhury S, Patra HK, Panda SK (2013) Zinc ameliorates copper-induced oxidative stress in developing rice (Oryza sativa L.) seedlings. Protoplasma 251(1):61–69PubMedCrossRefGoogle Scholar
  213. Tombuloglu H, Semizoglu N, Sakcali S, Kekec G (2012) Boron induced expression of some stress-related genes in tomato. Chemosphere 86:433–438PubMedCrossRefGoogle Scholar
  214. Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633. Scholar
  215. Van Asshe F, Clijsters H (1990) Effects of metals on enzyme activity in plant. Plant Cell Environ 13:195–206CrossRefGoogle Scholar
  216. Vatamaniuk OK, Mari S, Lu Y, Rea PA (2000) Mechanism of heavy metal ion activation of phytochelatin (PC) synthase. J Biol Chem 275:31451–31459. Scholar
  217. Venkatachalam P, Jayalakshmi N, Geetha N, Sahi SV, Sharma NC, Rene ER, Sarkar SK, Favas PJC (2017) Accumulation efficiency, genotoxicity and antioxidant defense mechanisms in medicinal plant Acalypha indica L. under lead stress. Chemosphere 171:544–553PubMedCrossRefGoogle Scholar
  218. Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372PubMedCrossRefGoogle Scholar
  219. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRefGoogle Scholar
  220. Wang YX, Wu P, Wu YR, Yan XL (2002) Molecular marker analysis of manganese toxicity tolerance in rice under greenhouse conditions. Plant Soil 238:227–233CrossRefGoogle Scholar
  221. Wang C, Zhang SH, Wang PF, Hou J, Zhang WJ, Li W (2009) The effect of excess Zn on mineral nutrition and antioxidative response in rapeseed seedlings. Chemosphere 75:1468–1476PubMedCrossRefGoogle Scholar
  222. Wani AS, Tahir I, Ahmad SS, Dar RA, Nisar S (2017) Efficacy of 24-epibrassinolide in improving the nitrogen metabolism and antioxidant system in chickpea cultivars under cadmium and/or NaCl stress. Sci Hortic 225:48–55. Scholar
  223. Weng XY, Zhao LL, Zheng CJ, Zhu JW (2013) Characteristics of the hyperaccumulator plant Phytolacca acinosa (Phytolaccaceae) in response to excess manganese. J Plant Nutr 36:1355–1365CrossRefGoogle Scholar
  224. Wu ZL, Banuelos GS, Lin ZQ, Liu Y, Yuan LX, Yin XB, Li M (2015a) Biofortification and phytoremediation of selenium in China. Front Plant Sci 6:136. Scholar
  225. Wu X, He J, Ding H, Zhu Z, Chen J, Xu S, Zha D (2015b) Modulation of zinc-induced oxidative damage in Solanum melongena by 6-benzylaminopurine involves ascorbate–glutathione cycle metabolism. Environ Exp Bot 116:1–11CrossRefGoogle Scholar
  226. Wu Z, Liu S, Zhao J, Wang F, Du Y, Zou S, Li H, Wen D, Huang Y (2017) Comparative responses to silicon and selenium in relation to antioxidant enzyme system and the glutathione-ascorbate cycle in flowering Chinese cabbage (Brassica campestris L. ssp. chinensis var. utilis) under cadmium stress. Environ Exp Bot 133:1–11CrossRefGoogle Scholar
  227. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179CrossRefGoogle Scholar
  228. Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005) Methylglyoxal detoxifcation by glyoxalase system: a survival strategy during environmental stresses. Physiol Mol Biol Plants 11:1–11Google Scholar
  229. Yadav SK, Singla-Pareek SL, Sopory SK (2008) An overview on the role of methylglyoxal and glyoxalases in plants. Drug Metabol Drug Interact 23(1–2):51–68PubMedGoogle Scholar
  230. Yan R, Gao S, Yang W, Cao M, Wang S, Chen F (2008) Nickel toxicity induced antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. cotyledons. Plant Soil Environ 54(7):294–300CrossRefGoogle Scholar
  231. Yang XE, Jin XF, Feng Y, Islam E (2005) Molecular mechanisms and genetic basis of heavy metal tolerance/hyperaccumulation in plants. J Integr Plant Biol 47:1025–1035CrossRefGoogle Scholar
  232. Yin L, Mano J, Wang S, Tsuji W, Tanaka K (2010) The involvement of lipid peroxide-derived aldehydes in aluminum toxicity of tobacco roots. Plant Physiol 152:1406–1417PubMedCrossRefGoogle Scholar
  233. Yin L, Mano JI, Tanak K, Wang S, Zhang M, Deng X, Zhang S (2017) High level of reduced glutathione contributes to detoxification of lipid peroxide derived reactive carbonyl species in transgenic Arabidopsis overexpressing glutathione reductase under aluminum stress. Physiol Plant 161:211–223PubMedCrossRefGoogle Scholar
  234. Yusuf M, Fariduddin Q, Ahmad A (2011) 28-Homobrassinolide mitigates boron induced toxicity through enhanced antioxidant system in Vigna radiata plants. Chemosphere 85:1574–1584PubMedCrossRefGoogle Scholar
  235. Yusuf M, Khan TA, Fariduddin Q (2016) Interaction of epibrassinolide and selenium ameliorates the excess copper in Brassica juncea through altered proline metabolism and antioxidants. Ecotoxicol Environ Saf 129:25–34. Scholar
  236. Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432. Scholar
  237. Zhang J, Gao X (2015) Heavy metals in surface sediments of the intertidal Laizhou Bay, Bohai Sea, China: distributions, sources and contamination assessment. Mar Pollut Bull 98:320–327PubMedCrossRefGoogle Scholar
  238. Zhang H, Hu LY, Li P, Hu KD, Jiang CX (2010) Hydrogen sulfide alleviated chromium toxicity in wheat. Biol Plant 54:743–747CrossRefGoogle Scholar
  239. Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252:911–924. Scholar
  240. Zhang T, Lu Q, Su C, Yang Y, Hu D, Xu Q (2017) Mercury induced oxidative stress, DNA damage, and activation of antioxidative system and Hsp70 induction in duckweed (Lemna minor). Ecotoxicol Environ Saf 143:46–56PubMedCrossRefGoogle Scholar
  241. Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559PubMedCrossRefGoogle Scholar
  242. Zhao X, Chen Q, Wang Y, Shen Z, Shen W, Xu X (2017) Hydrogen-rich water induces aluminum tolerance in maize seedlings by enhancing antioxidant capacities and nutrient homeostasis. Ecotoxicol Environ Saf 144:369–379PubMedCrossRefGoogle Scholar
  243. Zheng G, Lv HP, Gao S, Wang SR (2010) Effects of cadmium on growth and antioxidant responses in Glycyrrhiza uralensis seedlings. Plant Soil Environ 56:508–515CrossRefGoogle Scholar
  244. Zhou G, Xu Y, Li J, Yang L, Liu J-Y (2006) Molecular analyses of the metallothionein gene family in rice (Oryza sativa L.). J Biochem Mol Biol 39:595–606PubMedGoogle Scholar
  245. Zhou ZS, Huang SQ, Guo K, Mehta SK, Zhang PC, Yang ZM (2007) Metabolic adaptations to mercury-induced oxidative stress in roots of Medicago sativa L. J Inorg Biochem 101:1–9PubMedCrossRefGoogle Scholar
  246. Zhou B, Yao W, Wang S, Wang X, Jiang T (2014) The metallothionein gene, TaMT3, from Tamarix androssowii confers Cd2+ tolerance in Tobacco. Int J Mol Sci 15:10398–10409PubMedPubMedCentralCrossRefGoogle Scholar
  247. Zouari M, Ahmed CB, Elloumi N, Bellassoued K, Delmail D, Labrousse P, Rouina BB (2016) Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L. cv Chemlali exposed to cadmium stress. Ecotoxicol Environ Saf 128:195–205. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Jubayer Al Mahmud
    • 1
  • M. H. M. Borhannuddin Bhuyan
    • 2
    • 3
    • 4
  • Taufika Islam Anee
    • 5
  • Kamrun Nahar
    • 6
  • Masayuki Fujita
    • 2
  • Mirza Hasanuzzaman
    • 5
    Email author
  1. 1.Department of Agroforestry and Environmental Science, Faculty of AgricultureSher-e-Bangla Agricultural UniversityDhakaBangladesh
  2. 2.Laboratory of Plant Stress Responses, Department of Applied Biological Sciences, Faculty of AgricultureKagawa UniversityTakamatsuJapan
  3. 3.Bangladesh Agricultural Research InstituteJoydebpurBangladesh
  4. 4.Citrus Research Station, Bangladesh Agricultural Research Institute (BARI), JaintiapurSylhetBangladesh
  5. 5.Department of Agronomy, Faculty of AgricultureSher-e-Bangla Agricultural UniversityDhakaBangladesh
  6. 6.Department of Agricultural Botany, Faculty of AgricultureSher-e-Bangla Agricultural UniversityDhakaBangladesh

Personalised recommendations