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Oxidative Stress and Antioxidant Defence Under Metal Toxicity in Halophytes

  • Anita Kumari
  • Vinod Goyal
  • Sunita Sheokand
Chapter

Abstract

Halophytes are diverse group of plants with tolerance to high salinity due to specific mechanisms of salt uptake and tolerance. Saline areas are being affected by heavy metal pollution also due to many reasons like industrialization, etc. in the recent years. Use of halophytic species for heavy metal remediation is of significant importance as these plants are naturally present in soils characterized by excess of salts. They possess specific mechanisms for uptake, detoxification and extrusion of salts. These mechanisms could help in heavy metal remediation also. Halophytes are constitutively better equipped to cope with oxidative stress as reactive oxygen species (ROS) are overproduced when plants are exposed to high salt concentrations. Halophytes have higher antioxidant metabolism compared with glycophytes. Heavy metal stress also results in overproduction of ROS. ROS scavenging proteins are particularly critical for plants under salt and heavy metal stress to maintain redox homeostasis. Sulphur metabolism also plays a role in heavy metal detoxification. Heavy metal accumulators have increased cysteine biosynthesis induced by heavy metals. Highly reactive heavy metals such as Cr, Cu and Fe are directly involved in redox reactions and generate ROS, while the redox inactive heavy metals can induce indirect ROS through decrease in antioxidant activity. The oxidative damage caused by overproduction of ROS in heavy metal-contaminated soils of halophytes will be discussed. The antioxidant metabolism of halophytes in terms of heavy metal tolerance also will be discussed as some adaptations to these stresses are common. The role of osmolytes, phytochelatins and metallothionein in heavy metal tolerance will also be discussed.

Keywords

Antioxidants Halophytes Heavy metals Osmoprotectants Oxidative metabolism Salinity and sulphur metabolism 

References

  1. Abedi T, Pakniyat H (2010) Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus L.). Czech J Genet Plant Breed 46:27–34CrossRefGoogle Scholar
  2. Adrian-Romero, Wilson SJ, Blunden G, Bashir AK (1998) A betaines in coastal plants. Biochem Syst Ecol 26(5):535–543CrossRefGoogle Scholar
  3. Alscher RG, Erturk N, Heatrh LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341PubMedCrossRefGoogle Scholar
  4. Amjad M, Akhtar SS, Yang A, Akhtar J, Jacobsen SE (2015) Antioxidative response of Quinoa exposed to iso-osmotic, ionic and non-ionic salt stress. J Agron Crop Sci 201:452–460CrossRefGoogle Scholar
  5. Asada K (1994) Production and action of active oxygen species in photosynthetic tissues. In: Foyer CH, Mullineaux PM (eds) Causes of photo-oxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 77–104Google Scholar
  6. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639PubMedCrossRefGoogle Scholar
  7. Asada K (2000) The water-water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond Ser B Biol Sci 355:1419–1431CrossRefGoogle Scholar
  8. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedPubMedCentralCrossRefGoogle Scholar
  9. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. BioTechnol Adv 27:84–93PubMedCrossRefGoogle Scholar
  10. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  11. Ashraf M, Orooj A (2006) Salt stress effects on growth, ion accumulation and seed oil concentration in an arid zone traditional medicinal plants ajwain (Trachyspermum ammi [L.] Sprague). J Arid Environ 64:209–220CrossRefGoogle Scholar
  12. Aslund F, Beckwith J (1999) Bridge over troubled waters: sensing stress by disulfide bond formation. Cell 96:951–953CrossRefGoogle Scholar
  13. Baccouch S, Chaoui A, Ferjani EE (2001) Nickel toxicity induces oxidative damage in Zea mays root. J Plant Nutr 24:1085–1097CrossRefGoogle Scholar
  14. Banerjee S, Pramanik A, Sengupta S, Chattopadhyay D, Bhattacharyya M (2017) Distribution and source identification of heavy metal concentration in Chilika Lake, Odisha India: an assessment over salinity gradient. Curr Sci 112:87–94CrossRefGoogle Scholar
  15. Bankaji I, Sleimi N, Gomez Cadenas A, Perez Clemente RM (2016) NaCl protects against Cd and Cu-induced toxicity in the halophyte Atriplex halimus. Span J Agric Res 14:1–12CrossRefGoogle Scholar
  16. Barnes JD, Zheng Y, Lyons TM (2002) Plant resistance to ozone: the role of ascorbate. In: Omasa K, Saji H, Youssefian S, Kondo N (eds) Air pollution and plant biotechnology. Springer, Tokyo, pp 235–254CrossRefGoogle Scholar
  17. Begum MC, Islam MS, Islam M, Amin R, Parvez MS, Kabir AH (2016) Biochemical and molecular responses underlying differential arsenic tolerance in rice (Oryza sativa L.). Plant Physiol Biochem 104:266–277PubMedCrossRefGoogle Scholar
  18. Bela K, Horvátha E, Galle Á, Szabadosb L, Tari I, Csiszára J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201PubMedCrossRefGoogle Scholar
  19. Ben Amor N, Ben Hamed K, Debez A, Grignon C, Abdelly C (2005) Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity. Plant Sci 68:889–899CrossRefGoogle Scholar
  20. Bertrand M, Poirier I (2005) Photosynthetic organisms and excess of metal. Photosynthetica 43:345–353CrossRefGoogle Scholar
  21. Blindauer CA, Leszczyszyn OI (2010) Metallothioneins: unparalleled diversity in structures and functions for metal ion homeostasis and more. Nat Prod Rep 27:720–741PubMedCrossRefGoogle Scholar
  22. Boguszewska D, Grudkowska M, Zagdanska B (2010) Drought-responsive antioxidant enzymes in potato (Solanum tuberosum L.). Potato Res 53:373–382CrossRefGoogle Scholar
  23. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davis DR, Gardner SL, Gerish C, Minibayeva F (2002) The apoplastic oxidative brust in response to biotic stress in plants: a three-component system. J Exp Bot 53:1367–1376PubMedGoogle Scholar
  24. Boscaiu M, Lull C, Llinares J, Vicente O, Boira H (2013) Proline as a biochemical marker in relation to the ecology of two halophytic Juncus species. J Plant Ecol 6:177–186CrossRefGoogle Scholar
  25. Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity tolerance. J Exp Bot 65:1241–1257PubMedCrossRefGoogle Scholar
  26. Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116CrossRefGoogle Scholar
  27. Breusegem FV, Slooten L, Stassart JM, Moens T, Botterman J, Montagu MV, Inze D (1999) Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant Cell Physiol 40:515–523PubMedCrossRefGoogle Scholar
  28. Cai Y, Lin L, Cheng W, Zhang G, Wu F (2010) Genotypic dependent effect of exogenous glutathione on Cd-induced changes in cadmium and mineral uptake and accumulation in rice seedlings (Oryza sativa). Plant Soil Environ 56:516–525CrossRefGoogle Scholar
  29. Caregnato FF, Koller CE, MacFarlane GR, Moreira JCF (2008) The glutathione antioxidant system as a biomarker suite for the assessment of heavy metal exposure and effect in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull 56:1119–1127PubMedCrossRefGoogle Scholar
  30. Chai MW, Shi FC, Li RL, Liu FC, Qiu GY, Liu LM (2013) Effect of NaCl on growth and Cd accumulation of halophyte Spartina alterniflora under CdCl2 stress. South Afr J Bot 85:63–69CrossRefGoogle Scholar
  31. Chaturvedi AK, Avinash Mishra A, Tiwari V, Bhavanath Jha B (2012) Cloning and transcript analysis of type 2 metallothionein gene (SbMT-2) from extreme halophyte Salicornia brachiata and its heterologous expression in E. coli. Gene 499:280–287PubMedCrossRefGoogle Scholar
  32. Chaturvedi AK, Patel MK, Mishra A, Tiwari V, Jha B (2014) The SbMT-2 gene from a halophyte confers abiotic stress tolerance and modulates ROS scavenging in transgenic tobacco. PLoS One 9(10):e111379PubMedPubMedCentralCrossRefGoogle Scholar
  33. Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787PubMedPubMedCentralCrossRefGoogle Scholar
  34. Cherian MG, Kang YJ (2006) Metallothionein and liver cell regeneration. Exp Biol Med 231:138–144CrossRefGoogle Scholar
  35. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182PubMedCrossRefGoogle Scholar
  36. da Silva VFN (2010) Response of salt marsh plants to heavy metals in the Tagus Estuary. Thesis, Departamento de Biologia Vegetal, Faculdade de Ciências, Universidade de Lisboa, PortugalGoogle Scholar
  37. Dar MI, Naikoo MI, Ahmad Khan F, Rehman F, Green ID, Naushin F, Ansari AA (2017) An introduction to reactive oxygen species metabolism under changing climate in plants. In: MIR K, Khan NA (eds) Reactive oxygen species and antioxidant systems in plants: role and regulation under abiotic stress. Springer, Singapore.  https://doi.org/10.1007/978-981-10-5254-5_2 CrossRefGoogle Scholar
  38. Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53CrossRefGoogle Scholar
  39. Dat J, Vandenabeele S, Vranova E, van Montagu M, Inze D, van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795PubMedCrossRefGoogle Scholar
  40. Defew LH, Mair JM, Guzman HM (2005) An assessment of metal contamination in mangrove sediments and leaves from Punta Mala Bay, Pacific Panama. Mar Pollut Bull 50:547–552PubMedCrossRefGoogle Scholar
  41. Del-Rio LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272PubMedCrossRefGoogle Scholar
  42. Demidchik V (2014) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. J Exp Bot 109:212–228CrossRefGoogle Scholar
  43. Demidchik V, Cuin TA, Svistunenko D et al (2010) Arabidopsis root K+ efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123:1468–1479PubMedPubMedCentralCrossRefGoogle Scholar
  44. Demir E, Dinler BS, Ozdener Y (2013) Biochemical effects of arsenic stress in the leaves of halophyte Cakile maritima (scop.) plants under salinity. Fresenius Environ Bull 22:3465–3473Google Scholar
  45. Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad.). J Exp Bot 52:1101–1109PubMedCrossRefGoogle Scholar
  46. Dixon DP, Cummins L, Cole DJ, Edwards R (1998) Glutathione-mediated detoxification systems in plants. Curr Opin Plant Biol 1:258–266PubMedCrossRefGoogle Scholar
  47. Ellouzi H, Ben-Hamed KB, Cela J, Munné-Bosch S, Abdelly C (2011) Early effects of salt stress on the physiological and antioxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte). Physiol Plant 142:128–143PubMedPubMedCentralCrossRefGoogle Scholar
  48. Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225:1255–1264PubMedCrossRefGoogle Scholar
  49. Eyidogan F, Oz MT (2007) Effect of salinity on antioxidant responses of chickpea seedlings. Acta Physiol Plant 29:485–493CrossRefGoogle Scholar
  50. Fath A, Bethke P, Belligini V, Jones R (2002) Active oxygen and cell death in cereal aleurone cells. J Exp Bot 53:1273–1282PubMedCrossRefGoogle Scholar
  51. Fernandez O, Béthencourt L, Quero A, Sangwan RS, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417PubMedCrossRefGoogle Scholar
  52. Fini A, Brunetti C, DiFerdinando M, Ferrini F, Tattini M (2011) Stress- induced flavonoids biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 6:709–711PubMedPubMedCentralCrossRefGoogle Scholar
  53. Fitzgerald TL, Waters DL, Henry RJ (2009) Betaine aldehyde dehydrogenase in plants. Plant Biol (Stuttg) 11(2):119–130CrossRefGoogle Scholar
  54. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963PubMedCrossRefGoogle Scholar
  55. Flowers TJ, Flowers SA, Greenway H (1986) Effects of NaCl on tobacco plants. Plant Cell Environ 19:645–651CrossRefGoogle Scholar
  56. Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612CrossRefGoogle Scholar
  57. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875PubMedPubMedCentralCrossRefGoogle Scholar
  58. 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 16:2176–2191PubMedPubMedCentralCrossRefGoogle Scholar
  59. Freisinger E (2011) Structural features specific to plant metallothioneins. J Biol Inorg Chem 16:1035–1045PubMedCrossRefGoogle Scholar
  60. Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969PubMedCrossRefGoogle Scholar
  61. Gekeler W, Grill E, Winnacker EL, Zenk MH (1989) Survey of the plant kingdom for the ability to bind heavy metals through phytochelatins. Z Naturforsch 44:361–369CrossRefGoogle Scholar
  62. Ghosh S, Shawb AK, Azahar I, Adhikari S, Jana S, Roy S, Kundu A, Sherpa AR, Hossain Z (2016) Arsenate (AsV) stress response in maize (Zea mays L.). Environ Exp Bot 130:53–67CrossRefGoogle Scholar
  63. Gill SS, Tuteja N (2010) Reactive oxygen species and anti-oxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefPubMedGoogle Scholar
  64. Gill SS, Tuteja N (2011) Cadmium stress tolerance in crop plants: probing the role of sulphur. Plant Signal Behav 6:215–222PubMedCrossRefGoogle Scholar
  65. Gill SS, Anjum NA, Gill R, Yadav S, Hasanuzzaman M, Fujita M, Mishra P, Sabat SC, Tuteja N (2015) Superoxide dismutase – mentor of abiotic stress tolerance in crop plants. Environ Sci Pollut Res 22:10375–10394CrossRefGoogle Scholar
  66. Gisbert C, Gisbert C, Roc Ros A, De Haro DJ, Walker M, Pilar B, Ramón S, Juan Navarro A (2003) Plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochem Biophys Res Commun 303:440–445PubMedCrossRefGoogle Scholar
  67. Gonzalez-Mendoza D, Moreno AQ, Zapata-Perez O (2007) Coordinated responses of phytochelatin synthase and metallothionein genes in black mangrove, Avicennia germinans, exposed to cadmium and copper. Aquat Toxicol 83:306–314PubMedCrossRefGoogle Scholar
  68. Gorai M, Ennajeh M, Khemira H, Neffati M (2010) Combined effect of NaCl-salinity and hypoxia on growth, photosynthesis, water relations and solute accumulation in Phragmites australis plants. Flora 205:462–470CrossRefGoogle Scholar
  69. Gratao PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal stressed plant a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  70. Grill E, Winnacker EL, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of plants. Science 230:674–676PubMedCrossRefGoogle Scholar
  71. Guo JB, Dia XJ, Xu WZ, Ma M (2008) Overexpressing GSH1 and AsPCS1 simultaneously increases tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026PubMedCrossRefGoogle Scholar
  72. Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci 30:761–776PubMedCrossRefGoogle Scholar
  73. Halliwell B, Foyer CH (1978) Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromotography. Planta 139:9–17PubMedCrossRefGoogle Scholar
  74. Halliwell B, Gutteridge JM (1986) Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch Biochem Biophys 246:501–514PubMedCrossRefGoogle Scholar
  75. Haluskova L, Valentovicova K, Huttova J, Mistrık I, Tamas L (2009) Effect of abiotic stresses on glutathione peroxidase and glutathione S-transferase activity in barley root tips. Plant Physiol Biochem 47:1069–1074PubMedCrossRefGoogle Scholar
  76. Han RM, Lefèvre I, Ruan CJ, Qin P, Lutts S (2012) NaCl differently interferes with Cd and Zn toxicities in the wetland halophyte species Kosteletzkya virginica (L.) Presl. Plant Growth Regul 68:97–109CrossRefGoogle Scholar
  77. Han RM, Lefèvre I, Albacete A, Pérez-Alfocea F, Barba-Espin G, Díaz-Vivancos P, Quinet M, Ruan CJ, Hernández JA, Cantero-Navarro E, Lutts S (2013) Antioxidant enzyme activities and hormonal status in response to Cd stress in the wetland halophyte Kosteletzkya virginica under saline conditions. Physiol Plant 147:352–368PubMedCrossRefGoogle Scholar
  78. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102CrossRefGoogle Scholar
  79. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553CrossRefGoogle Scholar
  80. Hawkes SJ (1997) What is a “heavy metal”? J Chem Educ 74(11):1374CrossRefGoogle Scholar
  81. Helliwell B, Gutteridge JMC (1986) Iron and free radical reactions: two aspects of antioxidant protection. Trends Biochem Sci 11:375CrossRefGoogle Scholar
  82. Hernandez JA, Jimenez AP, Mullineaux SF (2000) Tolerance of pea (Pisum sativum L.) to long term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ 23:853–862CrossRefGoogle Scholar
  83. Hernandez JA, Ferrer MA, Jiménez A, Ros Barceló A, Sevilla F (2001) Antioxidant systems and O2 .−/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127(3):817–831PubMedPubMedCentralCrossRefGoogle Scholar
  84. Hirata K, Tsuji N, Miyamoto K (2005) Biosynthetic regulation of phytochelatins, heavy metal-binding peptides. J Biosci Bioeng 100:593–599PubMedCrossRefGoogle Scholar
  85. Hollander-Czytko H, Grabowski J, Sandorf I, Weckermann K, Weiler EW (2005) Tocopherol content and activities of tyrosine aminotransferase and cysteine lyase in Arabidopsis under stress conditions. J Plant Physiol 162:767–770PubMedCrossRefGoogle Scholar
  86. Hormann H, Neubauer C, Asada K, Scheiber U (1993) Intact chloroplast displays pH 5 optimum of O2 reduction in the absence of methyl vilogen: indirect evidence for a regulatory role of superoxide protonation. Photosynth Res 37:69–80PubMedCrossRefGoogle Scholar
  87. Hossain MA, Nakano Y, Asada K (1984) Mono-dehydroascorbate reductase in spinach choloroplast and its participation in regeneration of ascorbate scavenging hydrogen peroxide. Plant Cell Physiol 11:351–358Google Scholar
  88. Hossain Z, Nouri MZ, Komatsu S (2012) Plant cell organelle proteomics in response to abiotic stress. J Proteome Res 11:37–48PubMedCrossRefGoogle Scholar
  89. Huang GY, Wang YS (2009) Expression analysis of type 2 metallothionein gene in mangrove species (Bruguiera gymnorrhiza) under heavy metal stress. Chemosphere 77:1026–1029PubMedCrossRefGoogle Scholar
  90. Huang GY, Wang YS (2010) Expression and characterization analysis of type 2 metallothiobnein from grey mangrove species (Avicennia marina) in response to metal stress. Aquat Toxicol 99:86–92PubMedCrossRefGoogle Scholar
  91. Huang GY, Wang YS, Sun CC, Dong JD, Sun ZX (2010) The effect of multiple heavy metals on ascorbate, glutathione and related enzymes in two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Oceanol Hydrog Biol Stud 39(1):11–25Google Scholar
  92. Igamberdiev AU, Seregelyes C, Manac N, Hill RD (2004) NADH- dependent metabolism of nitric oxide in alfalfa root cultres expressing barley hemoglobin. Planta 219:95–102PubMedCrossRefGoogle Scholar
  93. Jha B, Sharma A, Mishra A (2011) Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicornia brachiata in tobacco for salt tolerance. Mol Biol Rep 38:4823–4832PubMedCrossRefGoogle Scholar
  94. Jimenez A, Hernandez JA, del Rio LA, Sevilla F (1997) Evidence for the presence of ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284PubMedPubMedCentralCrossRefGoogle Scholar
  95. Jitesh MN, Prashanth SR, Sivaprakash KR, Parida AK (2006) Antioxidative response mechanism in halophytes: their role in stress defence. J Genet 85:237–254CrossRefGoogle Scholar
  96. Kataya AR, Reumann S (2010) Arabidopsis glutathione reductase 1 is dually targeted to peroxisomes and the cytosol. Plant Signal Behav 5:171–175PubMedPubMedCentralCrossRefGoogle Scholar
  97. Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487CrossRefGoogle Scholar
  98. Khan I, Ahmad A, Iqbal M (2009) Modulation of antioxidant defence system for arsenic detoxification in Indian mustard. Ecotoxicol Environ Saf 72(2):626–634PubMedCrossRefGoogle Scholar
  99. Kiffin R, Bandyopadhyay U, Cuervo AM (2006) Oxidative stress and autophagy. Antioxid Redox Signal 8:152–162PubMedPubMedCentralCrossRefGoogle Scholar
  100. Kim DY, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932PubMedPubMedCentralCrossRefGoogle Scholar
  101. Klein M, Burla B, Martinoia E (2006) The multidrug resistance-associated proteins (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett 580:1112–1122PubMedCrossRefGoogle Scholar
  102. Koyro HW, Hussain T, Huchzermeyer B, Khan MA (2013) Photosynthetic and growth responses of a perennial halophytic grass Panicum turgidum to increasing NaCl concentrations. Environ Exp Bot 91:22–29CrossRefGoogle Scholar
  103. Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2013) Differential expression of rice Lambda class GST gene family members during plant growth, development, and in response to stress conditions. Plant Mol Biol Report 31:569–580CrossRefGoogle Scholar
  104. Kumari A, Sheokand S, Swaraj K (2010) Nitric oxide induced alleviation of toxic effects of short term and long term Cd stress on growth, oxidative metabolism and Cd accumulation in chickpea. Braz J Plant Physiol 22:271–284CrossRefGoogle Scholar
  105. Kumari A, Duhan S, Sheokand S, Kaur V (2017) Effects of short and long term salinity stress on physiological and oxidative metabolism in chickpea (Cicer arietinum) and its possible alleviation by nitric oxide. Indian J Ecol 44(2):250–258Google Scholar
  106. Lee S, Kim JH (2010) Establishment of tolerance to both cadmium and copper stress by expressing Arabidopsis phytochelatin synthase in Cu tolerant yeast mutant. J Korean Soc Appl Biol Chem 53:94–96CrossRefGoogle Scholar
  107. Lee J, Shim D, Song WY, Hwang I, Lee Y (2004) Arabidopsis metallo-thioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Mol Biol 54:805–815PubMedCrossRefGoogle Scholar
  108. Lefevre I, Marchal G, Meerts P, Corre’al E, Lutts S (2009) Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environ Exp Bot 65:142–152CrossRefGoogle Scholar
  109. Lefevre I, Marchal G, Ghanem ME, Correal E, Lutts S (2010) Cadmium has contrasting effects on polyethylene glycol – sensitive and resistant cell lines in the Mediterranean halophyte species Atriplex halimus. J Plant Physiol 167:365–374PubMedCrossRefGoogle Scholar
  110. Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51:141–165PubMedCrossRefGoogle Scholar
  111. Li Y, Trush MA (1993) Oxidation of hydrquinone by copper: chemical mechanism and biological effects. Biochim Biophys Acta 300:346–355Google Scholar
  112. Li Y, Zhou Y, Wang Z, Sun X, Tang K (2010) Engineering tocopherol biosynthetic pathway in Arabidopsis leaves and its effect on antioxidant metabolism. Plant Sci 178:312–320CrossRefGoogle Scholar
  113. Liang YC, Chen Q, Liu Q, Zhang WH, Ding RX (2003) Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). Plant Physiol 160:1157–1164CrossRefGoogle Scholar
  114. Liu Y, Wang X, Zeng G, Qu D, Gu J, Zhou M, Chai L (2007) Cadmium induced oxidative stress and response of the ascorbate-glutathione cycle in Bechmeria nivea (L.) Gaud. Chemosphere 69:99–107PubMedCrossRefGoogle Scholar
  115. Liu X, Duan D, Li W, Tadano T, Ajmal Khan M (2008) A comparative study on responses of growth and solute composition in halophytes Suaeda salsa and Limonium bicolor to salinity. In: Khan MA, Weber DJ (eds) Ecophysiology of high salinity tolerant plants. Springer, Dordrecht, pp 135–143Google Scholar
  116. Liu W, Zhang X, Liang L, Chen C, Wei S, Zhou Q (2015) Phytochelatin and oxidative stress under heavy metal stress tolerance in plants. In: Gupta DK, Palma JM, Corpas FJ (eds) Reactive oxygen species and oxidative damage in plants under stress. Springer, Cham, pp 191–217CrossRefGoogle Scholar
  117. Lokhande VH, Suprasanna P (2012) Prospectus of halophytes in understanding and managing abiotic stress tolerance. In: Ahmad P, MNV P (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 29–56CrossRefGoogle Scholar
  118. Lokhande VH, Nikam TD, Suprasanna P (2010) Differential osmotic adjustment to iso-osmotic salt and PEG stress in vitro in the halophyte Sesuvium portulacastrum L. J Crop Sci Biotechnol 13:251–256CrossRefGoogle Scholar
  119. Lokhande VH, Srivastava S, Patade VY, Dwivedi S, Tripathi RD, Nikam TD, Suprasanna P (2011) Investigation of arsenic accumulation and tolerance potential of Sesuvium portulacastrum (L.). Chemosphere 82:529–534PubMedCrossRefGoogle Scholar
  120. Lokhande VH, Mulye K, Patkar R, Nikam TD, Suprasanna P (2012) Biochemical and physiological adaptations of the halophyte Sesuvium portulacastrumm (L.), (Aiziaceae) to salinity. Arch Agron Soil Sci 59(10):1373–1391CrossRefGoogle Scholar
  121. Lopez-Chuken UJ, Young SD (2005) Plant screening of halophyte species for cadmium phytoremediation. Z Naturforsch 60:236–243Google Scholar
  122. López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez- Cadenas A (2011) Effects of cadmium on gas exchange and phytohormone contents in citrus. Biol Plant 55:187–190CrossRefGoogle Scholar
  123. Lunde C1, Baumann U, Shirley NJ, Drew DP, Fincher GB (2006) Gene structure and expression pattern analysis of three monodehydroascorbate reductase (Mdhar) genes in Physcomitrella patens: implications for the evolution of the MDHAR family in plants. Plant Mol Biol 60(2):259–275PubMedCrossRefGoogle Scholar
  124. Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J 79:544–567PubMedCrossRefGoogle Scholar
  125. Lutts S, Lefevre I (2015) How can we take advantage of halophyte properties to cope with heavy metal toxicity in salt affected areas? Ann Bot 115:509–528PubMedPubMedCentralCrossRefGoogle Scholar
  126. MacFarlane GR, Burchett MD (2001) Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the grey mangrove, Avicennia marina (Forsk) Vierh. Mar Pollut Bull 42:233–240PubMedCrossRefGoogle Scholar
  127. Madhusudhan R, Ishikawa T, Sawa Y, Shigeoka S, Shibata H (2003) Characterization of an ascorbate peroxidase in plastids of tobacco BY-2 cells. Physiol Plant 117:550–557PubMedCrossRefGoogle Scholar
  128. Mallick N (2004) Copper induced oxidative stress in the chlorophycean microalga Chlorella vulgaris response of the antioxidant system. J Plant Physiol 161:591–597PubMedCrossRefGoogle Scholar
  129. Mallick N, Rai LC (1999) Responses of the antioxidant systems of the nitrogen fixing cyanobacterium Anabaena doliolum to copper. J Plant Physiol 155:146–149CrossRefGoogle Scholar
  130. Mandal SK, Dey M, Ganguly D, Sen S, Jana TK (2009) Biogeochemical controls of arsenic occurrence and mobility in the Indian sundarban mangrove ecosystem. Mar Pollut Bull 58:652–657PubMedCrossRefGoogle Scholar
  131. Manousaki E, Kalogerakis N (2009) Phytoextraction of Pb and Cd by the Mediterranean saltbush (triplex halimus L.): metal uptake in relation to salinity. Environ Sci Pollut Res 16:844–854CrossRefGoogle Scholar
  132. Manuel J, Reigosa R (2001) Handbook of plant ecophysiol techniques. Kluwer Academic Publishers, Dordrecht, pp 365–383Google Scholar
  133. Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Ann Rev Plant Physiol Plant Mol Biol 47:127–158CrossRefGoogle Scholar
  134. Martinez M, Bernal P, Almela C, Vélez D, García Agustín P, Serrano R, Navarro-Aviñó J (2006) An engineered plant that accumulates higher levels of heavy metals than Thlaspi caerulescens, with yields of 100 times more biomass in mine soils. Chemosphere 64:478–485PubMedCrossRefGoogle Scholar
  135. Mendoza-Cozatl D, Loza-Tavera H, Hernández-Navarro A, Moreno-Sánchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29:653–671PubMedCrossRefGoogle Scholar
  136. Mendoza-Cozatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol–peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259PubMedPubMedCentralCrossRefGoogle Scholar
  137. Mesnoua M, Mateos-Naranjo E, Barcia-Piedras JM, Perez-Romero JA, Lotmani B, Redondo-Gomez S (2016) Physiological and biochemical mechanisms preventing Cd-toxicity in the hyperaccumulator Atriplex halimus L. Plant Physiol Biochem 106:30–38PubMedCrossRefGoogle Scholar
  138. Meychik NR, Nikolaeva IY, Yermakov IP (2013) Physiological response of halophyte (Suaeda altissima (L.) Pall.) and glycophyte (Spinacia oleracea L.) to salinity. Am J Plant Sci 4:427–435CrossRefGoogle Scholar
  139. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCrossRefGoogle Scholar
  140. Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  141. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2010) ROS signalling: the new wave? Trends Plant Sci 16:300–309CrossRefGoogle Scholar
  142. Moseki B, Buru JC (2010) Ionic and water relations of Sesuvium portulacastrum (L.). Sci Res Essay 5(1):035–040Google Scholar
  143. Nagarani N, JanakiDevi V, YokeshBabu M, Kumaraguru AK (2012) Protective effect of Kappaphycus alvarezii (Rhodophyta) extract against DNA damage induced by mercury chloride in marine fish. Toxicol Environ Chem 94:1401–1410CrossRefGoogle Scholar
  144. Nedjimi B, Daoud Y (2009) Cadmium accumulation in Atriplex halimus subsp. schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. Flora 204:316–324CrossRefGoogle Scholar
  145. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as a signaling molecules in plants. J Exp Bot 53:1237–1247PubMedCrossRefGoogle Scholar
  146. Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148PubMedPubMedCentralCrossRefGoogle Scholar
  147. Nocito FF, Lancilli C, Giacomini B, Sacchi GA (2007) Sulfur metabolism and cadmium stress in higher plants. Plant Stress 1:142–156Google Scholar
  148. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279PubMedCrossRefGoogle Scholar
  149. Noctor G, Arisi ACM, Jouanin L, Kuner KJ, Rennenberg H, Foyer C (1998) Glutathione biosynthesis metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647Google Scholar
  150. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484PubMedCrossRefGoogle Scholar
  151. Noiraud N, Maurousset L, Lemoine R (2001) Transport of polyols in higher plants. Plant Physiol Biochem 39:717–728CrossRefGoogle Scholar
  152. Oztetik E (2012) An introduction to oxidative stress in plants and the role of non-enzymatic antioxidants. In: Anjum NA, Umar S, Ahmad A (eds) Oxidative stress in plants: causes, consequences and tolerance. IK International Publishers, New Delhi, pp 1–50Google Scholar
  153. Pagani MA, Tomas M, Carrillo J, Bofill R, Capdevila M, Atrian S, Andreo CS (2012) The response of the different soybean metallothionein isoforms to cadmium intoxication. J Inorg Biochem 117:306–315PubMedCrossRefGoogle Scholar
  154. Panda A, Rangania J, Kumari A, Parida AK (2017) Efficient regulation of arsenic translocation to shoot tissue and modulation of phytochelatin levels and antioxidative defense system confers salinity and arsenic tolerance in the Halophyte Suaeda maritima. Environ Exp Bot 143:149–171CrossRefGoogle Scholar
  155. Pandey S, Fartyal D, Agarwal A, Shukla T, James D, Kaul T, Negi YK, Arora S, Reddy MK (2017) Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci 8:581PubMedPubMedCentralCrossRefGoogle Scholar
  156. Pardo-Domènech LL, Tifrea A, Grigore MN, Boscaiu M, Vicente O (2016) Proline and glycine betaine accumulation in two succulent halophytes under natural and experimental conditions. Plant Biosystems. Int J Dealing Asp Plant Biol 150(5):904–915Google Scholar
  157. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedCrossRefGoogle Scholar
  158. Parida AK, Jha B (2010) Antioxidative defense potential to salinity in the euhalophyte Salicornia brachiata. J Plant Growth Regul 29:137–148CrossRefGoogle Scholar
  159. Parida AK, Das AB, Das P (2002) NaCl stress causes changes in photosynthetic pigments, proteins and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. J Plant Biol 45:28–36CrossRefGoogle Scholar
  160. Perry JJP, Shin DS, Getzoff ED, Tainer JA (2010) The structural biochemistry of the superoxide dismutases. Biochim Biophys Acta 1804:245–262PubMedCrossRefGoogle Scholar
  161. Petraglia A, De-Benedictis M, Degoila F (2014) The capability to synthesize phytochelatins and the presence of constitutive and functional phytochelatin synthases are ancestral (plesiomorphic) characters for basal land plants. J Exp Bot 65:1153–1163PubMedCrossRefGoogle Scholar
  162. Piechalak A, Tomaszewska B, Baralkiewicz D, Malecka A (2002) Accumulation and detoxification of lead ions in legumes. Phytochemistry 60:153–162PubMedCrossRefGoogle Scholar
  163. Pilon-Smits EA, Zhu YL, Sears T, Terry N (2000) Over expression of glutathione reductase in Brassica juncea: effects on cadmium accumulation and tolerance. Physiol Plant 110:455–460CrossRefGoogle Scholar
  164. Pinto AP, Alves AS, Candeias AJ, Cardoso AI, de Varennes A, Martins LL et al (2009) Cadmium accumulation and antioxidative defenses in Brassica juncea L. Czern, Nicotiana tabacum L. and Solanum nigrum L. Int J Environ Anal Chem 89:661–676CrossRefGoogle Scholar
  165. Pomponi M, Censi V, Di-Garolamo V, De-Paolis A, Sanita-di-Toppi L, Aromolo R, Costantino P, Cardarelli M (2006) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta 223:180–190PubMedCrossRefGoogle Scholar
  166. Racchi ML, Bagnoli F, Balla I, Danti S (2001) Differential activity of catalase and superoxide dismutase in seedlings and in vitro micropropagated oak (Quercus robur L.). Plant Cell Rep 20:169–174PubMedCrossRefGoogle Scholar
  167. Ramos J, Clemente MR, Naya L, Loscos J, Pérez-Rontomé C, Sato S, Tabata S, Becana M (2007) Phytochelatin synthases of the model legume Lotus japonicus. A small multigene family with differential response to cadmium and alternatively spliced variants. Plant Physiol 143:1110–1118PubMedPubMedCentralCrossRefGoogle Scholar
  168. Ramos J, Naya L, Gay M, Abian J, Becana M (2008) Functional characterization of an unusual phytochelatin synthase, LjPCS3, of Lotus japonicus. Plant Physiol 148:536–545PubMedPubMedCentralCrossRefGoogle Scholar
  169. Rangani J, Parida AK, Panda A, Kumari A (2016) Coordinated changes in antioxidative enzymes protect the photosynthetic machinery from salinity induced oxidative damage and confer salt tolerance in an extreme halophyte Salvadora persica L. Front Plant Sci 7:1–18CrossRefGoogle Scholar
  170. Rastgoo L, Alemzadeh A (2011) Biological responses of Gouan (Aeluropus littoralis) to heavy metal stress. Aust J Crop Sci 5(4):375–383Google Scholar
  171. Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509PubMedCrossRefGoogle Scholar
  172. Redondo-Gomez S, Mateos-Naranjo E, Figueroa ME, Davy AJ (2010) Salt stimulation of growth and photosynthesis in an extreme halophyte, Arthrocnemum macrostachyum. Plant Biol 12:79–87PubMedCrossRefGoogle Scholar
  173. Redondo-Gomez S, Andrades-Moreno L, Mateos-Naranjo E, Parra R, Valera-Burgos J, Aroca R (2011) Synergic effect of salinity and zinc stress on growth and photosynthetic responses of the cordgrass, Spartina densiflora. J Exp Bot 62:5521–5530PubMedPubMedCentralCrossRefGoogle Scholar
  174. Rhodes D, Nadolska-Orczyk A, Rich PJ (2002) Salinity, osmolytes and compatible solutes. In: Läuchli A, Lüttge U (eds) Salinity: environment – plants – molecules. Kluwer, Dordrecht, pp 181–204Google Scholar
  175. Rodrıguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gomez M, Del Rio LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544PubMedCrossRefGoogle Scholar
  176. Rozema J, Muscolo A, Flowers T (2013) Sustainable cultivation and exploitation of halophyte crops in a salinising world. Environ Exp Bot 92:1–3CrossRefGoogle Scholar
  177. Ruan CJ, Li H, Guo YQ, Qin P, Gallagher JL, Seleskar DM, Lutts S, Mahy G (2008) Kosteletzkya virginica, an agroecoengineering halophytic species for alternative agricultural production in China’s east coast: ecological adaptation and benefits, seed yield, oil content, fatty acid and biodiesel properties. Ecol Eng 32:320–328CrossRefGoogle Scholar
  178. Ruan CJ, Teixeira da Silva JA, Mopper S, Qin P, Lutts S (2010) Halophyte improvement for a salinized world. Crit Rev Plant Sci 29:329–359CrossRefGoogle Scholar
  179. Sabarinath S, Khanna S, Khanna-Chopra R (2009) Purification and characterization of thermostable monomeric chloroplastic Cu/Zn superoxide dismutase from Chenopodium murale. Physiol Mol Biol Plants 15:199–209CrossRefGoogle Scholar
  180. Sachiko M, Mundelanji V, Takafumi K, Shingo N, Kentaro S, Naoki T (2009) Role of C-terminal Cys-rich region of phytochelatin synthase in tolerance to cadmium ion toxicity. J Plant Biochem Biotechnol 18:175–180CrossRefGoogle Scholar
  181. Safafar H, van Wagenen J, Moller P, Jacobsen C (2015) Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater. Mar Drugs 13:7339–7356PubMedPubMedCentralCrossRefGoogle Scholar
  182. Sai Kachout S, Ben Mansoura A, Leclerc JC, Mechergui R, Rejeb MN, Ouerghi Z (2009) Effects of heavy metals on antioxidant activities of Atriplex hortensis and A. Rosea. Electron J Environ Agric Food Chem 9:444–457Google Scholar
  183. Sai Kachout S, Ben Mansoura A, Ennajah A, Leclerc JC, Ouerghi Z, Karray Bouraoui N (2015) Effects of metal toxicity on growth and pigment contents of annual halophyte (A. hortensis and A. rosea). Int J Environ Res 9(2):613–620Google Scholar
  184. Saiyood S, Vangnai AS, Inthorn D, Thiravetyan P (2012) Treatment of total dissolved solids from plastic industrial effluent by halophyte plants. Water Air Soil Pollut 223:4865–4873CrossRefGoogle Scholar
  185. Sandalio LM, Romero-Puertas MC (2015) Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. Ann Bot 116(4):475–485PubMedPubMedCentralCrossRefGoogle Scholar
  186. Saxena I, Srikanth S, Chen Z (2016) Cross talk between H2O2 and interacting signal molecules under plant stress response. Front Plant Sci 7:570PubMedPubMedCentralCrossRefGoogle Scholar
  187. Sbartai H, Djebar MR, Sbartai I, Berrabbah H (2012) Bioaccumulation of cadmium and zinc in tomato (Lycopersicon esculentum L.). Comptes Rendus. Biology 335:585–593Google Scholar
  188. Scandalias JG (1990) Response of plant antioxidant defense genes to environmental stress. Adv Genet 28:1–41CrossRefGoogle Scholar
  189. Schickler H, Caspi H (1999) Response of antioxidative enzymes to nickel and cadmium stress in hyperaccumulator plants of the genus Alyssum. Physiol Plant 105:39–44CrossRefGoogle Scholar
  190. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365PubMedGoogle Scholar
  191. Schutzendubel A, Nikolova P, Rudolf C, Polle A (2002) Cadmium and H2O2-induced oxidative stress in Populus canescens roots. Plant Physiol Bichem 40:577–584CrossRefGoogle Scholar
  192. Sekmen AH, Turkan I, Takio S (2007) Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol Plant 131:399–411PubMedCrossRefGoogle Scholar
  193. Servet C, Ghelis T, Richard L, Zilberstein A, Savoure’ A (2012) Proline dehydrogenase: a key enzyme in controlling cellular homeostasis. Front Biosci 17:607–620CrossRefGoogle Scholar
  194. Sghaier DB, Duarte B, Bankaji I, Caçador I, Sleimi N (2015) Growth, chlorophyll fluorescence and mineral nutrition in the halophyte Tamarix gallica cultivated in combined stress conditions: arsenic and NaCl. J Photochem Photobiol B Biol 149:204–214CrossRefGoogle Scholar
  195. Shackira AM, Puthur JT (2013) An assessment of heavy metal contamination in soil sediments, leaves and roots of Acanthus ilicifolius L. Proceedings of 23rd Swadeshi Science Congress, pp 689–692Google Scholar
  196. Shackira M, Puthur JT (2017) Enhanced phytostabilization of cadmium by a halophyte—Acanthus ilicifolius L. Int J Phytoremediation 19(4):319–326PubMedCrossRefGoogle Scholar
  197. Shaheen S, Naseer S, Ashraf M, Akram NA (2013) Salt stress affects water relations, photosynthesis, and oxidative defense mechanisms in Solanum melongena L. J Plant Interact 8:85–96CrossRefGoogle Scholar
  198. Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Rev Environ Contam Toxicol 232:1–44PubMedGoogle Scholar
  199. Shao HB, Liang ZS, Shao MA, Sun Q (2005) Dynamic changes of anti- oxidative enzymes of 10 wheat genotypes at soil water deficits. Colloids Surf B: Biointerfaces 42:187–195PubMedCrossRefGoogle Scholar
  200. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726PubMedCrossRefGoogle Scholar
  201. Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50PubMedCrossRefGoogle Scholar
  202. Sharma P, Dubey RS (2004) Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci 167:541–550CrossRefGoogle Scholar
  203. Sharma V, Ramawat KG (2014) Salt stress enhanced antioxidant response in callus of three halophytes (Salsola baryosma, Trianthema triquetra, Zygophyllum simplex) of Thar Desert. Biologia 69(2):178–185CrossRefGoogle Scholar
  204. Sharma A, Gontia I, Agarwal PK, Jha B (2010) Accumulation of heavy metals and its biochemical responses in Salicornia brachiata, an extreme halophyte. Mar Biol Res 6(5):511–518CrossRefGoogle Scholar
  205. 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.  https://doi.org/10.1155/2012/217037 CrossRefGoogle Scholar
  206. Sheokand S, Bhankar V, Sawhney V (2010) Ameliorative effect of exogenous nitric oxide on oxidative metabolism in NaCl treated chickpea plants. Braz J Plant Physiol 22:81–90CrossRefGoogle Scholar
  207. Shevyakova NI, Netronina IA, Aronova EE, Kuznetsov VIV (2003) Compartmentation of cadmium and iron in Mesembryanthemum crystallinum plants during the adaptation to cadmium stress. Russ J Plant Physiol 179:57–64Google Scholar
  208. Shi X, Dalal NS (1993) Vanadate-mediated hydroxyl radical generation from superoxide radical in the presence of NADH: Haber-Weiss versus Fenton mechanism. Biochim Biophys Acta 307:336–341Google Scholar
  209. Shi X, Dalal NS, Kasprzak KS (1993) Generation of free radicals from hydrogen peroxide and lipid hydroperoxides in the presence of Cr (III). Biochim Biophys Acta 302:294–299Google Scholar
  210. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y et al (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319PubMedCrossRefGoogle Scholar
  211. Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14(11):2837–2847PubMedPubMedCentralCrossRefGoogle Scholar
  212. Sirko A, Blaszczyk A, Liszewska F (2004) Overproduction of SAT and/or OASTL in transgenic plants: a survey of effects. J Exp Bot. 2004 55:1881–1888PubMedCrossRefGoogle Scholar
  213. Smeets K, Ruytinx J, Semane B, Van Belleghem F, Remans T, Van Sanden S et al (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63:1–8CrossRefGoogle Scholar
  214. Smirnoff N (2005) Ascorbate, tocopherol and carotenoids: metabolism, pathway engineering and functions. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell Publishing Ltd, Oxford, pp 53–86CrossRefGoogle Scholar
  215. Srinivasa Reddy M, Basha S, Sravan KVG, Joshi HV, Ghosh PK (2003) Quantification and classification of ship scraping waste at Alang–Sosiya, India. Mar Pollut Bull 46:1609–1614PubMedCrossRefGoogle Scholar
  216. Sruthi P, Majeed AS, Puthur JT (2017) Heavy metal detoxification mechanisms in halophytes: an overview. Wetl Ecol Manag 25:129–148CrossRefGoogle Scholar
  217. Szabados L, Savoure’ A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97PubMedCrossRefGoogle Scholar
  218. Takagi H, Yamada S (2013) Roles of enzymes in anti-oxidative response system on three species of chenopodiaceous halophytes under NaCl-stress condition. Soil Sci Plant Nutr 59:603–611CrossRefGoogle Scholar
  219. Tao YM, Chen YZ, Tan T, Liu XC, Yang DL, Liang SC (2012) Comparison of antioxidant responses to cadmium and lead in Bruguiera gymnorrhiza seedlings. Biol Plant 56:149–152CrossRefGoogle Scholar
  220. Tennstedt P, Peisker D, Böttcher C, Trampczynska A, Clemens S (2009) Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol 149:938–948PubMedPubMedCentralCrossRefGoogle Scholar
  221. Tewari A, Joshi HV, Trivedi RH, Srvankumar VG, Raghunathan C, Khambhati Y, Kotiwar OS, Mandal SK (2001) Studies on the effect of ship scraping industry and its associated waste on the biomass production and biodiversity of biota in in-situ condition at Alang. Mar Pollut Bull 42:462–469PubMedCrossRefGoogle Scholar
  222. Thangavel P, Long S, Minocha R (2007) Changes in phytochelatins and their biosynthetic intermediates in red spruce (Picea rubens Sarg.) cell suspension culture under cadmium and zinc stress. Plant Cell Tissue Organ Cult 88:201–216CrossRefGoogle Scholar
  223. Thomas JC, Malick FK, Endreszl C, Davies EC, Murray KS (1998) Distinct responses to copper stress in the halophyte Mesembryanthemum Crystallinum. Physiol Plant 102:360–368CrossRefGoogle Scholar
  224. Tiryakioglu M, Eker S, Ozkutlu F, Husted S, Cakmak I (2006) Anitioxidant defence and system and cadmium uptake in barley genotypes differing in cadmium tolerance. J Trace Elem Med Biol 20:181–189PubMedCrossRefGoogle Scholar
  225. Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJM (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trend BioTechnol 25:158–165CrossRefGoogle Scholar
  226. Tripathi P, Mishra A, Dwivedi S, Chakrabarty D, Trivedi PK, Singh RP, Tripathi RD (2012) Differential response of oxidative stress and thiol metabolism in contrasting rice genotypes for arsenic tolerance. Ecotoxicol Environ Saf 79:189–198PubMedCrossRefGoogle Scholar
  227. Usha B, Venkataraman G, Parida A (2009) Heavy metal and abiotic stress inducible metallothionein isoforms from Prosopis juliflora (SW) D.C. show differences in binding to heavy metals in vitro. Mol Gen Genomics 281:99–108CrossRefGoogle Scholar
  228. Vatamaniuk OK, Mari S, Lu YP, Rea PA (2000) Mechanism of heavy metal ion activation of phytochelatin (PC) synthase. J Biol Chem 275:31451–31459PubMedCrossRefGoogle Scholar
  229. Venkatesan A, Chellappan KP (1998) Accumulation of proline and glycinebetaine in Ipomoea pes-caprae induced by NaCl. Biol Plant 41:271–276CrossRefGoogle Scholar
  230. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759PubMedCrossRefGoogle Scholar
  231. Verma S, Dubey RS (2001) Effect of cadmium on soluble sugars and enzymes of their metabolism in rice. Biol Plant 44:117–123CrossRefGoogle Scholar
  232. Vranova E, Inze D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236PubMedCrossRefGoogle Scholar
  233. Vromman D, Lefèvre I, Šlejkovec Z, Martínez JP, Vanhecke N, Briceño M, Kumar M, Lutts S (2016) Salinity influences arsenic resistance in the xerohalophyte Atriplex atacamensis. Philos Environ Exp Bot 126:32–43CrossRefGoogle Scholar
  234. Wachter A, Wolf S, Steiniger H, Bogs J, Rausch T (2005) Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J 41:15–30PubMedCrossRefGoogle Scholar
  235. Walker DJ, Lutts S, Sánchez-García M, Correal E (2014) Atriplex halimus L.: its biology and uses. J Arid Environ 100–101:111–121CrossRefGoogle Scholar
  236. Wang Y, Ying Y, Chen J, Wang XC (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci 167:671–677CrossRefGoogle Scholar
  237. Wang C, Sun Q, Wang L (2009) Cadmium toxicity and phytochelatins production in a rooted-submerged macrophyte Vallisneria spiralis exposed to low concentrations of cadmium. Environ Toxicol 24:271–278PubMedCrossRefGoogle Scholar
  238. Wang HL, Tian CY, Jiang L, Wang L (2014) Remediation of heavy metals contaminated saline soils: a halophyte choice. Environ Sci Technol 48:21–22PubMedCrossRefGoogle Scholar
  239. Wei ZW, Wong JJ, Chen D (2003) Speciation of heavy metal binding non protein thiols in Agropyronelongaturn by size-exclusion HPLC- ICP-MS. Microchem J 74:207–213CrossRefGoogle Scholar
  240. Willenkens H, Inze D, Van Montagu M, Van Camp W (1995) Catalase in plants. Mol Breed 1:207–228CrossRefGoogle Scholar
  241. Wu G, Wei ZK, Shao HB (2007) The mutual responses of higher plants to environment: physiological and microbiological aspects. Biointerfaces 59:113–119CrossRefGoogle Scholar
  242. Wu H, Liu X, Zhao J, Yu J (2013) Regulation of metabolites, gene expression, and antioxidant enzymes to environmentally relevant lead and zinc in the halophyte Suaeda salsa. J Plant Growth Regul 32:353–361CrossRefGoogle Scholar
  243. 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 126:564–574PubMedPubMedCentralCrossRefGoogle Scholar
  244. Xue T, Li X, Zhu W, Wu C, Yang G, Zheng C (2009) Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast. J Exp Bot 60:339–349PubMedCrossRefGoogle Scholar
  245. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South Afr J Bot 76:167–179CrossRefGoogle Scholar
  246. Yang Z, Wu Y, Li Y, Ling HQ, Chu C (2009) OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice. Plant Mol Biol 70:219–229PubMedCrossRefGoogle Scholar
  247. Yildiztugay E, Ozfidan-Konakci C, Kucukoduk M (2014) The role of antioxidant responses on the tolerance range of extreme halophyte Salsola crassa grown under toxic salt concentrations. Ecotoxicol Environ Saf 110:21–30PubMedCrossRefGoogle Scholar
  248. Yuanyuan M, Yali Z, Jiang L, Hongbo S (2009) Roles of plant soluble sugars and their responses to plant cold stress. Afr J Biotechnol 8:2004–2010Google Scholar
  249. Zaefyzadeh M, Quliyev RA, Babayeva SM, Abbasov MA (2009) The effect of the interaction between genotypes and drought stress on the superoxide dismutase and chlorophyll content in durum wheat landraces. Turk J Biol 33:1–7Google Scholar
  250. Zenk MH (1996) Heavy metal detoxification in higher plants: a review. Gene 79:21–30CrossRefGoogle Scholar
  251. Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50PubMedCrossRefGoogle Scholar
  252. Zhao FJ, Ago Y, Mitani N, Li RY, Su YH, Yamaji N, McGrath SP, Ma JF (2010) The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol 186:392–399PubMedCrossRefGoogle Scholar
  253. Zhu YL, Pilon-Smits EAH, Jouanin L, Terry N (1999) Over-expression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:3–79Google Scholar
  254. Zhu J, Zhang Q, Wu R, Zhang Z (2010) HbMT2, an ethephon-induced metallothionein gene from Hevea brasiliensis responds to H2O2 stress. Plant Physiol Biochem 48(8):710–715PubMedCrossRefGoogle Scholar
  255. Zimeri AM, Dhankher OP, McCaig B, Meagher RB (2005) The plant MT1 metallothioneins are stabilized by binding cadmiums and are required for cadmium tolerance and accumulation. Plant Mol Biol 58(6):839–855PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Anita Kumari
    • 1
  • Vinod Goyal
    • 1
  • Sunita Sheokand
    • 2
  1. 1.Chaudhary Charan Singh Haryana Agricultural UniversityHisarIndia
  2. 2.Department of Botany and Plant PhysiologyCCS Haryana Agricultural UniversityHisarIndia

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