Environmental Science and Pollution Research

, Volume 26, Issue 8, pp 7821–7839 | Cite as

Joint effects of Si and mycorrhiza on the antioxidant metabolism of two pigeonpea genotypes under As (III) and (V) stress

  • Neera GargEmail author
  • Lakita Kashyap
Research Article


Arsenic (As) is the most hazardous soil contaminant, which inactivates metabolic enzymes and restrains plant growth. To withstand As stress conditions, use of some alleviative tools, such as arbuscular mycorrhizal (AM) fungi and silicon (Si), has gained importance. Therefore, the present study evaluated comparative and interactive effects of Si and arbuscular mycorrhiza-Rhizophagus irregularis on phytotoxicity of arsenate (As V) and arsenite (As III) on plant growth, ROS generation, and antioxidant defense responses in pigeonpea genotypes (Tolerant-Pusa 2002; Sensitive-Pusa 991). Roots of As III treated plants accumulated significantly higher total As than As V supplemented plants, more in Pusa 991 than Pusa 2002, which corresponded to proportionately decreased plant growth, root to biomass ratio, and oxidative burst. Although Si nutrition and AM inoculations improved plant growth by significantly reducing As uptake and the resultant oxidative burst, AM was relatively more efficient in upregulating enzymatic and non-enzymatic antioxidant defense responses as well as ascorbate–glutathione pathway when compared with Si. Pusa 2002 was more receptive to Si nourishment due to its ability to establish more efficient mycorrhizal symbiosis, which led to higher Si uptake and lower As concentrations. Moreover, +Si+AM bestowed better metalloid resistance by further reducing ROS and strengthening antioxidants. Results demonstrated that the genotype with more efficient AM symbiosis in As-contaminated soils could accrue higher benefits of Si fertilization in terms of metalloid tolerance in pigeonpea.


Arbuscular mycorrhiza Silicon Arsenate Arsenite Oxidative burden Ascorbate-glutathione pool 



We gratefully acknowledge the University Grants Commission (UGC-No.f.25-1/2013-14(BSR)/7-151/2007(BSR) and Department of Biotechnology (DBT-BT/PR9466/AGR/21/231/2007), Government of India, for providing financial support in undertaking the research work. We are also thankful to TERI, New Delhi, and Pulse Laboratory, IARI, New Delhi, for providing the biological research material.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abbas MH, Meharg AA (2008) Arsenate, arsenite and dimethyl arsinic acid (DMA) uptake and tolerance in maize (Zea mays L.). Plant Soil 304:277–289CrossRefGoogle Scholar
  2. Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology, 105th edn. Academic Press, Orlando, pp 121–126Google Scholar
  3. Arakawa N, Tsutsumi K, Sanceda NG, Kurata T, Inagaki C (1981) A rapid and sensitive method for the determination of ascorbic acid using 4, 7-diphenyl-l, 10-phenanthroline. Agric Biol Chem 45(5):1289–1290Google Scholar
  4. Asada K (1984) Chloroplasts: formation of active oxygen and its scavenging. Meth Enzymol 105:422–429CrossRefGoogle Scholar
  5. Awasthi S, Chauhan R, Srivastava S, Tripathi RD (2017) The journey of arsenic from soil to grain in rice. Front Plant Sci 8:1007Google Scholar
  6. Bhargava P, Srivastava AK, Urmil S, Rai LC (2005) Phytochelatin plays a role in UV-B tolerance in N2-fixing cyanobacterium Anabaena doliolum. J Plant Physiol 162:1220–1225CrossRefGoogle Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  8. Casieri L, Gallardo K, Wipf D (2012) Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta 235:1431–1447CrossRefGoogle Scholar
  9. Castillo FI, Penel I, Greppin H (1984) Peroxidase release induced by ozone in Sedum album leaves. Plant Physiol 74:846–851CrossRefGoogle Scholar
  10. Castillo FJ, Greppin H (1988) Extracellular ascorbic acid and enzyme activities related to ascorbic acid metabolism in Sedum album L. leaves after ozone exposure. Environ Exp Bot 28:232–233CrossRefGoogle Scholar
  11. Chaturvedi I (2005) Effects of arsenic concentrations and forms on growth and arsenic uptake and accumulation by Indian mustard (Brassica juncea L.) genotypes. J Cent Eur Agri 7:31–40Google Scholar
  12. Choudhary AK, Singh D (2011) Screening of pigeonpea genotypes for nutrient uptake efficiency under aluminium toxicity. Physiol Mol Biol Plants 17(2):145–152CrossRefGoogle Scholar
  13. Chung JY, Yu SD, Hong YS (2014) Environmental source of arsenic exposure. J Prev Med Public Health 47(5):253–257CrossRefGoogle Scholar
  14. Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902CrossRefGoogle Scholar
  15. da Silva AJ, Nascimento CW, Gouveia-Neto AS, Silva Junior EA (2015) Effects of silicon on alleviating arsenic toxicity in maize plants. Rev Bras Ci Solo 39:289–296CrossRefGoogle Scholar
  16. Dave R, Mishra A, Tripathi RD, Dwivedi S, Tripathi P, Dixit G, Sharma YK, Trivedi PK, Corpus FJ, Barroso JB, Chakrabarty D (2013) Arsenate and arsenite exposure modulate antioxidants and amino acids in contrasting arsenic accumulating rice (Oryza sativa L.) genotypes. J Hazard Mater 262:1123–1131CrossRefGoogle Scholar
  17. del Longo OT, Gonzalez CA, Pastori GM, Tripps VS (1993) Antioxidant defenses under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought. Plant Cell Physiol 34:1023–1028Google Scholar
  18. Dhindsa RS, Plumb-Dhindsa P, Throne TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101CrossRefGoogle Scholar
  19. Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophtora infestans and the hyphal wall components. Physiol Plant Pathol 23:345–357CrossRefGoogle Scholar
  20. Dresler S, Wójci M, Bednarek W, Hanaka A, Tukiendorf A (2015) The effect of silicon on maize growth under cadmium stress. Russ J Plant Physiol 62(1):86–92CrossRefGoogle Scholar
  21. Duan CG-L, Zhu Y-G, Tong Y-P, Cai C, Kneer R (2005) Characterization of arsenate reductase in the extract of roots and fronds of Chinese Brake Fern, an arsenic hyperaccumulator. Plant Physiol 138:461–469CrossRefGoogle Scholar
  22. Elliott CL, Snyder GH (1991) Autoclave-induced digestion for the colorimetric determination of silicon in rice straw. J Agric Food Chem 39:1118–1119CrossRefGoogle Scholar
  23. Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:756120–756118. CrossRefGoogle Scholar
  24. Finnegan PM, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 3:182. CrossRefGoogle Scholar
  25. Fleck AT, Mattusch J, Schenk MK (2013) Silicon decreases the arsenic level in rice grain by limiting arsenite transport. J Plant Nutr Soil Sci 176:785–794Google Scholar
  26. Garg N, Bhandari P (2016) Silicon nutrition and mycorrhizal inoculations improve growth, nutrient status, K+ /Na+ ratio and yield of Cicer arietinum L. genotypes under salinity stress. Protoplasma 78:371–387Google Scholar
  27. Garg N, Kashyap L (2017) Silicon and Rhizophagus irregularis: potential candidates for ameliorating negative impacts of arsenate and arsenite stress on growth, nutrient acquisition and productivity in Cajanus cajan (L.) Millsp. genotypes. Environ Sci Pollut Res24 (22): 18520–18535Google Scholar
  28. Garg N, Pandey R (2015) Effectiveness of native and exotic arbuscular mycorrhizal fungi on nutrient uptake and ion homeostasis in salt-stressed Cajanus cajan L. (Millsp.) genotypes. Mycorrhiza 25(3):165–180CrossRefGoogle Scholar
  29. Garg N, Singla P (2012) The role of Glomus mosseae on key physiological and biochemical parameters of pea plants grown in arsenic contaminated soil. Sci Hortic 143:92–101CrossRefGoogle Scholar
  30. Georgiadis M, Cai Y, Solo-Gabriele HM (2006) Extraction of arsenate and arsenite species from soils and sediments. Environ Pollut 141(1):22–29CrossRefGoogle Scholar
  31. Ghosh N, Adak MK, Ghosh PD, Gupta S, Sen Gupta DN, Mandal C (2011) Differential responses of two rice varieties to salt stress. Plant Biotechnol Rep 5(1):89–103CrossRefGoogle Scholar
  32. Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  33. Gonzalez-Chavez MC, Harris PJ, Dodd J, Meharg AA (2002) Arbuscular mycorrhizal fungi enhanced arsenate resistance on Holcus lanatus. New Phytol 155:163–171CrossRefGoogle Scholar
  34. González-Chávez MDC, Miller B, Maldonado-Mendoza IE, Scheckel K, Carrillo-González R (2014) Localization and speciation of arsenic in Glomus irregularis by synchrotron radiation spectroscopic analysis. Fungal Biol 118:444–452CrossRefGoogle Scholar
  35. González-Chávez MDC, Ortega-Larrocea MDP, Carrillo-González R, López-Meyer M, Xoconostle-Cázares B, Gomez SK, Harrison MJ, Figueroa-López AM, Maldonado-Mendoza LE (2011) Arsenate induces the expression of fungal genes involved in as transport in arbuscular mycorrhiza. Fungal Biol 115:1197–1209CrossRefGoogle Scholar
  36. González-Guerrero M, Oger E, Benabdellah K, Azcón-Aguilar C, Lanfranco L, Ferrol N (2010) Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices. Curr Genet 56:265–274CrossRefGoogle Scholar
  37. Greger M, Bergqvist C, Sandhi A, Landberg T (2015) Influence of silicon on arsenic uptake and toxicity in lettuce. J App Bot Food Qual 88:234–240Google Scholar
  38. Guerriero G, Hausman J-F, Legay S (2016) Silicon and the plant extracellular matrix. Front Plant Sci 7:463Google Scholar
  39. Gunes A, Pilbeam DJ, Inal A (2009) Effect of arsenic–phosphorus interaction on arsenic-induced oxidative stress in chickpea plants. Plant Soil 314:211–220CrossRefGoogle Scholar
  40. Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21(2):117–129CrossRefGoogle Scholar
  41. Hart MM, Forsythe JA (2012) Using arbuscular mycorrhizal fungi to improve the nutrient quality of crops; nutritional benefits in addition to phosphorus. Sci Hortic 148:206–214CrossRefGoogle Scholar
  42. Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plants 23(2):249–268CrossRefGoogle Scholar
  43. Hashem A, Abd_Allah EF, Alqarawi AA, Al Huqail AA, Egamberdieva D, Wirth S (2016) Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23:272–281CrossRefGoogle Scholar
  44. Heath RLC, Packer I (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stochiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  45. Hillocks RJ, Minja E, Nahdy MS, Subrahmanyam P (2000) Diseases and pests of pigeonpea in eastern Africa. Int J Pest Manag 46:7–18CrossRefGoogle Scholar
  46. Huda AKMN, Haque MA, Zaman R, Swaraz AM, Kabir AH (2017) Silicon ameliorates chromium toxicity through phytochelatin mediated vacuolar sequestration in roots of Oryza sativa (L.) Inter J Phyto19: 246–253.
  47. Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13:3145–3175CrossRefGoogle Scholar
  48. Khan I, Ahmad A, Iqbal M (2009) Modulation of antioxidant defence system for arsenic detoxification in Indian mustard. Ecotoxicol Environ Saf 72:626–634CrossRefGoogle Scholar
  49. Labudda M, Azam FMS (2014) Glutathione-dependent responses of plants to drought: a review. Acta Soc Bot Pol 83(1):3–12CrossRefGoogle Scholar
  50. Liu J, Zhang H, Zhang Y, Chai T (2013) Silicon attenuates cadmium toxicity in Solanum nigrum L. by reducing cadmium uptake and oxidative stress. Plant Physiol Biochem 68:1–7CrossRefGoogle Scholar
  51. Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci U S A 105(29):9931–9935CrossRefGoogle Scholar
  52. Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MN (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44(1):25–37CrossRefGoogle Scholar
  53. Mohammadi K, Khalesro S, Sohrabi Y, Heidari G (2011) A review: beneficial effects of the mycorrhizal fungi for plant growth. J Appl Environ Biol Sci 1(9): 310–319Google Scholar
  54. Moreno-Jiménez E, Esteban E, Peñalosa JM (2012) The fate of arsenic in soil-plant systems. In: Whitacre DM (ed) Reviews of environmental contamination and toxicology. Springer Science+Business Media, New York, pp 1–37Google Scholar
  55. Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299CrossRefGoogle Scholar
  56. Nagarajan VK, Ebbs SD (2010) Arsenate reductase activity in roots from the arsenic hyperaccumulator Pteris vittata utilizes both glutathione and dithiothreitol as reductants. Plant Biosystems 144(4):857–859CrossRefGoogle Scholar
  57. Nakagawara S, Sagisaka S (1984) Increase in enzyme activities related to ascorbate metabolism during cold acclimation in poplar twigs. Plant Cell Physiol 25(6):899–906Google Scholar
  58. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880Google Scholar
  59. Neumann D, zur Nieden U (2001) Silicon and heavy metal tolerance of higher plants. Phytochemistry 56:685–692CrossRefGoogle Scholar
  60. Odeny DA (2007) The potential of pigeonpea (Cajanus cajan (L.) Millsp.) in Africa. Nat Res Forum 31:297–305CrossRefGoogle Scholar
  61. Oye Anda CC, Opfergelt S, Declerk S (2016) Silicon acquisition by banannas (c.V. Grande Naine) is increased in presence of the arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 41833. Plant Soil 409:77–85CrossRefGoogle Scholar
  62. Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol Soc 55(1):158–161CrossRefGoogle Scholar
  63. Pigna M, Caporale AG, Cavalca L, Sommella A, Violante A (2015) Arsenic in the soil environment: mobility and phytoavailability. Environ Eng Sci 32(7):551–563CrossRefGoogle Scholar
  64. Raza MM, Ullah S, Ahmad Z, Saqib S, Ahmad S, Bilal HM, Wali F (2016) Silicon mediated arsenic reduction in rice by limiting its uptake. Agric Sci 7:1–10Google Scholar
  65. Sbareto VM, Sanchez HJ (2001) Analysis of arsenic pollution in groundwater aquifers by X-ray fluorescence. Appl Rad Iso 54(5):37–740Google Scholar
  66. Schüβler A, Walker C (2010) The Glomeromycota: a species list with new families and genera. Edinburgh & Kew, UK, The Royal Botanic Garden; Munich, Germany: Botanische Staatssammlung Munich and Oregon, USA: Oregon State UniversityGoogle Scholar
  67. Sharma I (2012) Arsenic induced oxidative stress in plants. Biologia 67(3):447–453CrossRefGoogle Scholar
  68. Sharma S, Anand G, Singh N and Kapoor R (2017) Arbuscular mycorrhiza augments arsenic tolerance in wheat (Triticum aestivum L.) by strengthening antioxidant defense system and thiol metabolism. Front Plant Sci 8: 906Google Scholar
  69. Shekari F, Abbasi A, Mustafavi SH (2016) Effect of silicon and selenium on enzymatic changes and productivity of dill in saline condition. J Saudi Society Agri Sci 11(3):219–238Google Scholar
  70. Shen S, Li X-F, Cullen WR, Weinfeld M, Le XC (2013) Arsenic binding to proteins. Chem Rev 113:7769–7792CrossRefGoogle Scholar
  71. Shereefa LA, Kumaraswamy M (2016) Reactive oxygen species and ascorbate–glutathione interplay in signaling and stress responses in Sesamum orientale L. against Alternaria sesami (Kawamura) Mohanty and Behera. J Saudi Soc Agric Sci 15(1):48–56Google Scholar
  72. Shi G, Cai Q, Liu C, Wu L (2010) Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. Plant Growth Regul 61:45–52CrossRefGoogle Scholar
  73. Shi Q, Bao Z, Zhu Z, He Y, Qian Q, Yu J (2005) Silicon-mediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66:1551–1559CrossRefGoogle Scholar
  74. Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110CrossRefGoogle Scholar
  75. Siddiqui F, Tandon PK, Srivastava S (2015a) Arsenite and arsenate impact the oxidative status and antioxidant responses in Ocimum tenuiflorum L. Physiol Mol Biol Plants 21(3):453–458CrossRefGoogle Scholar
  76. Siddiqui F, Tandon PK, Srivastava S (2015b) Analysis of arsenic induced physiological and biochemical responses in a medicinal plant, Withania somnifera. Physiol Mol Biol Plants 21(1):61–69CrossRefGoogle Scholar
  77. Singh N, Raj A, Khare PB, Tripathi RD, Jamil S (2010) Arsenic accumulation pattern in 12 Indian ferns and assessing the potential of Adiantum capillus-veneris, in comparison to Pteris vittata, as arsenic hyperaccumulator. Bioresour Technol 101:8960–8968CrossRefGoogle Scholar
  78. Singh S, Tripathi DK, Chauhan DK, Dubey NK (2016) Glutathione and phytochelatins mediated redox homeostasis and stress signal transduction in plants: an integrated overview. In: Ahmad P (ed) Plant metal interaction, emerging remediation techniques. Elsevier Amsterdam, Netherlands, pp 285–310CrossRefGoogle Scholar
  79. Singh VK, Upadhyay RS (2014) Effects of arsenic on reactive oxygen species and antioxidant defense system in tomato plants. Toxicol Environ Chem 96(9):13741383CrossRefGoogle Scholar
  80. Smith IK, Vierhaller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5-dithiobis (2-nitrobenzoic acid). Anal Biochem 175:408–413CrossRefGoogle Scholar
  81. Soares C, Branco-Neves S, de Sousa A, Teixeira J, Pereira R, Fidalgo F (2018a) Can nano-SiO2 reduce the phytotoxicity of acetaminophen?—a physiological, biochemical and molecular approach. Environ Pollut 241:900–911CrossRefGoogle Scholar
  82. Soares C, Branco-Neves S, de Sousa A, Azenha M, Cunha A, Pereira R, Fidalgo F (2018b) SiO2 nanomaterial as a tool to improve Hordeum vulgare L. tolerance to nano-NiO stress. Sci Total Environ 622:517–525CrossRefGoogle Scholar
  83. Soares C, Carvalho ME, Azevedo RA, Fidalgo F (2018c) Plants facing oxidative challenges-a little help from the antioxidant networks. Environ Exp Bot.
  84. Spagnoletti FN, Balestrasse K, Lavado RS, Giacometti R (2016) Arbuscular mycorrhiza detoxifying response against arsenic and pathogenic fungus in soybean. Ecotoxicol Environ Safety 133:47–56CrossRefGoogle Scholar
  85. Srivastava S, Sharma YK (2013) Arsenic phytotoxicity in black gram (Vigna mungo L. Var. PU19) and its possible amelioration by phosphate application. J Plant Physiol Pathol 1:3Google Scholar
  86. Stoeva N, Berova M, Zlatev Z (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Plantarum 49:293–296CrossRefGoogle Scholar
  87. Tale Ahmad S, Haddad R (2011) Study of silicon effects on antioxidant enzyme activities and osmotic adjustment of wheat under drought stress. Czech J Genet Plant Breed 47(1):17–27CrossRefGoogle Scholar
  88. Talukdar D (2013a) Arsenic induced changes in growth and antioxidant metabolism of fenugreek. Russ J Plant Physiol 60:652–660CrossRefGoogle Scholar
  89. Talukdar D (2013b) Arsenic-induced oxidative stress in the common bean legume, Phaseolus vulgaris L. seedlings and its amelioration by exogenous nitric oxide. Physiol Mol Biol Plants 19(1):69–79CrossRefGoogle Scholar
  90. Tang T, Miller DM (1991) Growth and tissue composition of rice grown in soil treated with inorganic copper, nickel, and arsenic. Commun Sci Plant Anal 22:19–12Google Scholar
  91. Tiwari S, Sarangi BK (2015) Arsenic and chromium-induced oxidative stress in metal accumulator and nonaccumulator plants and detoxification mechanisms. In: Dharmendra G, Palma JM, Corpas FJ (eds), Reactive oxygen species and oxidative damage in plants under stress, Springer International Publishing, Switzerland, pp-165-182Google Scholar
  92. Tripathi P, Tripathi RD, Singh RP, Dwivedi S, Goutam D, Shri M, Trivedi PK, Chakrabarty D (2013) Silicon mediates arsenic tolerance in rice (Oryza sativa L.) through lowering of arsenic uptake and improved antioxidant defence system. Ecolo Eng 52:96–103CrossRefGoogle Scholar
  93. Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJ (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotech 25:158–165CrossRefGoogle Scholar
  94. Turnau K, Henriques FS, Anielska T, Renker C, Buscot F (2007) Metal uptake and detoxification mechanisms in Erica andevalensis growing in a pyrite mine tailing. Environ Exp Bot 61:117–123CrossRefGoogle Scholar
  95. Upadhyaya H, Shome S, Roy D, Bhattacharya MK (2014) Arsenic induced changes in growth and physiological responses in Vigna radiata seedling: effect of curcumin interaction. Amer J Plant Sci 5:3609–3618CrossRefGoogle Scholar
  96. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidative systems in acid rain treated bean plants. Plant Sci 151:59–66CrossRefGoogle Scholar
  97. Yadav RK, Srivastava SK (2015) Effect of arsenite and arsenate on lipid peroxidation, enzymatic and non-enzymatic antioxidants in Zea mays Linn. Biochem Physiol 4:186. CrossRefGoogle Scholar
  98. Yu Y, Zhang S, Huang H, Luo L, Wen B (2009) Arsenic accumulation and speciation in maize as affected by inoculation with arbuscular mycorrhizal fungus Glomus mosseae. J Agric Food Chem 57(9):3695–3701CrossRefGoogle Scholar
  99. Zhang J, Martinoia E, Lee Y (2018) Vacuolar transporters for cadmium and arsenic in plants and their applications in phytoremediation and crop development. Plant Cell PhysiolGoogle Scholar
  100. Zhao F-J, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Ann Rev Plant Biol 61:535–559CrossRefGoogle Scholar
  101. Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 164:527–533CrossRefGoogle Scholar
  102. Zhu YG, Yoshinaga M, Zhao FJ, Rosen BP (2014) Earth abides arsenic biotransformations. Annu Rev Earth Planet Sci 42:443–467CrossRefGoogle Scholar
  103. Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Picea mariana). Can J For Res 21:401–404CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of BotanyPanjab UniversityChandigarhIndia

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