Problem of Mercury Toxicity in Crop Plants: Can Plant Growth Promoting Microbes (PGPM) Be an Effective Solution?

  • Swapnil Sapre
  • Reena Deshmukh
  • Iti Gontia-MishraEmail author
  • Sharad Tiwari
Part of the Sustainable Development and Biodiversity book series (SDEB, volume 23)


Mercury is ranked as the most toxic heavy metals. It enters into the environment due to some natural processes and anthropogenic activities. It has a property of bioaccumulation into the food chain through uptake by crop plants from the contaminated agricultural lands, leading to detrimental impact on human health. Mercury has the toxic effect on plants as it disturbs many biological processes, including photosynthesis, respiration, transpiration, cell division and so on. Phytoremediation involves several plant species which have the ability to accumulate or degrade contaminants, including heavy metals. Another important strategy is the utilization of transgenic plants transformed with bacterial mer genes to increase phytoremediation of mercury. The mercury-resistant plant growth promoting microbes (PGPM) enhance plant growth under mercury stress as well as increase the mercury uptake by plants. This chapter summarizes the present understanding toward the mercury toxicity and their molecular responses in plants. It also illustrates the plethora of mechanism adapted by PGPM for plant growth promotion and detoxification of mercury. It also highlights the paradigms for synergistic use of PGPM for improved phytoremediation of mercury from agricultural lands.


Mercury Mercury hyperaccumulators Mer genes Plant growth promotion PGPM-assisted phytoremediation 



The author I. Gontia-Mishra acknowledges the funding provided by Science and Engineering Research Board, New Delhi, India, grant number PDF/2017/001001.


  1. AMAP/UNEP (2013) AMAP/UNEP geospatially distributed mercury emissions dataset 2010v1.
  2. Amin A, Latif Z (2017) Screening of mercury-resistant and indole-3-acetic acid producing bacterial-consortium for growth promotion of Cicer arietinum L. J Basic Microbiol 57:204–217CrossRefPubMedPubMedCentralGoogle Scholar
  3. Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol 25:356–362CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ashraf MA, Hussain I, Rasheed R, Iqbal M, Riaz M, Arif MS (2017) Advances in microbe-assisted reclamation of heavy metal contaminated soils over the last decade: a review. J Environ Manag 198:132–143CrossRefGoogle Scholar
  5. Azevedo R, Rodriguez E (2012) Phytotoxicity of mercury in plants: a review. J Bot 2012:848614Google Scholar
  6. Balan BM, Shini S, Krishnan KP, Mohan M (2018) Mercury tolerance and biosorption in bacteria isolated from Ny-Alesund, Svalbard, Arctic. J Basic Microbiol 58:286–295CrossRefGoogle Scholar
  7. Beckers F, Rinklebe J (2017) Cycling of mercury in the environment: sources, fate, and human health implications: a review. Crit Rev Environ Sci Technol 47:693–794CrossRefGoogle Scholar
  8. Bizily SP, Rugh CL, Summers AO, Meagher RB (1999) Phytoremediation of methylmercury pollution: merB expression in Arabidopsis thaliana confers resistance to organomercurials. Proc Natl Acad Sci USA 96:6808–6813CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bizily SP, Rugh CL, Meagher RB (2000) Phytodetoxification of hazardous organomercurials by genetically engineered plants. Nat Biotechnol 18:213CrossRefPubMedPubMedCentralGoogle Scholar
  10. Braud A, Hoegy F, Jezequel K, Lebeau T, Schalk IJ (2009) New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway. Environ Microbiol 11:1079–1091CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bücker-Neto L, Paiva AL, Machado RD, Arenhart RA, Margis-Pinheiro M (2017) Interactions between plant hormones and heavy metals responses. Genet Mol Biol 40:373–386CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chatziefthimiou AD, Crespo-Medina M, Wang Y, Vetriani C, Barkay T (2007) The isolation and initial characterization of mercury resistant chemolithotrophic thermophilic bacteria from mercury rich geothermal springs. Extremophiles 11:469–479CrossRefPubMedPubMedCentralGoogle Scholar
  13. Che D, Meagher RB, Heaton AC, Lima A, Rugh CL, Merkle SA (2003) Expression of mercuric ion reductase in Eastern cottonwood (Populus deltoides) confers mercuric ion reduction and resistance. Plant Biotechnol J 1:311–319CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41CrossRefGoogle Scholar
  15. Chen YA, Chi WC, Trinh NN, Huang LY, Chen YC, Cheng KT et al (2014) Transcriptome profiling and physiological studies reveal a major role for aromatic amino acids in mercury stress tolerance in rice seedlings. PLoS One 9:e95163CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chien MF, Narita M, Lin KH, Matsui K, Huang CC, Endo G (2010) Organomercurials removal by heterogeneous merB genes harboring bacterial strains. J Biosci Bioeng 110:94–98CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chowdhury AS, Das P, Sarkar I, Islam R, Aksharin L, Parvin F, Islam Z, Faris M, Shaekh MP (2015) Phytoremediation of heavy metals (Ar, Cd, Pb) using transgenic rice plants-an overview. Int J Sci Eng Res 6:878Google Scholar
  18. Clark D, Weiss AA, Silver S (1977) Mercury and organomercurial volatilization activities associated with plasmids in Pseudomonas aeruginosa and Pseudomonas putida. J Bacteriol 132:186–196PubMedPubMedCentralGoogle Scholar
  19. Czako M, Feng X, He Y, Liang D, Marton L (2006) Transgenic Spartina alterniflora for phytoremediation. Environ Geochem Health 28:103–110CrossRefPubMedPubMedCentralGoogle Scholar
  20. Czakó M, Feng X, He Y, Liang D, Márton L (2005) Genetic modification of wetland grasses for phytoremediation. Zeitschrift für Naturforschung C 60:285–291CrossRefGoogle Scholar
  21. Dash HR, Das S (2012) Bioremediation of mercury and the importance of bacterial mer genes. Int Biodeterior Biodegrad 75:207–214CrossRefGoogle Scholar
  22. Dash HR, Mangwani N, Das S (2014) Characterization and potential application in mercury bioremediation of highly mercury-resistant marine bacterium Bacillus thuringiensis PW-05. Environ Sci Pollut Res 21:2642–2653CrossRefGoogle Scholar
  23. Dash HR, Sahu M, Mallick B, Das S (2017a) Functional efficiency of MerA protein among diverse mercury resistant bacteria for efficient use in bioremediation of inorganic mercury. Biochimie 142:207–215CrossRefPubMedGoogle Scholar
  24. Dash HR, Basu S, Das S (2017b) Evidence of mercury trapping in biofilm-EPS and mer operon-based volatilization of inorganic mercury in a marine bacterium Bacillus cereus BW-201B. Arch Microbiol 199:445–455CrossRefPubMedGoogle Scholar
  25. Desale P, Patel B, Singh S, Malhotra A, Nawani N (2014) Plant growth promoting properties of Halobacillus sp. and Halomonas sp. in presence of salinity and heavy metals. J Basic Microbiol 54:781–791CrossRefPubMedGoogle Scholar
  26. Dimkpa C, Svatoš A, Merten D, Büchel G, Kothe E (2008) Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can J Microbiol 54:163–172CrossRefPubMedGoogle Scholar
  27. Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333CrossRefPubMedGoogle Scholar
  28. Etesami H (2018) Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicol Environ Safety 147:175–191CrossRefPubMedGoogle Scholar
  29. Ferrara R (1998) Atmospheric mercury sources in the Mt. Amiata area, Italy. Sci Total Environ 213:13–23CrossRefGoogle Scholar
  30. Ferrara R (2000) Volcanoes as emission sources of atmospheric mercury in the Mediterranean basin. Sci Total Environ 259:115–121CrossRefGoogle Scholar
  31. Figueiredo NL, Canário J, O’Driscoll NJ, Duarte A, Carvalho C (2016) Aerobic Mercury-resistant bacteria alter mercury speciation and retention in the Tagus Estuary (Portugal). Ecotoxicol Environ Safety 124:60–67CrossRefGoogle Scholar
  32. Frossard A, Hartmann M, Frey B (2017) Tolerance of the forest soil microbiome to increasing mercury concentrations. Soil Biol Biochem 105:162–176CrossRefGoogle Scholar
  33. Gadd GM (2010) Metals: minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gangwar S, Singh VP, Prasad SM, Maurya JN (2010) Modulation of manganese toxicity in Pisum sativum L. seedlings by kinetin. Sci Hortic 126:467–474CrossRefGoogle Scholar
  35. Giovanella P, Cabral L, Bento FM, Gianello C, Camargo FAO (2016) Mercury (II) removal by resistant bacterial isolates and mercuric (II) reductase activity in a new strain of Pseudomonas sp. B50A. New Biotechnol 33:216–223CrossRefGoogle Scholar
  36. Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374CrossRefGoogle Scholar
  37. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39CrossRefGoogle Scholar
  38. Glick BR, Patten CL, Holguin G et al (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, LondonCrossRefGoogle Scholar
  39. Gondor OK, Pál M, Darkó É, Janda T, Szalai G (2016) Salicylic acid and sodium salicylate alleviate cadmium toxicity to different extents in maize (Zea mays L.). PLoS One 11:e0160157Google Scholar
  40. Gontia-Mishra I, Sasidharan S, Tiwari S (2014) Recent developments in use of 1-amino cyclopropane-1-carboxylate (ACC) deaminase for conferring tolerance to biotic and abiotic stress. Biotechnol Lett 36:889–898CrossRefGoogle Scholar
  41. Gontia-Mishra I, Sapre S, Sharma A, Tiwari S (2016) Alleviation of mercury toxicity in wheat by the interaction of mercury-tolerant plant growth-promoting rhizobacteria. J Plant Grow Regul 35:1000–1012CrossRefGoogle Scholar
  42. Gontia-Mishra I, Sapre S, Kachare S, Tiwari S (2017a) Molecular diversity of 1-aminocyclopropane-1-carboxylate (ACC) deaminase producing PGPR from wheat (Triticum aestivum L.) rhizosphere. Plant Soil 414:213–227CrossRefGoogle Scholar
  43. Gontia-Mishra I, Sapre S, Tiwari S (2017b) Zinc solubilizing bacteria from the rhizosphere of rice as prospective modulator of zinc biofortification in rice. Rhizosphere 3:185–190CrossRefGoogle Scholar
  44. Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech 5:355–377Google Scholar
  45. Gupta P, Diwan B (2017) Bacterial exopolysaccharide mediated heavy metal removal: a Review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep 13:58–71CrossRefGoogle Scholar
  46. Gupta S, Nirwan J (2015) Evaluation of mercury biotransformation by heavy metal-tolerant Alcaligenes strain isolated from industrial sludge. Int J Environ Sci Technol 12:995–1002CrossRefGoogle Scholar
  47. Gupta A, Rai V, Bagdwal N, Goel R (2005) In situ characterization of mercury-resistant growth-promoting fluorescent pseudomonads. Microbiol Res 160:385–388CrossRefGoogle Scholar
  48. Han Y, Wang R, Yang Z, Zhan Y, Ma Y, Ping S, Zhang L, Lin M, Yan Y (2015) 1-aminocyclopropane-1-carboxylate deaminase from Pseudomonas stutzeri A1501 facilitates the growth of rice in the presence of salt or heavy metals. J Microbiol Biotechnol 25:1119–1128CrossRefGoogle Scholar
  49. Haque S, Zeyaullah M, Nabi G, Srivastava PS, Ali A (2010) Transgenic tobacco plant expressing environmental E. coli merA gene for enhanced volatilization of ionic mercury. J Microbiol Biotechnol 20:917–924CrossRefGoogle Scholar
  50. Heaton AC, Rugh CC, Kim T, Meagher RB (2003) Toward detoxifying mercury-polluted aquatic sediments with rice genetically engineered for mercury resistance. Environ Toxicol Chem 22:2940–2947CrossRefGoogle Scholar
  51. Hesse E, O’Brien S, Tromas N, Bayer F, Luján AM, van Veen EM, Hodgson DJ, Buckling A (2018) Ecological selection of siderophore-producing microbial taxa in response to heavy metal contamination. Ecol Lett 21:117–127CrossRefGoogle Scholar
  52. Hindersah R, Mulyani O, Osok R (2017) Proliferation and exopolysaccharide production of Azotobacter in the presence of mercury. Biodivers J 8:21–26Google Scholar
  53. Hindersah R, Handyman Z, Indriani FN, Suryatmana P, Nurlaeny N (2018) Azotobacter population, soil nitrogen and groundnut growth in mercury-contaminated tailing inoculated with Azotobacter. J Degraded Mining Lands Manag 5:1269–1274CrossRefGoogle Scholar
  54. Hseu ZY, Su SW, Lai HY, Guo HY, Chen TC, Chen ZS (2010) Remediation techniques and heavy metal uptake by different rice varieties in metal-contaminated soils of Taiwan: new aspects for food safety regulation and sustainable agriculture. Soil Sci Plant Nutr 56:31–52CrossRefGoogle Scholar
  55. Huang CC, Narita M, Yamagata T, Endo G, Silver S (2002) Characterization of two regulatory genes of the mercury resistance determinants from TnMERI1 by luciferase-based examination. Gene 301:13–20CrossRefGoogle Scholar
  56. Hussein HS, Ruiz ON, Terry N, Daniell H (2007) Phytoremediation of mercury and organomercurials in chloroplast transgenic plants: enhanced root uptake, translocation to shoots, and volatilization. Environ Sci Technol 41:8439–8446CrossRefPubMedPubMedCentralGoogle Scholar
  57. Hutchison AR (2003) Mercury pollution and remediation: the chemist’s response to a global crisis. J Chem Crystallogr 33:631–645CrossRefGoogle Scholar
  58. Im Choi Y, Noh EW, Lee HS, Han MS, Lee JS, Choi KS (2007) Mercury-tolerant transgenic poplars expressing two bacterial mercury-metabolizing genes. J Plant Biol 50:658CrossRefGoogle Scholar
  59. Israr M, Sahi S, Datta R, Sarkar D (2006) Bioaccumulation and physiological effects of mercury in Sesbania drummonii. Chemosphere 65:591–598CrossRefGoogle Scholar
  60. Jha B, Gontia I, Hartmann A (2012) The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth promoting potential. Plant Soil 356:265–277CrossRefGoogle Scholar
  61. Kalaivanan D, Ganeshamurthy AN (2016) Mechanisms of heavy metal toxicity in plants. In: Rao N, Shivashankara K, Laxman R (eds) Abiotic stress physiology of horticultural crops. Springer, New Delhi, pp 85–102CrossRefGoogle Scholar
  62. Kamran S, Shahid I, Baig DN, Rizwan M, Malik KA, Mehnaz S (2017) Contribution of zinc solubilizing bacteria in growth promotion and zinc content of wheat. Front Microbiol 8:2593CrossRefPubMedPubMedCentralGoogle Scholar
  63. Kang SH, Singh S, Kim JY, Lee W, Mulchandani A, Chen W (2007) Bacteria metabolically engineered for enhanced phytochelatin production and cadmium accumulation. Appl Environ Microbiol 73:6317–6320CrossRefPubMedPubMedCentralGoogle Scholar
  64. Kavita B, Shukla S, Kumar GN, Archana G (2008) Amelioration of phytotoxic effects of Cd on mung bean seedlings by gluconic acid secreting rhizobacterium Enterobacter asburiae PSI3 and implication of role of organic acid. World J Microbiol Biotechnol 24:2965–2972CrossRefGoogle Scholar
  65. Kawahigashi H, Hirose S, Hayashi E, Ohkawa H, Ohkawa Y (2002) Phytotoxicity and metabolism of ethofumesate in transgenic rice plants expressing the human CYP2B6 gene. Pesticide Biochem Physiol 74:139–147CrossRefGoogle Scholar
  66. Kim KY, Jordan D, McDonald GA (1998) Effect of phosphate solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol Fertil Soils 26:79–87CrossRefGoogle Scholar
  67. Kiyono M, Pan-Hou H (1999) The merG gene product is involved in phenylmercury resistance in Pseudomonas strain K-62. J Bacteriol 181:726–730PubMedPubMedCentralGoogle Scholar
  68. Kloepper JW, Leong J, Teintze M, Schiroth MN (1980) Enhanced plant growth by siderophores produced by plant growth promoting rhizobacteria. Nature 286:885–886CrossRefGoogle Scholar
  69. Krishnamurthy A, Rathinasabapathi B (2013) Auxin and its transport play a role in plant tolerance to arsenite-induced oxidative stress in Arabidopsis thaliana. Plant Cell Environ 36:1838–1849CrossRefGoogle Scholar
  70. Kumar B, Smita K, Flores LC (2017) Plant mediated detoxification of mercury and lead. Arab J Chem 10:S2335–S2342CrossRefGoogle Scholar
  71. Lafrance-Vanasse J, Lefebvre M, Di Lello P, Sygusch J, Omichinski JG (2009) Crystal structures of the organomercurial lyase merb in its free and mercury-bound forms insights into the mechanism of methylmercury degradation. J Biol Chem 284:938–944CrossRefPubMedPubMedCentralGoogle Scholar
  72. Lebrazi S, Fikri-Benbrahim K (2018) Rhizobium-legume symbiosis: heavy metal effects and principal approaches for bioremediation of contaminated soil. In: Meena R, Das A, Yadav G, Lal R (eds) Legumes for soil health and sustainable management. Springer, Singapore, pp 205–233CrossRefGoogle Scholar
  73. Lee J, Bae H, Jeong J, Lee JY, Yang YY, Hwang I, Martinoia E, Lee Y (2003) Functional expression of a bacterial heavy metal transporter in Arabidopsis enhances resistance to and decreases uptake of heavy metals. Plant Physiol 133:589–596CrossRefPubMedPubMedCentralGoogle Scholar
  74. Li HY, Wei DQ, Shen M, Zhou ZP (2012) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18CrossRefGoogle Scholar
  75. Ma Y, Oliveira RS, Wu L, Luo Y, Rajkumar M, Rocha I, Freitas H (2015) Inoculation with metal-mobilizing plant-growth-promoting rhizobacterium Bacillus sp. SC2b and its role in rhizoremediation. J Toxicol Environ Health Part A 78:931–944CrossRefPubMedGoogle Scholar
  76. 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
  77. Ma Q, Grones P, Robert S (2018) Auxin signaling: a big question to be addressed by small molecules. J Exp Bot 69:313–328CrossRefGoogle Scholar
  78. Maestri E, Marmiroli N (2011) Transgenic plants for phytoremediation. Int J Phytoremediation 13:264–279CrossRefGoogle Scholar
  79. Mahbub KR, Krishnan K, Megharaj M, Naidu R (2016a) Bioremediation potential of a highly mercury resistant bacterial strain Sphingobium SA2 isolated from contaminated soil. Chemosphere 144:330–337CrossRefGoogle Scholar
  80. Mahbub KR, Krishnan K, Naidu R, Megharaj M (2016b) Mercury resistance and volatilization by Pseudoxanthomonas sp. SE1 isolated from soil. Environ Technol Innov 6:94–104CrossRefGoogle Scholar
  81. Mason RP, Choi AL, FitzgeraldWF Hammerschmidt CR, Lamborg CH, Soerensen AL, Sunderland EM (2012) Mercury biogeochemical cycling in the ocean and policy implications. Environ Res 119:101–117CrossRefPubMedPubMedCentralGoogle Scholar
  82. Mathema VB, Thakuri BC, Sillanpää M (2011) Bacterial mer operon-mediated detoxification of mercurial compounds: a short review. Arch Microbiol 193:837–844CrossRefPubMedPubMedCentralGoogle Scholar
  83. Mathew DC, Ho YN, Gicana RG, Mathew GM, Chien MC, Huang CC (2015) A rhizosphere-associated symbiont, Photobacterium spp. strain MELD1, and its targeted synergistic activity for phytoprotection against mercury. PLoS One 10:e0121178Google Scholar
  84. Meagher RB, Heaton AC (2005) Strategies for the engineered phytoremediation of toxic element pollution: mercury and arsenic. J Ind Microbiol Biotechnol 32:502–513CrossRefPubMedPubMedCentralGoogle Scholar
  85. Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol Adv 29:645–653CrossRefPubMedPubMedCentralGoogle Scholar
  86. Mishra J, Singh R, Arora NK (2017) Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front Microbiol 8:1706CrossRefPubMedPubMedCentralGoogle Scholar
  87. Mobeen N, Latif Z (2016) Characterization of mercury resistant and growth promoting Enterobacter sp. from rhizosphere to use as a biofertilizer. Adv Life Sci 3:36–41Google Scholar
  88. Møller AK, Barkay T, Hansen MA, Norman A, Hansen LH, Sørensen SJ, Boyd ES, Kroer N (2014) Mercuric reductase genes (merA) and mercury resistance plasmids in High Arctic snow, freshwater and sea-ice brine. FEMS Microbiol Ecol 87:52–63CrossRefPubMedPubMedCentralGoogle Scholar
  89. Muddarisna N, Krisnayanti BD, Utami SR, Handayanto E (2013) Phytoremediation of mercury-contaminated soil using three wild plant species and its effect on maize growth. Appl Ecol Environ Sci 1:27–32Google Scholar
  90. Mukkata K, Kantachote D, Wittayaweerasak B, Techkarnjanaruk S, Mallavarapu M, Naidu R (2015) Distribution of mercury in shrimp ponds and volatilization of Hg by isolated resistant purple non-sulfur bacteria. Water Air Soil Pollut 226:148CrossRefGoogle Scholar
  91. Nascimento AM, Chartone-Souza E (2003) Operon mer: bacterial resistance to mercury and potential for bioremediation of contaminated environments. Genet Mol Res 2:92–101PubMedGoogle Scholar
  92. Neilands J (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 45:26723–26726CrossRefGoogle Scholar
  93. Neubauer U, Furrer G, Kayser A, Schulin R (2000) Siderophores, NTA, and citrate: potential soil amendments to enhance heavy metal mobility in phytoremediation. Int J Phytoremediation 2:353–368CrossRefGoogle Scholar
  94. Ní Chadhain SM, Schaefer JK, Crane S, Zylstra GJ, Barkay T (2006) Analysis of mercuric reductase (merA) gene diversity in an anaerobic mercury-contaminated sediment enrichment. Environ Microbiol 8:1746–1752CrossRefPubMedPubMedCentralGoogle Scholar
  95. Nocelli N, Bogino PC, Banchio E, Giordano W (2016) Roles of extracellular polysaccharides and biofilm formation in heavy metal resistance of rhizobia. Materials 9:418CrossRefGoogle Scholar
  96. Nonnoi F, Chinnaswamy A, García de la Torre VS, Coba de la Peña T, Lucas MM, Pueyo JJ (2012) Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes Medicago spp. and Trifolium spp. growing in mercury contaminated soils. Appl Soil Ecol 61:49–59CrossRefGoogle Scholar
  97. Ortiz-Ojeda P, Ogata-Gutiérrez K, Zúñiga-Dávila D (2017) Evaluation of plant growth promoting activity and heavy metal tolerance of psychrotrophic bacteria associated with maca (Lepidium meyenii Walp.) rhizosphere. AIMS Microbiology 3:279–292CrossRefPubMedPubMedCentralGoogle Scholar
  98. Osmolovskaya N, Vu D, Kuchaeva L (2018) The role of organic acids in heavy metal tolerance in plants. Biol Comm 63:9–16CrossRefGoogle Scholar
  99. Oves M, Khan MS, Zaidi A (2013) Chromium reducing and plant growth promoting novel strain Pseudomonas aeruginosa OSG41 enhance chickpea growth in chromium amended soils. Eur J Soil Biol 56:72–83CrossRefGoogle Scholar
  100. Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyperaccumulation metals in plants. Water Air Soil Pollut 184(1–4):105–126CrossRefGoogle Scholar
  101. Patra M, Sharma A (2000) Mercury toxicity in plants. Bot Rev 66:379–422CrossRefGoogle Scholar
  102. Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52:199–223CrossRefGoogle Scholar
  103. Patten CL, Glick BR (2002) Role of Pseudomonas putida indole acetic acid in development of host plant root system. Appl Environ Microbiol 48:3795–3801CrossRefGoogle Scholar
  104. Pietro-Souza W, Mello IS, Vendruscullo SJ, da Silva GF, da Cunha CN, White JF, Soares MA (2017) Endophytic fungal communities of Polygonum acuminatum and Aeschynomene fluminensis are influenced by soil mercury contamination. PLoS One 12:e0182017CrossRefPubMedPubMedCentralGoogle Scholar
  105. Pirrone N, Costa P, Pacyna JM, Ferrara R (2001) Mercury emissions to the atmosphere from natural and anthropogenic sources in the Mediterranean region. Atmos Environ 35:2997–3006CrossRefGoogle Scholar
  106. Powlowski J, Sahlman L (1999) Reactivity of the two essential cysteine residues of the periplasmic mercuric ion-binding protein, MerP. J Biol Chem 274:33320–33326CrossRefPubMedGoogle Scholar
  107. Puglisi I, Faedda R, Sanzaro V, Piero ARL, Petrone G, Cacciola SO (2012) Identification of differentially expressed genes in response to mercury I and II stress in Trichoderma harzianum. Gene 506:325–330CrossRefPubMedGoogle Scholar
  108. Pushkar B, Sevak P, Sounderajan S (2018) Assessment of the bioremediation efficacy of the mercury resistant bacterium isolated from the Mithi River. Water Sci Technol Water Supply, ws2018064.
  109. Quiñones MA, Ruiz-Díez B, Fajardo S, López-Berdonces MA, Higueras PL, Fernández-Pascual M (2013) Lupinus albus plants acquire mercury tolerance when inoculated with an Hg-resistant Bradyrhizobium strain. Plant Physiol Biochem 73:168–175CrossRefPubMedGoogle Scholar
  110. Rafique A, Amin A, Latif Z (2015) Screening and characterization of mercury-resistant nitrogen fixing bacteria and their use as biofertilizers and for mercury bioremediation. Pakistan J Zool 47:1271–1277Google Scholar
  111. Rajkumar M, Ae N, Prasad MN, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149CrossRefPubMedPubMedCentralGoogle Scholar
  112. Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574CrossRefGoogle Scholar
  113. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181CrossRefPubMedPubMedCentralGoogle Scholar
  114. Reddy MS, Prasanna L, Marmeisse R, Fraissinet-Tachet L (2014) Differential expression of metallothioneins in response to heavy metals and their involvement in metal tolerance in the symbiotic basidiomycete Laccaria bicolor. Microbiology 160:2235–2242CrossRefGoogle Scholar
  115. Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, pp 193–229Google Scholar
  116. Reniero D, Galli E, Barbieri P (1995) Cloning and comparison of mercury and organomercurial resistance determinants from a Pseudomonas stutzeri plasmid. Gene 166:77–82CrossRefGoogle Scholar
  117. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906Google Scholar
  118. Rizvi A, Khan MS (2017) Biotoxic impact of heavy metals on growth, oxidative stress and morphological changes in root structure of wheat (Triticum aestivum L.) and stress alleviation by Pseudomonas aeruginosa strain CPSB1. Chemosphere 185:942–952CrossRefPubMedPubMedCentralGoogle Scholar
  119. Rugh CL, Wilde HD, Stack NM, Thompson DM, Summers AO, Meagher RB (1996) Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modified bacterial merA gene. Proc Natl Acad Sci USA 93:3182–3187CrossRefPubMedPubMedCentralGoogle Scholar
  120. Rugh CL, Senecoff JF, Meagher RB, Merkle SA (1998) Development of transgenic yellow poplar for mercury phytoremediation. Nat Biotechnol 16:925CrossRefPubMedPubMedCentralGoogle Scholar
  121. Ruiz ON, Daniell H (2009) Genetic engineering to enhance mercury phytoremediation. Curr Opin Biotechnol 20:213–219CrossRefPubMedPubMedCentralGoogle Scholar
  122. Ruiz ON, Hussein HS, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol 132:1344–1352CrossRefPubMedPubMedCentralGoogle Scholar
  123. Ruiz-Diez B, Quinones MA, Fajardo S, Lopez MA, Higueras P, Fernandez-Pascual M (2012) Mercury-resistant rhizobial bacteria isolated from nodules of leguminous plants growing in high Hg-contaminated soils. Appl Microbiol Biotechnol 96:543–554CrossRefPubMedPubMedCentralGoogle Scholar
  124. Saranya K, Sundaramanickam A, Shekhar S, Swaminathan S, Balasubramanian T (2017) Bioremediation of mercury by Vibrio fluvialis screened from industrial effluents. Biomed Res Int 2017:6509648CrossRefPubMedPubMedCentralGoogle Scholar
  125. Saravanan VS, Madhaiyan M, Thangaraju M (2007) Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66:1794–1798CrossRefPubMedPubMedCentralGoogle Scholar
  126. Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854CrossRefPubMedPubMedCentralGoogle Scholar
  127. Schottel JL (1978) The mercury and organomercurial detoxifying enzymes from a plasmid-bearing strain of Escherichia coli. J Biol Chem 253:4341–4349PubMedPubMedCentralGoogle Scholar
  128. Schroeder WH, Munthe J (1998) Atmospheric mercury—an overview. Atmospheric Environ 32:809–822CrossRefGoogle Scholar
  129. Selin NE (2009) Global biogeochemical cycling of mercury: a review. Ann Rev Environ Res 34:43CrossRefGoogle Scholar
  130. Shehu J, Imeri A, Kupe L, Dodona E, Shehu A, Mullaj A (2014) Hyperaccumulators of mercury in the industrial area of a PVC factory in Vlora (Albania). Arch Biol Sci Belgrade 66:1457–1464CrossRefGoogle Scholar
  131. Sotero-Martins A, Jesus MS, Lacerda M, Moreira JC, Filgueiras AL, Barrocas PR (2008) A conservative region of the mercuric reductase gene (merA) as a molecular marker of bacterial mercury resistance. Braz J Microbiol 39:307–310CrossRefPubMedPubMedCentralGoogle Scholar
  132. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448CrossRefPubMedPubMedCentralGoogle Scholar
  133. Storey EP, Boghozian R, Little JL, Lowman DW, Chakraborty R (2006) Characterization of ‘Schizokinen’; a dihydroxamate-type siderophore produced by Rhizobium leguminosarum IARI 917. Biometals 19:637–649CrossRefGoogle Scholar
  134. Su Y, Han F, Shiyab S, Monts DL (2007) Phytoextraction and accumulation of mercury in selected plant species grown in soil contaminated with different mercury compounds. In: WM’07 Conference February 25–March 1, 2007, Tucson, Arizon, USAGoogle Scholar
  135. Sunil KCR, Swati K, Bhavya G, Nandhini M, Veedashree M, Prakash HS, Kini KR, Geetha N (2015) Streptomyces flavomacrosporus, a multi-metal tolerant potential bioremediation candidate isolated from paddy field irrigated with industrial effluents. Int J Life Sci 3:9–15Google Scholar
  136. Tangahu BV, Sheikh Abdullah SR, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 2011:939161CrossRefGoogle Scholar
  137. Tariq A, Latif Z (2014) Bioremediation of mercury compounds by using immobilized nitrogen-fixing bacteria. Inter J Agric Biol 16:1129–1134Google Scholar
  138. Tariq S, Amin A, Latif Z (2015) PCR based DNA fingerprinting of mercury resistant and nitrogen fixing Pseudomonas spp. Pure Appl Biol 4:129–136CrossRefGoogle Scholar
  139. Teng Y, Wang X, Li L, Li Z, Luo Y (2015) Rhizobia and their bio-partners as novel drivers for functional remediation in contaminated soils. Front Plant Sci 6:32CrossRefPubMedPubMedCentralGoogle Scholar
  140. Tiwari S, Lata C (2018) Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview. Front Plant Sci 9:452CrossRefPubMedPubMedCentralGoogle Scholar
  141. Ullah A, Heng S, Munis MFH, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40CrossRefGoogle Scholar
  142. Weiss AA, Murphy SD, Silver S (1977) Mercury and organomercurial resistances determined by plasmids in Staphylococcus aureus. J Bacteriol 132:197–208PubMedPubMedCentralGoogle Scholar
  143. Wood JL, Tang C, Franks AE (2016) Microbial associated plant growth and heavy metal accumulation to improve phytoextraction of contaminated soils. Soil Biol Biochem 103:131–137CrossRefGoogle Scholar
  144. Yong X, Chen Y, Liu W, Xu L, Zhou J, Wang S, Chen P, Ouyang P, Zheng T (2014) Enhanced cadmium resistance and accumulation in Pseudomonas putida KT2440 expressing the phytochelatin synthase gene of Schizosaccharomyces pombe. Lett Appl Microbiol 58:255–261CrossRefGoogle Scholar
  145. Zhou ZS, Wang SJ, Yang ZM (2008) Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere 70:1500–1509CrossRefGoogle Scholar
  146. Zhu XF, Jiang T, Wang ZW, Lei GJ, Shi YZ, Li GX, Zheng SJ (2012) Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J Hazard Mater 239:302–307CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Swapnil Sapre
    • 1
  • Reena Deshmukh
    • 1
  • Iti Gontia-Mishra
    • 1
    Email author
  • Sharad Tiwari
    • 2
  1. 1.Biotechnology Centre, Jawaharlal Nehru Agriculture UniversityJabalpurIndia
  2. 2.Department of Plant Breeding and GeneticsJawaharlal Nehru Agriculture UniversityJabalpurIndia

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