Role of Micro-organisms in Modulating Antioxidant Defence in Plants Exposed to Metal Toxicity

  • Kanika Khanna
  • Sukhmeen Kaur Kohli
  • Shagun Bali
  • Parminder Kaur
  • Poonam Saini
  • Palak Bakshi
  • Puja Ohri
  • Bilal Ahmad Mir
  • Renu Bhardwaj


Micro-organisms play diverse role rhizosphere where they interact and develop mutualistic associations. They stimulate plant growth by synthesising various metabolites and phytohormones like auxins (IAA), cytokinins and gibberellins etc. They also help to alleviate the oxidative stress induced by heavy metals by lowering the free radical formation and activation of different antioxidants and antioxidative enzymes (SOD, APOX, CAT, GR, POD, MDHAR, GPX etc.). Furthermore, they modulate the activity of ROS- scavenging pathways and maintain ROS homeostasis thereby, averts ROS- initiated inhibition of plant cellular processes and enhance their survival under metal stress. Moreover, they elevate redox state of plants by increasing the activities of ascorbate-glutathione recycling enzymes under metal stress. They also alter the levels of organic acids, phenols, flavonoids and siderophores which act as a part of metal detoxification and antioxidative defence system in metal-stressed plants. Plant- microbe symbiosis enables accumulation of stress-responsive phytohormones and trigger antioxidative defence responsive genes which enhance overall survival of plants under metal stress.


Oxidative damage Reactive oxygen species Antioxidative defense Phenolic compounds Siderophore production Organic acid production 


  1. Abadi VAJM, Sepehri M (2016) Effect of Piriformospora indica and Azotobacter chroococcum on mitigation of zinc deficiency stress in wheat (Triticum aestivum L.). Symbiosis 69:9–19CrossRefGoogle Scholar
  2. Abd-Alla MH, Khalil Bagy M, El-enany AWE, Bashandy SR (2014a) Activation of Rhizobium tibeticum with flavonoid enhances nodulation, nitrogen fixation and growth of fenugreek (Trignoella foenum-graecum L.) grown in cobalted-polluted soil. Arch Environ Contam Toxicol 66:303–315PubMedCrossRefGoogle Scholar
  3. Abd-Alla MH, Bashandy SR, Bagy MK, El-enany AWE (2014b) Rhizobium tibeticum activated with a mixture of flavonoids alleviates nickel toxicity in symbiosis with fenugreek (Trigonella foenumgraecum L). Ecotoxicology 23:946–959PubMedCrossRefGoogle Scholar
  4. Abdel-Lateif K, Bogusz D, Hocher V (2012) The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal Behav 7:636–641PubMedPubMedCentralCrossRefGoogle Scholar
  5. Ahmad A, Hadi F, Ali N (2015a) Effective phytoextraction of cadmium (Cd) with increasing concentration of total phenolics and free proline in Cannabis sativa (L) plant under various treatments of fertilizers, plant growth regulators and sodium salt. Int J Phytoremediation 17:56–65PubMedCrossRefGoogle Scholar
  6. Ahmad P, Hashem A, Abd-Allah EF, Alqarawi AA, John R, Egamberdieva D, Gucel S (2015b) Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L.) through antioxidative defense system. Front Plant Sci 6:868PubMedPubMedCentralGoogle Scholar
  7. Ahmad P, Latef AAA, Abd_Allah EF, Hashem A, Sarwat M, Anjum NA, Gucel S (2016a) Calcium and potassium supplementation enhanced growth, osmolyte secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Front Plant Sci 7:513PubMedPubMedCentralGoogle Scholar
  8. Ahmad S, Tabassum H, Alam A (2016b) Role of microbial bioremediation of heavy metal from contaminated soils: an update. Int J Biol Pharm Allied Sci 5:1605–1622Google Scholar
  9. Akram NA, Shafiq F, Ashraf M (2017) Ascorbic acid-A potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front Plant Sci 8:613PubMedPubMedCentralCrossRefGoogle Scholar
  10. Aloui A, Dumas-Gaudot E, Daher Z, Tuinen D, Aschi-Smit S, Morandi D (2012) Influence of arbuscular mycorrhizal colonisation on cadmium induced Medicago truncatula root isoflavonoid accumulation. Plant Physiol Biochem 60:233–239PubMedCrossRefGoogle Scholar
  11. Amal-Ghamdi AMAL, Jais HM (2012) Interaction between arbuscular mycorrhiza and heavy metals in the rhizosphere and roots of Juniperus procera. Int J Agri Biol 14(1)Google Scholar
  12. Andrade SAL, Gratao PL, Azevedo RA, Silveira APD, Schiavinato MA, Mazzafera P (2010) Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. Environ Exp Bot 68:198–207CrossRefGoogle Scholar
  13. Andrews M, Cripps MG, Edwards GR (2012) The potential of beneficial microorganisms in agricultural systems. Ann Appl Biol 160:1–5CrossRefGoogle Scholar
  14. Arao T, Ishikawa S, Murakami M, Abe K, Maejima Y, Makino T (2010) Heavy metal contamination of agricultural soil and countermeasures in Japan. Paddy Water Environ 8:247–257CrossRefGoogle Scholar
  15. Arora A, Byrem TM, Nair MG, Strasburg GM (2000) Modulation of liposomal membrane fluidity by flavonoids and isoflavonoids. Arch Biochem Biophys 373:102–109CrossRefGoogle Scholar
  16. Azevedo RA, Gratao PL, Monteiro CC, Carvalho RF (2012) What is new in the research on cadmium‐induced stress in plants? Food Energy Secur 1(2):133–140Google Scholar
  17. Bano SA, Ashfaq D (2013) Role of mycorrhiza to reduce heavy metal stress. Nat Sci 5:16Google Scholar
  18. Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34CrossRefGoogle Scholar
  19. Bhaduri AM, Fulekar MH (2012) Assessment of arbuscular mycorrhizal fungi on the phytoremediation potential of Ipomoea aquatica on cadmium uptake. 3. Biotech 2:193–198Google Scholar
  20. Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transducation in plants. Curr Sci 89:1113–1121Google Scholar
  21. Bilal S, Khan AL, Shahzad R, Asaf S, Kang SM, Lee IJ (2017) Endophytic Paecilomyces formosus LHL10 augments Glycine max L. Adaptation to Ni-contamination through affecting endogenous phytohormones and oxidative stress. Front Plant Sci 8:870PubMedPubMedCentralCrossRefGoogle Scholar
  22. Borsetti F, Tremaroli V, Michelacci F, Borghese R, Winterstein C, Daldal F, Zannoni D (2005) Tellurite effects on Rhodobacter capsulatus cell viability and superoxide dismutase activity under oxidative stress conditions. Res Microbiol 156:807–813PubMedCrossRefGoogle Scholar
  23. Braud A, Hoegy F, Jezequel K, Lebeau T, Schalk IJ (2009a) New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine–iron uptake pathway. Environ Microbiol 11:1079–1091PubMedCrossRefGoogle Scholar
  24. Braud A, Jézéquel K, Bazot S, Lebeau T (2009b) Enhanced phytoextraction of an agricultural Cr-and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286PubMedCrossRefGoogle Scholar
  25. Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52:98–111PubMedCrossRefGoogle Scholar
  26. Cao YR, Zhang XY, Deng JY, Zhao QQ, Xu H (2012) Lead and cadmium-induced oxidative stress impacting mycelial growth of Oudemansiella radicata in liquid medium alleviated by microbial siderophores. World J Microbiol Biotechnol 28:1727–1737PubMedCrossRefGoogle Scholar
  27. Cao S, Wang W, Wang F, Zhang J, Wang Z, Yang S, Xue Q (2016) Drought-tolerant Streptomyces pactum Act12 assist phytoremediation of cadmium-contaminated soil by Amaranthus hypochondriacus: great potential application in arid/semi-arid areas. Environ Sci Pollut Res 23:14898–14907CrossRefGoogle Scholar
  28. Chen YX, Wang YP, Lin Q, Luo YM (2005) Effect of copper-tolerant rhizosphere bacteria on mobility of copper in soil and copper accumulation by Elsholtzia splendens. Environ Int 31:861–866PubMedCrossRefPubMedCentralGoogle Scholar
  29. Cohen MF, Sakihama Y, Yamasaki H (2001) Roles of plant flavonoids in interactions with microbes: from protection against pathogens to the mediation of mutualism. TC 2:157–173Google Scholar
  30. Cooper JE (2004) Multiple responses of rhizobia to flavonoids during legume root infection. Adv Bot Res 41:1–62CrossRefGoogle Scholar
  31. DalCorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 6:663–667CrossRefGoogle Scholar
  32. D'Autréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8:813PubMedCrossRefPubMedCentralGoogle Scholar
  33. Delvasto P, Ballester A, Muñoz JA, González F, Blázquez ML, Igual JM, Valverde A, García-Balboa C (2009) Mobilization of phosphorus from iron ore by the bacterium Burkholderia caribensis FeGL03. Miner Eng 22:1–9CrossRefGoogle Scholar
  34. Denarie J, Debelle F, Prome JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535PubMedCrossRefPubMedCentralGoogle Scholar
  35. Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E (2009a) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162CrossRefGoogle Scholar
  36. Dimkpa C, Weinand T, Asch F (2009b) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694PubMedCrossRefGoogle Scholar
  37. Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E (2009c) Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 107:1687–1696PubMedCrossRefPubMedCentralGoogle Scholar
  38. Dourado MN, Martins PF, Quecine MC, Piotto FA, Souza LA, Franco MR, Tezotto T, Azevedo R (2013) Burkholderia sp SCMS54 reduces cadmium toxicity and promotes growth in tomato. Ann Appl Biol 165:494–507Google Scholar
  39. Farshian SJK, Malekzadeh P (2007) Effect of arbuscular mycorrhizal (G. etunicatum) fungus on antioxidant enzymes activity under zinc toxicity in lettuce plants. Pak J Biol Sci 10:1865–1869Google Scholar
  40. Fasim F, Ahmed N, Parsons R, Gadd GM (2002) Solubilization of zinc salts by a bacterium isolated from the air environment of a tannery. FEMS Microbiol Lett 213:1–6PubMedCrossRefPubMedCentralGoogle Scholar
  41. Fomina MA, Alexander IJ, Colpaert JV, Gadd GM (2005) Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biol Biochem 37:851–866CrossRefGoogle Scholar
  42. 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
  43. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905PubMedCrossRefPubMedCentralGoogle Scholar
  44. 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
  45. Fuentes A, Almonacid L, Ocampo JA, Arriagada C (2016) Synergistic interactions between a saprophytic fungal consortium and Rhizophagus irregularis alleviate oxidative stress in plants grown in heavy metal contaminated soil. Plant Soil 407:355–366CrossRefGoogle Scholar
  46. Gao Y, Miao C, Mao L, Zhou P, Jin Z, Shi W (2010) Improvement of phytoextraction and antioxidative defense in L. under cadmium stress by application of cadmium-resistant strain and citric acid. J Hazard Mater 181:771–777PubMedCrossRefPubMedCentralGoogle Scholar
  47. Gao Y, Miao C, Xia J, Luo C, Mao L, Zhou P, Shi W (2012) Effect of citric acid on phytoextraction and antioxidative defense in Solanum nigrum L. as a hyperaccumulator under Cd and Pb combined pollution. Earth Sci 65:1923–1932Google Scholar
  48. Garg N, Aggarwal N (2011) Effects of interactions between cadmium and lead on growth, nitrogen fixation, phytochelatin, and glutathione production in mycorrhizal Cajanus cajan (L.) Millsp. J Plant Growth Regul 30:286–300CrossRefGoogle Scholar
  49. Garg N, Aggarwal N (2012) Effect of mycorrhizal inoculations on heavy metal uptake and stress alleviation of Cajanus cajan (L.) Millsp. genotypes grown in cadmium and lead contaminated soils. Plant Growth Regul 66:9–26CrossRefGoogle Scholar
  50. Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. A review. Agron Sustain Dev 30:581–599CrossRefGoogle Scholar
  51. Garg N, Kaur H (2013) Impact of cadmium-zinc interactions on metal uptake, translocation and yield in pigeonpea genotypes colonized by arbuscular mycorrhizal fungi. J Plant Nutr 36:67–90CrossRefGoogle Scholar
  52. Gill M (2014) Heavy metal stress in plants: a review. Int J Adv Res 2:1043–1055Google Scholar
  53. Gill SS, Khan NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182:112–120Google Scholar
  54. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedCrossRefPubMedCentralGoogle Scholar
  55. Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  56. Gratao PL, Monteiro CC, Peres LEP, Azevedo RA (2008) The isolation of antioxidant enzymes from mature tomato (cv. Micro-Tom) plants. Hortic Sci 43:1608–1610Google Scholar
  57. Gratao PL, Monteiro CC, Rossi ML, Martinelli AP, Peres LEP, Medici LO, Lea PJ, Azevedo RA (2009) Differential ultrastructural changes in tomato hormonal mutants exposed to cadmium. Environ Exp Bot 67:387–394CrossRefGoogle Scholar
  58. Greaney KM (2005) An assessment of heavy metal contamination in the marine sediments of Las Perlas Archipelago, Gulf of Panama. School of Life Sci Heriot-Watt University, EdinburghGoogle Scholar
  59. Guarino C, Sciarrillo R (2017) Effectiveness of in situ application of an Integrated Phytoremediation System (IPS) by adding a selected blend of rhizosphere microbes to heavily multi-contaminated soils. Ecol Eng 99:70–82CrossRefGoogle Scholar
  60. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322PubMedPubMedCentralCrossRefGoogle Scholar
  61. Han F, Shan X, Zhang S, Wen B, Owens G (2006) Enhanced cadmium accumulation in maize roots—the impact of organic acids. Plant Soil 289:355–368CrossRefGoogle Scholar
  62. 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 23:272–281PubMedCrossRefPubMedCentralGoogle Scholar
  63. Hassan W, Bano R, Bashir F, David J (2014) Comparative effectiveness of ACC-deaminase and/or nitrogen-fixing rhizobacteria in promotion of maize (Zea mays L.) growth under lead pollution. Environ Sci Pollut Res 21:10983–10996CrossRefGoogle Scholar
  64. Hassan W, Bashir S, Ali F, Ijaz M, Hussain M, David J (2016) Role of ACC-deaminase and/or nitrogen fixing rhizobacteria in growth promotion of wheat (Triticum aestivum L.) under cadmium pollution. Environ Earth Sci 75:267CrossRefGoogle Scholar
  65. Higdon JV, Frei B (2003) Tea catechins and polyphenols: health effects, metabolism, and antioxidant functions. Crit Rev Food Sci Nutr 43:89–143CrossRefGoogle Scholar
  66. Hristozkova M, Geneva M, Stancheva I, Boychinova M, Djonova E (2016) Contribution of arbuscular mycorrhizal fungi in attenuation of heavy metal impact on Calendula officinalis development. Appl Soil Ecol 101:57–63CrossRefGoogle Scholar
  67. Huang WY, Cai YZ, Xing J, Corke H, Sun M (2007) A potential antioxidant resource: endophytic fungi from medicinal plants. Econ Bot 61:14–30CrossRefGoogle Scholar
  68. Huffmeyer N, Klasmeier J, Matthies M (2009) Geo-referenced modeling of zinc concentrations in the Ruhr river basin (Germany) using the model GREAT-ER. Sci Total Environ 407:2296–2305PubMedCrossRefGoogle Scholar
  69. Ibiang YB, Mitsumoto H, Sakamoto K (2017) Bradyrhizobia and arbuscular mycorrhizal fungi modulate manganese, iron, phosphorus, and polyphenols in soybean (Glycine max (L.) Merr.) under excess zinc. Environ Exp Bot 137:1–13CrossRefGoogle Scholar
  70. Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597PubMedCrossRefGoogle Scholar
  71. Islam F, Yasmeen T, Riaz M, Arif M, Ali S, Raza SH (2014a) Proteus mirabilis alleviates zinc toxicity by preventing oxidative stress in maize (Zea mays) plants. Ecotoxicol Environ Saf 110:143–152PubMedCrossRefGoogle Scholar
  72. Islam F, Yasmeen T, Ali Q, Ali S, Arif MS, Hussain S, Rizvi H (2014b) Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol Environ Saf 10:285–293CrossRefGoogle Scholar
  73. Islam F, Yasmeen T, Arif MS, Riaz M, Shahzad SM, Imran Q, Ali I (2016a) Combined ability of chromium (Cr) tolerant plant growth promoting bacteria (PGPB) and salicylic acid (SA) in attenuation of chromium stress in maize plants. Plant Physiol Biochem 108:456–467PubMedCrossRefGoogle Scholar
  74. Islam F, Yasmeen T, Ali Q, Mubin M, Ali S, Arif MS, Hussain S, Riaz M, Abbas F (2016b) Copper-resistant bacteria reduces oxidative stress and uptake of copper in lentil plants: potential for bacterial bioremediation. Environ Sci Pollut Res 23:220–233CrossRefGoogle Scholar
  75. Janmohammadi M, Bihamta MR, Ghasemzadeh F (2013) Influence of rhizobacteria inoculation and lead stress on the physiological and biochemical attributes of wheat genotypes. Cercetări Agronomice Moldova 46:153Google Scholar
  76. Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182PubMedCrossRefGoogle Scholar
  77. Jiang Q-Y, Zhuo F, Long S-H, Zhao H-D, Yang D-J, Ye Z-H, Li S-S, Jing Y-X (2016) Can arbuscular mycorrhizal fungi reduce cd uptake and alleviate cd toxicity of Lonicera japonica grown in cd-added soils? Sci Rep 6(1)Google Scholar
  78. Jiang QY, Zhuo F, Long SH, Zhao HD, Yang DJ, Ye ZH, Li SS, Jing YX (2016a) Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Sci Rep 6:21805PubMedPubMedCentralCrossRefGoogle Scholar
  79. Jiang QY, Tan SY, Zhuo F, Yang DJ, Ye ZH, Jing YX (2016b) Effect of Funneliformis mosseae on the growth, cadmium accumulation and antioxidant activities of Solanum nigrum. Appl Soil Ecol 98:112–120CrossRefGoogle Scholar
  80. Jones DL (1998) Organic acids in the rhizosphere–a critical review. Plant Soil 205:25–44CrossRefGoogle Scholar
  81. Jones DL, Prabowo AM, Kochian LV (1996) Kinetics of malate transport and decomposition in acid soils and isolated bacterial populations: the effect of microorganisms on root exudation of malate under Al stress. Plant Soil 182:239–247CrossRefGoogle Scholar
  82. Jones DL, Dennis PG, Owen AG, Van Hees PAW (2003) Organic acid behavior in soils–misconceptions and knowledge gaps. Plant Soil 248:31–41CrossRefGoogle Scholar
  83. 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(3):3145–3175Google Scholar
  84. Kang J, Choi MS, Yi HI, Song YH, Lee D, Cho JH (2011) A five-year observation of atmospheric metals on Ulleung Island in the East/Japan Sea: temporal variability and source identification. Atmos Environ 45:4252–4262CrossRefGoogle Scholar
  85. Kang SM, Radhakrishnan R, You YH, Khan AL, Lee KE, Lee JD, Lee IJ (2015) Enterobacter asburiae KE17 association regulates physiological changes and mitigates the toxic effects of heavy metals in soybean. Plant Biol 17:1013–1022PubMedCrossRefGoogle Scholar
  86. Karthik C, Oves M, Thangabalu R, Sharma R, Santhosh SB, Arulselvi PI (2016) Cellulosimi crobium fungi-like enhances the growth of Phaseolus vulgaris by modulating oxidative damage under Chromium (VI) toxicity. J Adv Res 7:839–850PubMedPubMedCentralCrossRefGoogle Scholar
  87. Keunen E, Remans T, Bohler S, Vangronsveld J, Cuypers A (2011) Metal-induced oxidative stress and plant mitochondria. Int J Mol Sci 12:6894–6918PubMedPubMedCentralCrossRefGoogle Scholar
  88. Khan MS, Wani AZPA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19CrossRefGoogle Scholar
  89. Khan AR, Ullah I, Khan AL, Park GS, Waqas M, Hong SJ, Jung BK, Kwak Y, Lee IJ, Shin JH (2015) Improvement in phytoremediation potential of Solanum nigrum under cadmium contamination through endophytic-assisted Serratia sp. RSC-14 inoculation. Environ Sci Pollut Res 22:14032–14042CrossRefGoogle Scholar
  90. Khodadoust AP, Reddy KR, Maturi K (2004) Removal of nickel and phenanthrene from kaolin soil using different extractants. Environ Eng Sci 21:691–704CrossRefGoogle Scholar
  91. Kibria G (2014) Trace metals/heavy metals and its impact on environment, biodiversity and human health – a short review.
  92. Kim DY, Bovet L, Kushnir S, Woon Noh E, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932PubMedPubMedCentralCrossRefGoogle Scholar
  93. Kohli S, Poonam K, Bali S, Kaur H, Bhardwaj R (2013) Analysis of ameliorative effects of 24-EBL on growth characteristics, photosynthetic pigment cascade and metal uptake of 60 day old plants of B. juncea plants under Cu metal stress. Biospectra 8:147–154Google Scholar
  94. Kohli SK, Handa N, Sharma A, Gautam V, Arora S, Bhardwaj R, Nasser Alyemeni M, Wijaya L, Ahmad P (2017) Combined effect of 24-epibrassinolide and salicylic acid mitigates lead (Pb) toxicity by modulating various metabolites in Brassica juncea L. seedlings. Protoplasma 2017:1–14Google Scholar
  95. Kong Z, Glick BR, Duan J, Ding S, Tian J, McConkey BJ, Wei G (2015) Effects of 1-aminocyclopropane-1-carboxylate (ACC) deaminase-overproducing Sinorhizobium meliloti on plant growth and copper tolerance of Medicago lupulina. Plant Soil 391:383–398CrossRefGoogle Scholar
  96. Kopittke PM, Blamey FPC, Menzies NW (2010) Toxicity of Cd to signal grass (Brachiaria decumbens Stapf.) and Rhodes grass (Chloris gayana Kunth.). Plant Soil 330:515–523CrossRefGoogle Scholar
  97. Kowalski A, Siepak M, Boszke L (2007) Mercury contamination of surface and ground waters of Poznań, Poland. Pol J Environ Stud 16:67–74Google Scholar
  98. Li WC, Ye ZH, Wong MH (2010) Metal mobilization and production of short-chain organic acids by rhizosphere bacteria associated with a Cd/Zn hyperaccumulating plant, Sedum alfredii. Plant Soil 326:453–467CrossRefGoogle Scholar
  99. Li Y, Yang R, Zhang A, Wang S (2014) The distribution of dissolved lead in the coastal waters of the East China Sea. Mar Pollut Bull 85:700–709PubMedCrossRefGoogle Scholar
  100. Li JF, He XH, Li H, Zheng WJ, Li JF, Wang MY (2015a) Arbuscular mycorrhizal fungi increase growth and phenolics synthesis in Poncirus trifoliata under iron deficiency. Sci Hortic 183:87–92CrossRefGoogle Scholar
  101. Li P, Lin C, Cheng H, Duan X, Lei K (2015b) Contamination and health risks of soil heavy metals around a lead/zinc smelter in south western China. Ecotoxicol Environ Saf 113:391–399PubMedCrossRefGoogle Scholar
  102. Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37PubMedCrossRefGoogle Scholar
  103. Ma Y, Rajkumar M, Vicente JAF, Freitas H (2010) Inoculation of Ni-resistant plant growth promoting bacterium Psychrobacter sp. strain SRS8 for the improvement of nickel phytoextraction by energy crops. Int J Phytoremediation 13:126–139CrossRefGoogle Scholar
  104. Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011a) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258PubMedCrossRefGoogle Scholar
  105. Ma Y, Rajkumar M, Luo YM, Freitas H (2011b) Inoculation of endophytic bacteria on host and non-host plants—effects on plant growth and Ni uptake. J Hazard Mater 195:230–237PubMedCrossRefGoogle Scholar
  106. Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25CrossRefGoogle Scholar
  107. Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69:220–228PubMedCrossRefGoogle Scholar
  108. Mahmud JA, Hasanuzzaman M, Nahar K, Rahman A, Hossain MS, Fujita M (2017) Maleic acid assisted improvement of metal chelation and antioxidant metabolism confers chromium tolerance in Brassica juncea L. Ecotoxicol Environ Saf 144:216–226PubMedCrossRefGoogle Scholar
  109. Maksymiec W, Wojcik M, Krupa Z (2007) Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere 66:421–427PubMedCrossRefGoogle Scholar
  110. Malinowski DP, Belesky DP (2006) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassl Sci 52:1–14CrossRefGoogle Scholar
  111. Márquez-García B, Fernández-Recamales M, Córdoba F (2012) Effects of cadmium on phenolic composition and antioxidant activities of Erica andevalensis. J Bot 6Google Scholar
  112. Martin JAR, Ramos-Miras JJ, Boluda R, Gil C (2013) Spatial relations of heavy metals in arable and greenhouse soils of a Mediterranean environment region (Spain). Geoderma 200:180–188CrossRefGoogle Scholar
  113. Martino E, Perotto S, Parsons R, Gadd GM (2003) Solubilization of insoluble inorganic zinc compounds by ericoid mycorrhizal fungi derived from heavy metal polluted sites. Soil Biol Biochem 35:133–141CrossRefGoogle Scholar
  114. Mendoza-Cozatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562PubMedPubMedCentralCrossRefGoogle Scholar
  115. Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15:523–530Google Scholar
  116. Mierziak J, Kostyn K, Kulma A (2014) Flavonoids as important molecules of plant interactions with the environment. Molecules 19:16240–16265PubMedCrossRefGoogle Scholar
  117. Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefPubMedCentralGoogle Scholar
  118. Mohod CV, Dhote J (2013) Review of heavy metals in drinking water and their effect on human health. Int J Innovat Res Sci Engin Technol 2:2992–2996Google Scholar
  119. Mollavali M, Bolandnazar SA, Schwarz D, Rohn S, Riehle P, Nahandi FZ (2016) Flavonol glucoside, antioxidant enzyme biosynthesis affected by mycorrhizal fungi in various cultivars of onion (Allium cepa L.). J Agr Food Fhem 64:71–77CrossRefGoogle Scholar
  120. Mukherjee A, Sengupta MK, Hossain MA, Ahamed S, Das B, Nayak B, Lodh D, Rahman MM, Chakraborti D (2006) Arsenic contamination in groundwater: a global perspective with emphasis on the Asian scenario. J Health Popul Nutr 24:142–163PubMedPubMedCentralGoogle Scholar
  121. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence, toxicity for plants: a review. Environ Chem Lett 8:199–216CrossRefGoogle Scholar
  122. Nell M, Voetsch M, Vierheilig H, Steinkellner S, Zitterl-Eglseer K, Franz C, Novak J (2009) Effect of phosphorus uptake on growth and secondary metabolites of garden sage (Salvia officinalis L.). J Sci Food Agric 89:1090–1096CrossRefGoogle Scholar
  123. Nordstrom DK (2002) Worldwide occurrences of arsenic in ground water. Science 296:2143–2145PubMedCrossRefPubMedCentralGoogle Scholar
  124. Ovečka M, Takáč T (2014) Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv 32:73–86PubMedCrossRefPubMedCentralGoogle Scholar
  125. Oves M, Khan MS, Qari AH, Felemban MN, Almeelbi T (2016) Heavy metals: biological importance and detoxification strategies. J Bioremed Biodegr 7:2Google Scholar
  126. Pandey S, Barai PK, Maiti TK (2013) Influence of heavy metals on the activity of antioxidant enzymes in the metal resistant strains of Ochrobactrum and Bacillus sp. J Environ Biol 34:1033PubMedPubMedCentralGoogle Scholar
  127. Panfili F, Schneider A, Vives A, Perrot F, Hubert P, Pellerin S (2009) Cadmium uptake by durum wheat in presence of citrate. Plant Soil 316:299–309CrossRefGoogle Scholar
  128. Pinter IF, Salomon MV, Berli F, Bottini R, Piccoli P (2017) Characterization of the As (III) tolerance conferred by plant growth promoting rhizobacteria to in vitro-grown grapevine. Appl Soil Ecol 109:60–68CrossRefGoogle Scholar
  129. Poyart C, Quesne G, Trieu-Cuot P (2002) Taxonomic dissection of the Streptococcus bovis group by analysis of manganese-dependent superoxide dismutase gene (sodA) sequences: reclassification of ‘Streptococcus infantarius subsp. coli’as Streptococcus lutetiensis sp. nov. and of Streptococcus bovis biotype 11.2 as Streptococcus pasteurianus sp. nov. Int J Syst Evol Microbiol 52:1247–1255PubMedGoogle Scholar
  130. Prasad MNV, Freitas H, Fraenzle S, Wuenschmann S, Markert B (2010) Knowledge explosion in phytotechnologies for environmental solutions. Environ Pollut 158:18–23PubMedCrossRefGoogle Scholar
  131. Rajkumar U, Reddy BLN, Rajaravindra KS, Niranjan M, Bhattacharya TK, Chatterjee RN, Sharma RP (2010) Effect of naked neck gene on immune competence, serum biochemical and carcass traits in chickens under a tropical climate. Asian-Australas J Anim Sci 23:867–872CrossRefGoogle Scholar
  132. Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574PubMedCrossRefGoogle Scholar
  133. Ray S, Singh V, Singh S, Sarma BK, Singh HB (2016) Biochemical and histochemical analyses revealing endophytic Alcaligenes faecalis mediated suppression of oxidative stress in Abelmoschus esculentus challenged with Sclerotium rolfsii. Plant Physiol Biochem 109:430–441PubMedCrossRefPubMedCentralGoogle Scholar
  134. Reddy AM, Reddy VS, Scheffler BE, Wienand U, Reddy AR (2007) Novel transgenic rice overexpressing anthocyanidin synthase accumulates a mixture of flavonoids leading to an increased antioxidant potential. Metab Eng 9:95–111PubMedCrossRefPubMedCentralGoogle Scholar
  135. Roychoudhury A, Basu S, Sengupta DN (2012) Antioxidants and stress-related metabolites in the seedlings of two indica rice varieties exposed to cadmium chloride toxicity. Acta Physiol Plant 34:835–847CrossRefGoogle Scholar
  136. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Biol 52:527–560CrossRefGoogle Scholar
  137. Sahoo RK, Ansari MW, Pradhan M, Dangar TK, Mohanty S, Tuteja N (2014a) A novel Azotobacter vinellandii (SRI Az 3) functions in salinity stress tolerance in rice. Plant Sig Behav 9:511–523Google Scholar
  138. Sahoo RK, Ansari MW, Dangar TK, Mohanty S, Tuteja N (2014b) Phenotypic and molecular characterisation of efficient nitrogen-fixing azotobacter strains from rice fields for crop improvement. Protoplasma 251:511–523PubMedCrossRefPubMedCentralGoogle Scholar
  139. Saravanan VS, Madhaiyan M, Thangaraju M (2007) Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66(9):1794–1798Google Scholar
  140. Saravanakumar D, Vijayakumar C, Kumar N, Samiyappan R (2007) PGPR-induced defense responses in the tea plant against blister blight disease. Crop Prot 26:556–565CrossRefGoogle Scholar
  141. Sayadi MH (2014) Impact of land use on the distribution of toxic metals in surface soils in Birjand city, Iran. Proc Int Acad Ecol Environ Sci 4:18Google Scholar
  142. Sayer JA, Cotter-Howells JD, Watson C, Hillier S, Gadd GM (1999) Lead mineral transformation by fungi. Curr Biol 9:691–694PubMedCrossRefPubMedCentralGoogle Scholar
  143. Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014PubMedCrossRefPubMedCentralGoogle Scholar
  144. Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854PubMedCrossRefPubMedCentralGoogle Scholar
  145. Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365PubMedPubMedCentralGoogle Scholar
  146. Seshadri B, Bolan NS, Naidu R (2015) Rhizosphere-induced heavy metal (loid) transformation in relation to bioavailability and remediation. J Soil Sci Plant Nutr 15:524–548Google Scholar
  147. Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35:334–346PubMedCrossRefPubMedCentralGoogle Scholar
  148. Seyoum A, Asres K, El-Fiky FK (2006) Structure–radical scavenging activity relationships of flavonoids. Phytochemistry 67:2058–2070PubMedCrossRefPubMedCentralGoogle Scholar
  149. Shahabivand S, Maivan HZ, Mahmoudi E, Soltani BM, Sharifi M, Aliloo AA (2016) Antioxidant activity and gene expression associated with cadmium toxicity in wheat affected by mycorrhizal fungus. Žemdirbystė (Agric) 103:53–60Google Scholar
  150. Shanker A, Cervantes KC, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753PubMedCrossRefPubMedCentralGoogle Scholar
  151. Sharma A, Johri BN (2003) Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.)under iron limiting conditions. Microbiol Res 158:243–248Google Scholar
  152. Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50PubMedCrossRefGoogle Scholar
  153. Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 26:2027–2038PubMedCrossRefGoogle Scholar
  154. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Aust J Bot 2012:1–26Google Scholar
  155. Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170PubMedCrossRefPubMedCentralGoogle Scholar
  156. Shi P, Zhu K, Zhang Y, Chai T (2016) Growth and cadmium accumulation of Solanum nigrum L. seedling were enhanced by heavy metal-tolerant strains of Pseudomonas aeruginosa. Water Air Soil Pollut 227:459CrossRefGoogle Scholar
  157. Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254CrossRefGoogle Scholar
  158. Sinha S, Mukherjee SK (2008) Cadmium–induced siderophore production by a high Cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Curr Microbiol 56:55–60PubMedCrossRefGoogle Scholar
  159. Smirnoff N (2000a) Ascorbate biosynthesis and function in photoprotection. Philos Trans Royal Soc Lond Ser B, Biol Sci 355:1455–1464CrossRefGoogle Scholar
  160. Smirnoff N (2000b) Ascorbic acid: metabolism and functions of a multifaceted molecule. Curr Opin Plant Biol 3:229–235PubMedCrossRefGoogle Scholar
  161. Sousa NR, Ramos MA, Marques APGC, Castro PML (2012) The effect of ectomycorrhizal fungi forming symbiosis with Pinus pinaster seedlings exposed to cadmium. Sci Total Environ 414:63–67PubMedCrossRefGoogle Scholar
  162. Su C (2014) A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environ Skeptics Critic 3:24Google Scholar
  163. Sumner ME (2000) Beneficial use of effluents, wastes, and biosolids. Commun Soil Sci Plant Anal 31:1701–1715CrossRefGoogle Scholar
  164. Tabrizi L, Mohammadi S, Delshad M, Zadeh BM (2015) Effect of arbuscular mycorrhizal fungi on yield and phytoremediation performance of pot marigold (Calendula officinalis L.) under heavy metals stress. Int J Phytoremediation 17:1244–1252PubMedCrossRefGoogle Scholar
  165. Tank N, Saraf M (2009) Enhancement of plant growth and decontamination of nickel-spiked soil using PGPR. J Basic Microbiol 49:195–204PubMedCrossRefPubMedCentralGoogle Scholar
  166. Temple MD, Perrone GG, Dawes IW (2005) Complex cellular responses to reactive oxygen species. Trends Cell Biol 15:319–326PubMedCrossRefGoogle Scholar
  167. Tian SK, Lu LL, Yang XE, Huang HG, Wang K, Brown PH (2012) Root adaptations to cadmium-induced oxidative stress contribute to Cd tolerance in the hyperaccumulator Sedum alfredii. Biol Plant 56:344–350CrossRefGoogle Scholar
  168. Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Breusegem FV, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968PubMedPubMedCentralCrossRefGoogle Scholar
  169. Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJM (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotechnol 2:158–165CrossRefGoogle Scholar
  170. Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387PubMedCrossRefGoogle Scholar
  171. van Doorn WG, Ketsa S (2014) Cross reactivity between ascorbate peroxidase and phenol (guaiacol) peroxidase. Postharvest Biol Technol 95:64–69CrossRefGoogle Scholar
  172. Viers J, Oliva P, Nonell A, Gélabert A, Sonke JE, Freydier R, Gainville R, Dupré B (2007) Evidence of Zn isotopic fractionation in a soil–plant system of a pristine tropical watershed (Nsimi, Cameroon). Chem Geol 239:124–137CrossRefGoogle Scholar
  173. Villiers F, Ducruix C, Hugouvieux V, Jarno N, Ezan E, Garin J, Junot C, Bourguignon J (2011) Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 11:1650–1663PubMedCrossRefGoogle Scholar
  174. Wan Y, Luo S, Chen J, Xiao X, Chen L, Zeng G, Liu C, He Y (2012) Effect of endophyte-infection on growth parameters and Cd-induced phytotoxicity of Cd-hyperaccumulator Solanum nigrum L. Chemosphere 89:743–750PubMedCrossRefGoogle Scholar
  175. Wang Q, Xiong D, Zhao P, Yu X, Tu B, Wang G (2011) Effect of applying an arsenic-resistant and plant growth–promoting rhizobacterium to enhance soil arsenic phytoremediation by Populus deltoides LH05-17. J Appl Microbiol 111:1065–1074PubMedCrossRefGoogle Scholar
  176. Wang H, Xu R, You L, Zhong G (2013) Characterization of Cu-tolerant bacteria and definition of their role in promotion of growth, Cu accumulation and reduction of Cu toxicity in Triticum aestivum L. Ecotoxicol Environ Saf 94:1–7PubMedCrossRefGoogle Scholar
  177. Wang S, Wang Y, Zhang R, Wang W, Xu D, Guo J, Li P, Yu K (2015) Historical levels of heavy metals reconstructed from sedimentary record in the Hejiang River, located in a typical mining region of Southern China. Sci Total Environ 532:645–654PubMedCrossRefPubMedCentralGoogle Scholar
  178. Wang JL, Li T, Liu G, Smith JM, Zhao Z (2016) Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological and genic aspects. Sci Report 6:22028CrossRefGoogle Scholar
  179. Wani PA, Khan MS, Zaidi A (2007) Chromium reduction, plant growth–promoting potentials, and metal solubilizatrion by Bacillus sp. isolated from alluvial soil. Curr Microbiol 54:237–243PubMedCrossRefPubMedCentralGoogle Scholar
  180. Xu X, Zhao Y, Zhao X, Wang Y, Deng W (2014) Sources of heavy metal pollution in agricultural soils of a rapidly industrializing area in the Yangtze Delta of China. Ecotoxicol Environ Saf 108:161–167PubMedCrossRefPubMedCentralGoogle Scholar
  181. Xu L, Yang W, Jiang F, Qiao Y, Yan Y, An S, Leng X (2016) Effects of reclamation on heavy metal pollution in a coastal wetland reserve. J Coast Conserv 1–7Google Scholar
  182. Xun F, Xie B, Liu S, Guo C (2015) Effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contaminated by petroleum to enhance phytoremediation. Environ Sci Pollut Res 22:598–608CrossRefGoogle Scholar
  183. 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
  184. Yanqun Z, Yuan L, Jianjun C, Haiyan C, Li Q, Schratz C (2005) Hyper accumulation of Pb, Zn and Cd in herbaceous grown on lead-zinc mining area in Yunnan, China. Environ Int 31:755–762PubMedCrossRefGoogle Scholar
  185. Yuan ZL, Zhang CL, Lin FC (2010) Role of diverse non-systemic fungal endophytes in plant performance and response to stress: progress and approaches. J Plant Growth Regul 29:116–126CrossRefGoogle Scholar
  186. Zaets I, Kramarev S, Kozyrovska N (2010) Inoculation with a bacterial consortium alleviates the effect of cadmium overdose in soybean plants. Open Life Sci 5:481–490Google Scholar
  187. Zawoznik MS, Groppa MD, Tomaro ML, Benavides MP (2007) Endogenous salicylic acid potentiates cadmium-induced oxidative stress in Arabidopsis thaliana. Plant Sci 173:190–197CrossRefGoogle Scholar
  188. Zhang Y, He L, Chen Z, Zhang W, Wang Q, Qian M, Sheng X (2011) Characterization of lead-resistant and ACC deaminase-producing endophytic bacteria and their potential in promoting lead accumulation of rape. J Hazard Mater 186:1720–1725PubMedCrossRefGoogle Scholar
  189. Zhao Y, Xu X, Sun W, Huang B, Darilek JL, Shi X (2008) Uncertainty assessment of mapping mercury contaminated soils of a rapidly industrializing city in the Yangtze River Delta of China using sequential indicator co-simulation. Environ Monit Assess 138:343–355PubMedCrossRefGoogle Scholar
  190. Zhuang P, McBride MB, Xia H, Li N, Li Z (2009) Health risk from heavy metals via consumption of food crops in the vicinity of Dabaoshan mine, South China. Sci Total Environ 407:1551–1561PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Kanika Khanna
    • 1
  • Sukhmeen Kaur Kohli
    • 2
  • Shagun Bali
    • 2
  • Parminder Kaur
    • 2
  • Poonam Saini
    • 1
  • Palak Bakshi
    • 1
  • Puja Ohri
    • 3
  • Bilal Ahmad Mir
    • 4
  • Renu Bhardwaj
    • 2
  1. 1.Plant Stress Physiology Lab, Department of Botanical and Environmental SciencesGuru Nanak Dev UniversityAmritsarIndia
  2. 2.Department of Botanical and Environmental SciencesGuru Nanak Dev UniversityAmritsarIndia
  3. 3.Department of Zoological SciencesGuru Nanak Dev UniversityAmritsarIndia
  4. 4.Department of Botany, School of Life SciencesSatellite Campus Kargil, University of KashmirKargilIndia

Personalised recommendations