Heavy metal stress and responses in plants

Abstract

Heavy metals such as Fe, Mn, Cu, Ni, Co, Cd, Zn, Hg and arsenic are for long being accumulated in soils through industrial waste and sewage disposal. Although some of these metals are essential micronutrients responsible for many regular processes in plants, their excess, however, can have detrimental effects and can directly influence the plant growth, metabolism, physiology and senescence. Plants have different mechanisms to fight stress, and they are responsible to maintain homeostasis of essential metals required by plants. These mechanisms also focus on prevention of plants exposure to heavy metals present in the soil or providing tolerance to the plant by detoxifying the metals. Other mechanisms are specific and are initiated when the respective stress is encountered. The first line of defense provided by a plant is to reduce the uptake of metals when stimulated with toxicity of heavy metals and includes the help offered by cellular and root exudates that restricts metals from entering the cell. Many plants have exclusive mechanisms for individual metal ions and are involved in sequestering these ions in compartments avoiding their exposure to sensitive components of the cells. As a second line of defense, other mechanisms for detoxification of these metals are introduced that chelates, transports, sequesters and detoxifies these metal ions in the plant’s vacuole. During the time of metal toxicity, oxidative stress is pronounced in the cells and production of stress-related proteins and hormones, antioxidants, signaling molecules including heat-shock proteins synthesis is initiated.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Abolghassem E, Ding Y, Farzad M, Xie Y (2018) Antioxidant response of bamboo (Indocalamus latifolius) as affected by heavy metal stress. J Elementol 23(1):341–352

    Google Scholar 

  2. Adrees M, Ali S, Rizwan M, Zia-ur-Rehman M, Ibrahim M, Abbas F, Farid M, Qayyum MF, Irshad MK (2015) Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol Environ Saf 119:186–197

    CAS  Article  Google Scholar 

  3. Adriano DC (1986) Elements in the terrestrial environment. Springer, Berlin

    Google Scholar 

  4. Ahmad P, Ozturk M, Gucel S (2012) Oxidative damage and antioxidants induced by heavy metal stress in two cultivars of mustard (Brassica juncea L.) plants. Fresenius Environ Bull 21(10):2953–2961

    CAS  Google Scholar 

  5. Aksoy A, Ozturk M (1996) Phoenix dactylifera as a biomonitor of heavy metal pollution in Turkey. J Trace Microprobe Tech 14(3):605–614

    CAS  Google Scholar 

  6. Aksoy A, Ozturk M (1997) Nerium oleander as a biomonitor of lead and other heavy metal pollution in mediterranean environments. Sci Total Environ 205:145–150

    CAS  Article  Google Scholar 

  7. Aksoy A, Celik A, Ozturk M, Tulu M (2000) Roadside plants as possible indicators of heavy metal pollution in Turkey. Chemia I Inzynieria Ekologiczna 7(11):1152–1162

    Google Scholar 

  8. Alaraidh IA, Alsahli AA, Razik ESA (2018) Alteration of antioxidant gene expression in response to heavy metal stress in Trigonella foenum-graecum L. S Afr J Bot 115:90–93

    CAS  Article  Google Scholar 

  9. Alharbi OM, Khattab RA, Ali I (2018) Health and environmental effects of persistent organic pollutants. J Mol Liq 263:442–453

    CAS  Article  Google Scholar 

  10. Ali I, Aboul-Enein HY (2002) Speciation of arsenic and chromium metal ions by reversed phase high performance liquid chromatography. Chemosphere 48(3):275–278

    CAS  Article  Google Scholar 

  11. Ali I, Aboul-Enein HY (eds) (2006) Instrumental methods in metal ion speciation. CRC Press, Boca Raton

    Google Scholar 

  12. Ali I, Jain CK (2004) Advances in arsenic speciation techniques. Int J Environ Anal Chem 84(12):947–964

    CAS  Article  Google Scholar 

  13. Ali I, Aboul-Enein HY, Gupta VK (2009) Nanochromatography and nanocapillary electrophoresis: pharmaceutical and environmental analyses. Wiley, Hoboken

    Google Scholar 

  14. Ali I, Khan TA, Asim M (2011) Removal of arsenic from water by electrocoagulation and electrodialysis techniques. Sep Purif Rev 40(1):25–42

    CAS  Article  Google Scholar 

  15. Ali I, Gupta VK, Khan TA, Asim M (2012a) Removal of arsenate from aqueous solution by electro-coagulation method using Al–Fe electrodes. Int J Electrochem Sci 7:1898–1907

    CAS  Google Scholar 

  16. Ali I, Khan TA, Asim M (2012b) Removal of arsenate from groundwater by electrocoagulation method. Environ Sci Pollut Res 19(5):1668–1676

    CAS  Article  Google Scholar 

  17. Ali I, Asim M, Khan TA (2013) Arsenite removal from water by electro-coagulation on zinc–zinc and copper–copper electrodes. Int J Environ Sci Technol 10(2):377–384

    CAS  Article  Google Scholar 

  18. Ali I, Al-Othman ZA, Alwarthan A, Asim M, Khan TA (2014) Removal of arsenic species from water by batch and column operations on bagasse fly ash. Environ Sci Pollut Res 21(5):3218–3229

    CAS  Article  Google Scholar 

  19. Ali I, AL-Othman ZA, Sanagi MM (2015) Green synthesis of iron nano-impregnated adsorbent for fast removal of fluoride from water. J Mol Liq 211:457–465

    CAS  Article  Google Scholar 

  20. Ali I, AL-Othman ZA, Alwarthan A (2016a) Molecular uptake of congo red dye from water on iron composite nano particles. J Mol Liq 224:171–176

    CAS  Article  Google Scholar 

  21. Ali I, Alothman ZA, Al-Warthan A (2016b) Sorption, kinetics and thermodynamics studies of atrazine herbicide removal from water using iron nano-composite material. Int J Environ Sci Technol 13(2):733–742

    CAS  Article  Google Scholar 

  22. Ali I, Al-Othman ZA, Al-Warthan A (2016c) Removal of secbumeton herbicide from water on composite nanoadsorbent. Desalin Water Treat 57(22):10409–10421

    CAS  Article  Google Scholar 

  23. Ali I, Al-Othman ZA, Alharbi OM (2016d) Uptake of pantoprazole drug residue from water using novel synthesized composite iron nano adsorbent. J Mol Liq 218:465–472

    CAS  Article  Google Scholar 

  24. Ali I, AL-Othman ZA, Alwarthan A (2016e) Green synthesis of functionalized iron nano particles and molecular liquid phase adsorption of ametryn from water. J Mol Liq 221:1168–1174

    CAS  Article  Google Scholar 

  25. Ali I, AL-Othman ZA, Alwarthan A (2016f) Synthesis of composite iron nano adsorbent and removal of ibuprofen drug residue from water. J Mol Liq 219:858–864

    CAS  Article  Google Scholar 

  26. Ali I, Suhail M, Basheer AA (2017a) Advanced spiral periodic classification of the elements. Chem Int 3:220–224

    Google Scholar 

  27. Ali I, Alothman ZA, Alwarthan A (2017b) Supra molecular mechanism of the removal of 17-β-estradiol endocrine disturbing pollutant from water on functionalized iron nano particles. J Mol Liq 241:123–129

    CAS  Article  Google Scholar 

  28. Ali I, Alharbi OM, Alothman ZA, Badjah AY, Alwarthan A (2018) Artificial neural network modelling of amido black dye sorption on iron composite nano material: kinetics and thermodynamics studies. J Mol Liq 250:1–8

    CAS  Article  Google Scholar 

  29. Ashraf M, Ozturk M, Ahmad MSA (eds) (2010a) Plant adaptation and phytoremediation. Springer, New York, p 481

    Google Scholar 

  30. Ashraf M, Ozturk M, Ahmad MSA (2010b) Toxins and their phytoremediation. In: Ashraf M, Ozturk M, Ahmad MSA (eds) Plant adaptation and phytoremediation. Springer, Dordrecht, pp 1–34

    Google Scholar 

  31. Ashraf MY, Roohi M, Iqbal Z, Ashraf M, Ozturk M, Gucel S (2015) Cadmium (Cd) and lead (Pb) induced inhibition in growth and alteration in some biochemical attributes and mineral accumulation in mung bean [Vigna radiata (L.) Wilczek]. Commun Soil Sci Plant Anal 47:405–413

    Google Scholar 

  32. Assche FV, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13(3):195–206

    Article  Google Scholar 

  33. Aydinalp C, Marinova S (2009) The effects of heavy metals on seed germination and plant growth on alfalfa plant (Medicago sativa). Bulg J Agric Sci 15(4):347–350

    Google Scholar 

  34. Aziz H, Sabir M, Ahmad HR, Aziz T, Zia-ur-Rehman M, Hakeem KR, Ozturk M (2015) Alleviating effect of calcium on nickel toxicity in rice. CLEAN-Soil Air Water 43(6):901–909

    CAS  Article  Google Scholar 

  35. Aziz MA, Ahmad HR, Corwin DL, Sabir M, Ozturk M, Hakeem KR (2016) Influence of farmyard manure on retention and availability of nickel, zinc and lead in metal-contaminated calcareous loam soils. J Environ Eng Landsc Manag 25(3):289–296

    Article  Google Scholar 

  36. Barconi D, Bernardini G, Santucci A (2011) Linking protein oxidation to environmental pollutants: redox proteome approaches. J Proteom 74(11):2324–2337

    Article  CAS  Google Scholar 

  37. Bargmann BO, Munnik T (2006) The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9:515–522

    CAS  Article  Google Scholar 

  38. Bartels S, Besteiro MAG, Lang D, Ulm R (2010) Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci 15:322–329

    CAS  Article  Google Scholar 

  39. Basheer AA (2018a) Chemical chiral pollution: impact on the society and science and need of the regulations in the 21st century. Chirality 30(4):402–406

    CAS  Article  Google Scholar 

  40. Basheer AA (2018b) New generation nano-adsorbents for the removal of emerging contaminants in water. J Mol Liq 261:583–593

    CAS  Article  Google Scholar 

  41. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65(5):1229–1240

    CAS  Article  Google Scholar 

  42. Bellomo G, Palladini G, Vairetti M (1997) Intranuclear distribution, function and fate of glutathione and glutathione-S-conjugate in living rat hepatocytes studied by fluorescence microscopy. Microsc Res Tech 36:243–252

    CAS  Article  Google Scholar 

  43. Boonyapookana B, Upatham ES, Kruatrachue M, Pokethitiyook P, Singhakaew S (2002) Phytoaccumulation and phytotoxicity of cadmium and chromium in duckweed Wolffia globosa. Int J Phytoremed 4:87–100

    CAS  Article  Google Scholar 

  44. Bouazizi H, Jouili H, Geitmann A, Ferjani EEI (2010) Copper toxicity in expanding leaves of Phaseolus vulgaris L.: antioxidant enzyme response and nutrient element uptake. Ecotoxicol Environ Saf 73:1304–1308

    CAS  Article  Google Scholar 

  45. Burakova EA, Dyachkova TP, Rukhov AV, Tugolukov EN, Galunin EV, Tkachev AG, Ali I (2018) Novel and economic method of carbon nanotubes synthesis on a nickel magnesium oxide catalyst using microwave radiation. J Mol Liq 253:340–346

    CAS  Article  Google Scholar 

  46. Celik Sh, Yucel E, Celik S, Gucel S, Ozturk M (2010) Carolina poplar (Populus x canadensis Moench) as a biomonitor of trace elements in the West Black Sea region of Turkey. J Environ Biol 31(Special Issue):225–232

    CAS  Google Scholar 

  47. Cempel M, Nikel G (2006) Nickel: a review of its sources and environmental toxicology. Pol J Environ Stud 15(3):375–382

    CAS  Google Scholar 

  48. Chakravarty B, Srivastava S (1992) Toxicity of some heavy metals in vivo and in vitro in Helianthus annuus. Mutat Res 283:287–294

    CAS  Article  Google Scholar 

  49. Chao YY, Hsu YT, Kao CH (2009) Involvement of glutathione in heat shock- and hydrogen peroxide-induced cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Soil 318(1–2):37–45

    CAS  Article  Google Scholar 

  50. Chaplen FWR (1998) Incidence and potential implications of the toxic metabolite methylglyoxal in cell culture: a review. Cytotechnology 26(3):173–183

    CAS  Article  Google Scholar 

  51. Chen CC, Dixon JB, Turner FT (1980) Iron coatings on rice roots: morphology and models of development. Soil Sci Soc Am J 44:1113–1119

    CAS  Article  Google Scholar 

  52. Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48(8):663–672

    CAS  Article  Google Scholar 

  53. Cobbett C, Goldsbroughn P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    CAS  Article  Google Scholar 

  54. Cunningham RP (1997) DNA repair: caretakers of the genome? Curr Biol 7:576–579

    Article  Google Scholar 

  55. Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755

    CAS  Article  Google Scholar 

  56. Dağhan H, Ozturk M (2015) Soil pollution in Turkey and remediation methods. In: Hakeem K, Sabir M, Ozturk M, Mermut A (eds) Soil remediation and plants: prospects and challenges. Elsevier, New York, pp 287–312

    Google Scholar 

  57. Dehghani MH, Sanaei D, Ali I, Bhatnagar A (2016) Removal of chromium (VI) from aqueous solution using treated waste newspaper as a low-cost adsorbent: kinetic modeling and isotherm studies. J Mol Liq 215:671–679

    CAS  Article  Google Scholar 

  58. Delhaize E, Ryan PR, Randall RJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.). II. Aluminum stimulated excretion of malic acid from root apices. Plant Physiol 103(3):695–702

    CAS  Article  Google Scholar 

  59. Diáz J, Bernal A, Pomar F, Merino F (2001) Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annum L.) seedlings in response to copper stress and its relation to lignification. Plant Sci 161:179

    Article  Google Scholar 

  60. DiDonato RJ Jr, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis Yellow Stripe-Like2(YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414

    CAS  Article  Google Scholar 

  61. El Msehli S, Lambert A, Cresp BF, Hopkins J, Boncompagni E, Smiti SA, Herouart D, Frendo P (2011) Crucial role of (homo)glutathione in nitrogen fixation in Medicago truncatula nodules. New Phytol 192:496–506

    Article  CAS  Google Scholar 

  62. Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:1–18

    Article  CAS  Google Scholar 

  63. Emery L, Whelan S, Hirschi KD, Pittman JK (2012) Phylogenetic analysis of Ca2+/cation antiporter genes and insights into their evolution in plants. Front Plant Sci 3:1

    CAS  Article  Google Scholar 

  64. Espartero J, Sanchez-Aguayo I, Pardo JM (1995) Molecular characterization of glyoxalase-I from a higher plant; upregulation by stress. Plant Mol Biol 29(6):1223–1233

    CAS  Article  Google Scholar 

  65. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    CAS  Article  Google Scholar 

  66. Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191

    CAS  Article  Google Scholar 

  67. Fujita M (1985) The presence of two Cd-binding components in the roots of water hyacinth cultivated in a Cd2+-containing medium. Plant Cell Physiol 26(2):295–300

    CAS  Google Scholar 

  68. Goldsbrough PB (1998) Metal tolerance in plants: the role of phytochelatins and metallothioneins. In: Terry N, Banuelos GS (eds) Phytoremediation of trace elements. CRC Press, Boca Raton, pp 221–233

    Google Scholar 

  69. Gough LP, Shacklette HT, Case AA (1979) Element concentrations toxic to plants, animals and man. U.S. Geological Survey, Washington, DC: 1466

  70. Gücel S, Ozturk M, Yucel E, Kadis C, Guvensen A (2009a) Studies on the trace metals in the soils and plants growing in the vicinity of Copper Mining Area—Lefke, Northern Cyprus. Fresenius Environ Bull 18(3):360–368

    Google Scholar 

  71. Gücel S, Kocbas F, Ozturk M (2009b) Metal bioaccumulation by barley in Mesaoria Plain alongside the Nicosia Famagusta Highway, Northern Cyprus. Fresenius Environ Bull 18(11):2034–2039

    Google Scholar 

  72. Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198

    CAS  Article  Google Scholar 

  73. Gupta VK, Ali I (2002) Encyclopedia of surface and colloid science. Marcel Dekker, New York, pp 136–166

    Google Scholar 

  74. Gupta VK, Ali I (2012) Environmental water: advances in treatment, remediation and recycling. Elsevier, Dordrecht

    Google Scholar 

  75. Gupta DK, Vandenhove H, Inouhe M (2013) Role of phytochelatins in heavy metal stress and detoxification mechanisms in plants. In: Gupta D, Corpas F, Palma J (eds) Heavy metal stress in plants. Springer, Berlin, pp 73–94

    Google Scholar 

  76. Hakeem KR, Sabir M, Ozturk M, Mermut A (2015) Soil remediation and plants: prospects and challenges. Elsevier, London, p 724

    Google Scholar 

  77. Hakeem KR, Sabir M, Ozturk M, Akhtar MS, Ibrahim FH (2017) Nitrate and nitrogen oxides: sources, health effects and their remediation. In: Gunther FA, de Voogt P (eds) Reviews of environmental contamination and toxicology, vol 242. Springer, Cham, pp 183–217

    Google Scholar 

  78. Hameed A, Qadri TN, Zaffar M, Siddiqi TO, Ozturk M, Altay V, Ahmad P (2017) Biochemical and nutritional responses of Abelmoschus esculentus L. exposed to mercury contamination. Fresenius Environ Bull 26(10):5814–5823

    CAS  Google Scholar 

  79. Haribabu TE, Sudha PN (2011) Effects of heavy metals copper and cadmium exposure on the antioxidants properties of the plant cleome gynandra. Ijpaes 1(2):80–87

    CAS  Google Scholar 

  80. Hasanuzzaman M, Nahar K, Hakeem KR, Ozturk M, Fujita M (2015) Arsenic toxicity in plants and possible remediation. In: Hakeem K, Sabir M, Ozturk M, Mermut A (eds) Soil remediation and plants: prospects and challenges. Elsevier, New York, pp 433–501

    Google Scholar 

  81. Hoque MA, Uraji M, Akhter Banu MN, Mori IC, Nakamura Y, Murata Y (2010) The effects of methylglyoxal on glutathione S-transferase from Nicotiana tabacum. Biosci Biotechnol Biochem 74(10):2124–2126

    CAS  Article  Google Scholar 

  82. Horst WJ (1983) Factors responsible for genotypic manganese tolerance in cowpea (Vigna unguiculata). Plant Soil 72(2–3):213–218

    CAS  Article  Google Scholar 

  83. Hossain MA, Hossain MZ, Fujita M (2009) Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust J Crop Sci 3(2):53–64

    CAS  Google Scholar 

  84. Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16(3):259–272

    CAS  Article  Google Scholar 

  85. Hossain MA, da Silva JAT, Fujita M (2011) Glyoxalase system and reactive oxygen species detoxification system in plant abiotic stress response and tolerance: an intimate relationship. In: Shanker AK, Venkateswarlu B (eds) Abiotic stress in plants-mechanisms and adaptations. Intech-Open Access Publisher, Rijeka, pp 235–266

    Google Scholar 

  86. Hossain MA, Piyatida P, 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 2012:1–37

    Article  CAS  Google Scholar 

  87. Huang JW, Pellet DM, Papernik LA, Kochian LV (1996) Aluminum interactions with voltage-dependent calcium transport in plasma membrane vesicles isolated from roots of aluminum-sensitive and -resistant wheat cultivars. Plant Physiol 110(2):561–569

    CAS  Article  Google Scholar 

  88. Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, Champion A, Kreis M, Zhang SQ, Hirt H, Wilson C, Heberle-Bors E et al (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308

    CAS  Article  Google Scholar 

  89. Jalmi SK, Bhagat PK, Verma D, Noryang S, Tayyeba S, Singh K, Sharma D, Sinha AK (2018) Traversing the links between heavy metal stress and plant signaling. Front Plant Sci 9:12. https://doi.org/10.3389/fpls.2018.00012

    Article  Google Scholar 

  90. Jonak C, Okresz L, Bogre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5:415–424

    CAS  Article  Google Scholar 

  91. Karplus PA, Daniels MJ, Herriot JR (1999) Atomic structure of ferredoxin-NADPH C reductase, prototype for a structurally novel flavoenzyme family. Science 251(4989):60–66

    Article  Google Scholar 

  92. Kasprzak KS (1995) Possible role of oxidative damage in metal induced carcinogenesis. Cancer Investig 13:411–430

    CAS  Article  Google Scholar 

  93. Kawachi M, Kobae Y, Mimura T, Maeshima M (2008) Deletion of a histidine-rich loop of AtMTP1, a vacuolar Zn2+/H+ antiporter of Arabidopsis thaliana, stimulates the transport activity. J Biol Chem 283:8374–8383

    CAS  Article  Google Scholar 

  94. Khan MN, Mohammad F, Mobin M, Saqib MA (2014) Tolerance of plants to abiotic stress: a role of nitric oxide and calcium. In: Khan M, Mobin M, Mohammad F, Corpas F (eds) Nitric oxide in plants: metabolism and role in stress physiology. Springer, Cham, pp 225–242

    Google Scholar 

  95. Kisa D, Elmastaş M, Öztürk L, Kayir Ö (2016) Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl Biol Chem 59(6):813–820

    CAS  Article  Google Scholar 

  96. Kopittke PM, Asher CJ, Blamey FP, Auchterlonie GJ, Guo YN, Menzies NW (2008) Localization and chemical speciation of Pb in roots of signal grass (Brachiaria decumbens) and Rhodes grass (Chloris gayana). Environ Sci Technol 42:4595–4599

    CAS  Article  Google Scholar 

  97. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945

    CAS  Article  Google Scholar 

  98. Kramer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379(6566):635–638

    CAS  Article  Google Scholar 

  99. Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33(1):35–51

    Article  CAS  Google Scholar 

  100. Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136

    CAS  Article  Google Scholar 

  101. Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C, Neumann D, Vansuyt G, Curie C, Schröder A, Krämer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051

    CAS  Article  Google Scholar 

  102. Lee CW, Choi JM, Pak CH (1996) Micronutrient toxicity in seed geranium (Pelargonium x Hortorum Bailey). J Am Soc Hortic Sci 121:77–82

    CAS  Article  Google Scholar 

  103. Lee K, Bae DW, Kim SH, Han HJ, Liu X, Park HC, Lim CO, Lee SY, Chung WS (2010) Comparative proteomic analysis of the short-term responses of rice roots and leaves to cadmium. J Plant Physiol 167(3):161–168

    CAS  Article  Google Scholar 

  104. Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79(4):83–593

    Article  Google Scholar 

  105. Li Y, Dhankher OP, Carreira L, Balish RS, Meagher RB (2005) Arsenic and mercury tolerance and cadmium sensitivity in Arabidopsis plants expressing bacterial γ-glutamylcysteine synthetase. Environ Toxicol Chem 24:1376–1386

    CAS  Article  Google Scholar 

  106. Liu H, Zhang J, Christie P, Zhang F (2008) Influence of iron plaque on uptake and accumulation of Cd by rice (Oryza sativa L.) seedlings grown in soil. Sci Total Environ 394(2–3):361–368

    CAS  Article  Google Scholar 

  107. Malar S, Vikram SS, Favas PJC, Perumal V (2014) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud Int J 55:54

    Article  CAS  Google Scholar 

  108. Malar S, Sahi SV, Favas PJC, Venkatachalam P (2015) Mercury heavy-metal-induced physiochemical changes and genotoxic alterations in water hyacinths [Eichhornia crassipes (Mart.)]. Environ Sci Pollut Res 22(6):4597–4608

    CAS  Article  Google Scholar 

  109. Manara A (2012) Plant responses to heavy metal toxicity. In: Furini A (ed) Plants and heavy metals. Springer, Dordrecht, pp 27–53

    Google Scholar 

  110. Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJM et al (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    Article  Google Scholar 

  111. Meharg AA (1994) Integrated tolerance mechanisms-constitutive and adaptive plant-response to elevated metal concentrations in the environment. Plant Cell Environ 17:989–993

    CAS  Article  Google Scholar 

  112. Meharg AA, Macnair MR (1992) Suppression of the high affinity phosphate uptake system; a mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot 43:519–524

    CAS  Article  Google Scholar 

  113. Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15(4):523–530

    CAS  Google Scholar 

  114. Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133:443–447

    CAS  Article  Google Scholar 

  115. Mills RF, Krijger GC, Baccarini PJ, Hall JL, Williams LE (2003) Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant J 35:164–176

    CAS  Article  Google Scholar 

  116. Minglin L, Yuxiu Z, Tuanyao C (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158

    Article  CAS  Google Scholar 

  117. Mittler R, Vanderauwera S, Gollery M, van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    CAS  Article  Google Scholar 

  118. Mullineaux P, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86:459–474

    CAS  Article  Google Scholar 

  119. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216

    CAS  Article  Google Scholar 

  120. National Research Council [US—Committee on Medical and Biological Effects of Environmental Pollutants] (1997) Arsenic: medical and biologic effects of environmental pollutants. National Academic Press, Washington

    Google Scholar 

  121. Navari-Izzo F (1998) Thylakoid-bound and stromal antioxidative enzymes in wheat treated with excess copper. Physiol Plant 104(4):630–638

    CAS  Article  Google Scholar 

  122. Neelima P, Reddy KJ (2002) Interaction of copper and cadmium with seedlings growth and biochemical responses in Solanum melongena. Environ Pollut Technol 1:285–290

    CAS  Google Scholar 

  123. Neumann D, zur Nieden U (2001) Silicon and heavy metal tolerance in higher plants. Phytochemistry 56:685–692

    CAS  Article  Google Scholar 

  124. Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta 1763:609–620

    CAS  Article  Google Scholar 

  125. Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148

    CAS  Article  Google Scholar 

  126. Opdenakker K, Remans T, Vangronsveld J, Cuypers A (2013) Mitogen-activated protein (MAP) kinases in plant metal stress: regulation and responses in comparison to other biotic and abiotic stresses. Int J Mol Sci 13(6):7828–7853

    Article  CAS  Google Scholar 

  127. Ortiz DF, Ruscitti T, McCue KF, Ow DW (1995) Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem 270:4721–4728

    CAS  Article  Google Scholar 

  128. Ouyang H, Vogel HJ (1998) Metal ion binding to calmodulin: NMR and fluorescence studies. Biometals 11(3):213–222

    CAS  Article  Google Scholar 

  129. Ovečka M, Takáč T (2014) Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv 32(1):73–86

    Article  CAS  Google Scholar 

  130. Ozturk M (ed) (1989) Plants and pollutants in developed and developing countries. Ege University Press, Izmir, p 759

    Google Scholar 

  131. Ozturk M, Turkan I (1993) Heavy metal accumulation by plants growing alongside the motor roads: a case study from Turkey. In: Markert B (ed) Plants as biomonitors: indicators for heavy metals in the terrestrial environment. VCH Publishers, Berlin, pp 515–522

    Google Scholar 

  132. Ozturk M, Yucel E, Gucel S, Sakcali S, Aksoy A (2008) Plants as biomonitors of trace elements pollution in soil. In: Prasad MNV (ed) Trace elements: environmental contamination, nutritional benefits and health implications. Wiley, New York, pp 723–744

    Google Scholar 

  133. Ozturk M, Memon AR, Gucel S, Sakcali MS (2012) Brassicas in Turkey and their possible role in the phytoremediation of degraded habitats. In: Anjum NA et al (eds) The plant family Brassicaceae: contribution towards phytoremediation, vol 21. Environmental Pollution Book Series. Springer, New York, pp 265–288

    Google Scholar 

  134. Ozturk M, Sakcali S, Celik A (2013a) A Biomonitor of heavy metal on ruderal habitats in Turkey—Diplotaxis tenuifolia (L.) DC. Sains Malaysiana 42(10):1371–1376

    CAS  Google Scholar 

  135. Ozturk M, Gucel S, Sakcali S, Baslar S (2013b) Nitrate and edible plants in the Mediterranean Region of Turkey: an overview. In: Umar S et al (eds) Nitrate in leafy vegetables-toxicity and safety measures. IK Intern Publ House Pvt Ltd, New Delhi, pp 17–51

    Google Scholar 

  136. Ozturk M, Ashraf M, Aksoy A, Ahmad MSA (eds) (2015a) Phytoremediation for green energy. Springer, New York

    Google Scholar 

  137. Ozturk M, Ashraf M, Aksoy A, Ahmad MSA (eds) (2015b) Plants, pollutants & remediation. Springer, New York

    Google Scholar 

  138. Ozturk M, Altay V, Karahan F (2017) Studies on trace elements in Glycyrrhiza taxa distributed in Hatay-Turkey. Int J Plant Environ 3(2):01–07

    Article  Google Scholar 

  139. Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196(4):788–795

    CAS  Article  Google Scholar 

  140. Pinto AP, Simoes I, Mota AM (2008) Cadmium impact on root exudates of sorghum and maize plants: a speciation study. J Plant Nutr 31(10):1746–1755

    CAS  Article  Google Scholar 

  141. Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8:1757–1764

    CAS  Article  Google Scholar 

  142. Pitzschke A, Djamei A, Bitton F, Hirt H (2009) A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol Plant 2:120–137

    CAS  Article  Google Scholar 

  143. Polle A, Schutzendubel A (2004) Heavy metal signaling in plants: linking cellular and organismic responses. In: Hirt H, Shinozaki K (eds) Plant responses to abiotic stress, vol 4. Topics in Current Genetics. Springer, Berlin, pp 187–215

    Google Scholar 

  144. Puig S, Thiele DJ (2002) Molecular mechanisms of copper uptake and distribution. Curr Opin Chem Biol 6:171–180

    CAS  Article  Google Scholar 

  145. Queval G, Foyer C (2012) Redox regulation of photosynthetic gene expression. Philos Trans R Soc B 367:3475–3485

    CAS  Article  Google Scholar 

  146. Rao KP, Vani G, Kumar K, Wankhede DP, Misra M, Gupta M, Sinha AK (2011) Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 506:73–82

    CAS  Article  Google Scholar 

  147. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180(2):169–181

    CAS  Article  Google Scholar 

  148. Ray S, Dutta S, Halder J, Ray M (1994) Inhibition of electron flow through complex I of the mitochondrial respiratory chain of Ehrlich ascites carcinoma cells by methylglyoxal. Biochem J 303(1):69–72

    CAS  Article  Google Scholar 

  149. Renard CMGC, Jarvis MC (1999) Acetylation and methylation of homogalacturonans. 2: effect on ion-binding properties and conformations. Carbohydr Polym 39:209–216

    CAS  Article  Google Scholar 

  150. Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858–861

    CAS  Article  Google Scholar 

  151. Richard JP (1993) Mechanism for the formation of methylglyoxal from triosephosphates. Biochem Soc Trans 21(2):549–553

    CAS  Article  Google Scholar 

  152. Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+–calmodulin in Cd 2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant Cell Environ 20(5):600–608

    CAS  Article  Google Scholar 

  153. Rizwan M, Ali S, Abbas T, Adrees M, Zia-ur-Rehman M, Ibrahim M, Abbas F, Qayyum MF, Nawaz R (2018) Residual effects of biochar on growth, photosynthesis and cadmium uptake in rice (Oryza sativa L.) under Cd stress with different water conditions. J Environ Manag 206:676–683

    CAS  Article  Google Scholar 

  154. Roelofs D, Aarts MGM, Schat H, van Straalen NM (2008) Functional ecological genomics to demonstrate general and specific responses to abiotic stress. Funct Ecol 22:8–18

    Google Scholar 

  155. Romero-Puertas MC, Palma JM, Gomez M, Del Rıo LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25(5):677–686

    CAS  Article  Google Scholar 

  156. Sabir M, Waraich EA, Hakeem KR, Ozturk M, Ahmad HR, Shahid M (2015) Phytoremediation: mechanisms and adaptations. In: Hakeem K, Sabir M, Ozturk M, Mermut A (eds) Soil remediation and plants: prospects and challenges. Elsevier, New York, pp 85–105

    Google Scholar 

  157. Saito R, Yamamoto H, Makino A, Sugimoto T, Miyake C (2011) Methylglyoxal functions as Hill oxidant and stimulates the photoreduction of O(2) at photosystem I: a symptom of plant diabetes. Plant Cell Environ 34(9):1454–1464

    CAS  Article  Google Scholar 

  158. Salt DE, Blaylock M, Kumar NPBA, Dushenkov V, Ensley D, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474

    CAS  Google Scholar 

  159. Sanita Di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41(2):105–130

    Article  Google Scholar 

  160. Saxena I, Shekhawat GS (2013) Nitric oxide (NO) in alleviation of heavy metal induced phytotoxicity and its role in protein nitration. Nitric Oxide 32:13–20

    CAS  Article  Google Scholar 

  161. Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wirén N (2004) ZmYS1 functions as a proton-coupled symporter for phyto siderophore- and nicotianamine-chelated metals. J Biol Chem 279:9091–9096

    CAS  Article  Google Scholar 

  162. Schaaf G, Schikora A, Häberle J, Vert G, Ludewig U, Briat JF, Curie C, von Wirén N (2005) A putative function for the Arabidopsis Fe-Phyto siderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant Cell Physiol 46:762–774

    CAS  Article  Google Scholar 

  163. Schmfger MEV (2001) Phytochelatins: complexation of metals and metalloids, studies on the phytochelatin synthase. Ph.D. Thesis, Munich University of Technology (TUM), Munich

  164. Shahid M, Khalid S, Abbas G, Shahid N, Nadeem M, Sabir M, Aslam M, Dumat C (2015) Heavy metal stress and crop productivity. In: Hakeem K et al (eds) Crop production and global environmental issues. Springer, Cham

    Google Scholar 

  165. Shahzad B, Tanveer M, Che Z, Rehman A, Cheema SA, Sharma A, Song H, Rehman S, Zhaorong D (2018) Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: a review. Ecotoxicol Environ Saf 147:935–944

    CAS  Article  Google Scholar 

  166. Shanker AK, Djanaguiraman M, Pathmanabhan G, Sudhagar R, Avudainayagam S (2003) Uptake and phytoaccumulation of chromium by selected tree species. In: Proceedings of the international conference on water and environment held in Bhopal, India

  167. Shao HB, Chu LY, Lu ZH, Kang CM (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4:8–14

    CAS  Article  Google Scholar 

  168. Shao HB, Chu LY, Ni FT, Guo DG, Li H, Li WX (2010) Perspective on phytoremediation for improving heavy metal contaminated soils. In: Ashraf M, Ozturk M, Ahmad M (eds) Plant adaptation and phytoremediation, vol 2. Springer, Dordrecht, pp 227–244

    Google Scholar 

  169. Sharma S, Ali I (2011) Adsorption of Rhodamine B dye from aqueous solution onto acid activated mango (Magnifera indica) leaf powder: equilibrium, kinetic and thermodynamic studies. J Toxicol Environ Health Sci 3(10):286–297

    Google Scholar 

  170. Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17(1):35–52

    CAS  Article  Google Scholar 

  171. Sharma P, Kumar A, Bhardwaj R (2016a) Plant steroidal hormone epibrassinolide regulate—heavy metal stress tolerance in Oryza sativa L. by modulating antioxidant defense expression. Environ Exp Bot 122:1–9

    Article  CAS  Google Scholar 

  172. Sharma SS, Dietz K-J, Mimura T (2016b) Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant Cell Environ 39:1112–1126. https://doi.org/10.1111/pce.12706

    CAS  Article  Google Scholar 

  173. Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45(8):542–550

    CAS  Article  Google Scholar 

  174. Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248(3):447–455

    CAS  Article  Google Scholar 

  175. Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2006) Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol 140(2):613–623

    CAS  Article  Google Scholar 

  176. Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytol 151:35–66

    CAS  Article  Google Scholar 

  177. Sobrino-Plata J, Ortega-Villasante C, Flores-Cáceres ML, Escobar C, Del Campo FF, Hernández LE (2009) Differential alterations of antioxidant defenses as bioindicators of mercury and cadmium toxicity in alfalfa. Chemosphere 77:946–954

    CAS  Article  Google Scholar 

  178. Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35(4):985–999

    CAS  Article  Google Scholar 

  179. Tangahu BV, Sheikh Abdullah SR, 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 2011:1–31

    Article  Google Scholar 

  180. Tauqeer HM, Ali S, Rizwan M, Ali Q, Saeed R, Iftikhar U, Ahmad R, Farid M, Abbasi GH (2016) Phytoremediation of heavy metals by Alternanthera bettzickiana: growth and physiological response. Ecotoxicol Environ Saf 126:138–146

    CAS  Article  Google Scholar 

  181. Tena G, Asai T, Chiu WL, Sheen J (2001) Plant mitogen activated protein kinase signaling cascades. Curr Opin Plant Biol 4:392–400

    CAS  Article  Google Scholar 

  182. Thao NP, Khan MIR, Thu NBA, Hoang XLT, Asgher M, Khan NA, Tran L-SP (2015) Role of ethylene and its cross talk with other signaling molecules in plant responses to heavy metal stress. Plant Physiol 169(1):73–84. https://doi.org/10.1104/pp.15.00663

    CAS  Article  Google Scholar 

  183. Thapa G, Sadhukhan A, Panda SK, Sahoo L (2012) Molecular mechanistic model of plant heavy metal tolerance. Biometals 25(3):489–505

    CAS  Article  Google Scholar 

  184. Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporters family in Arabidopsis with homology to NRAMP genes. Proc Natl Acad Sci USA 97:4991–4996

    CAS  Article  Google Scholar 

  185. Thomine S, Lelievre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multi specific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695

    CAS  Article  Google Scholar 

  186. Thornalley PJ (1990) The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J 269(1):1

    CAS  Article  Google Scholar 

  187. Todeschini V, Lingua G, D’Agostino G, Carniato F, Roccotiello E, Berta G (2011) Effects of high zinc concentration on poplar leaves: a morphological and biochemical study. Environ Exp Bot 71(1):50–56

    CAS  Article  Google Scholar 

  188. van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JAC, Hooykaas PJJ (1999) Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119:1047–1055

    Article  Google Scholar 

  189. Vatansever R, Ozyigit II, Filiz E (2017) Essential and beneficial trace elements in plants, and their transport in roots: a review. Appl Biochem Biotechnol 181(1):464–482

    CAS  Article  Google Scholar 

  190. Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312

    CAS  Article  Google Scholar 

  191. Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 77803:1–23

    Google Scholar 

  192. Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218

    CAS  Article  Google Scholar 

  193. Wu L, Juurlink BHJ (2002) Increased methylglyoxal and oxidative stress in hypertensive rat vascular smooth muscle cells. Hypertension 39(3):809–814

    CAS  Article  Google Scholar 

  194. Xiang C, Werner BL, Christensen EM, Oliver DJ (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564–574

    CAS  Article  Google Scholar 

  195. Xiumin C, Yikai Z, Xiuling C, Hong J, Xiaobin W (2009) Effects of exogenous nitric oxide protects tomato plants under copper stress. In: Proceedings of the 3rd international conference on bioinformatics and biomedical engineering (ICBBE’09), pp 1–7, Beijing, China

  196. 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(2):167–179

    CAS  Article  Google Scholar 

  197. Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005a) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337(1):61–67

    CAS  Article  Google Scholar 

  198. Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005b) Methylglyoxal detoxification by glyoxalase system: a survival strategy during environmental stresses. Physiol Mol Biol Plants 11(1):1–11

    CAS  Google Scholar 

  199. 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(9):1025–1035

    CAS  Article  Google Scholar 

  200. Yilmaz R, Sakcali S, Yarci C, Aksoy A, Ozturk M (2006) Use of Aesculus hippocastanum L. as a biomonitor of heavy metal pollution. Pak J Bot 38(5):1519–1527

    Google Scholar 

  201. Yuan HM, Liu WC, Jin Y, Lu YT (2013) Role of ROS and auxin in plant response to metal-mediated stress. Plant Signal Behav 8(7):e24671

    Article  Google Scholar 

  202. 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(4):7405–7432

    CAS  Article  Google Scholar 

  203. Zeid IM (2001) Responses of Phaseolus vulgaris to chromium and cobalt treatments. Biol Plant 44:111–115

    CAS  Article  Google Scholar 

  204. Zhao L, Sun YL, Cui SX (2011) Cd-induced changes in leaf proteome of the hyperaccumulator plant Phytolacca americana. Chemosphere 85(1):56–66

    CAS  Article  Google Scholar 

  205. Zhen Y, Qi JL, Wang SS, Jing S, Xu GH, Zhang MS, Miao L, Peng XX, Tian D, Yang YH (2007) Comparative proteome analysis of differentially expressed proteins induced by Al toxicity in soybean. Physiol Plant 131(4):542–554

    CAS  Article  Google Scholar 

  206. Zheng C, Jiang D, Liu F, Dai T, Liu W, Jing Q, Cao W (2009) Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot 67(1):222–227

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Authors extend sincere thanks to the Atta-ur-Rahman School of Applied Biosciences, NUST, Islamabad; Inst. of Mol. Biol./Biotech., The University of Lahore; Commission on Science and Technology for Sustainable Development in the South, Islamabad from Pakistan, and Ege University as well as Hatay Mustafa Kemal University in Turkey for their full support in this and ongoing project collaborations.

Author information

Affiliations

Authors

Corresponding author

Correspondence to M. Ozturk.

Additional information

Editorial responsibility: M. Abbaspour.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ghori, N., Ghori, T., Hayat, M.Q. et al. Heavy metal stress and responses in plants. Int. J. Environ. Sci. Technol. 16, 1807–1828 (2019). https://doi.org/10.1007/s13762-019-02215-8

Download citation

Keywords

  • Heavy metal
  • Abiotic stress
  • Plant responses
  • Oxidative stress
  • Reactive oxygen species
  • Plant hormones