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Heavy Metal Stress and Tolerance in Plants Mediated by Rhizospheric Microbes

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Salt Stress, Microbes, and Plant Interactions: Causes and Solution

Abstract

The environmental contamination has become a serious issue in recent times due to human engagements, such as application of pesticides, chemical preservatives, mining, coal combustion, etc. These anthropogenic activities have imposed escalated heavy metal concentrations in water, soil, and air. Specifically, heavy metal pollution of soils causes numerous environmental complications and imparts detrimental effect on living organisms including microbes, plants, and animals. In order to adapt, tolerate, and survive in these adverse situations, plants have evolved with multifaceted molecular and biological mechanisms. Though plants possess many defensive mechanisms to overcome heavy metal intoxication, these strategies of tolerance may not be effective beyond certain limit. Hence, plants will be at the risk of survival. Some of the methods used for removing heavy metals from soil include soil washing with physical or chemical methods; excavation, i.e., the physical elimination from polluted sites; and in situ fixation, the addition of chemicals to stabilize and alter heavy metals to a state that cannot be absorbed by plants. Still, these chemical and physical techniques are not very efficient and the process is expensive. Alternatively, the biological ways of cleaning the contaminated areas have gained more importance in recent times. These approaches include the phytoremediation and the application of rhizospheric microorganisms to clean up the soil. Particularly, rhizospheric microorganisms have the ability to shield the plant from heavy metal stress. To be specific, microbes have the molecular machinery to adopt and can survive even in the existence of toxic levels of heavy metals. In the present chapter, the knowledge of heavy metal toxicity and its remediation using microbes is discussed and the utilization of soil microbes for combating the heavy metal stress in plants is also highlighted.

Mallappa Kumara Swamy and Boregowda Purushotham have equally contributed for this chapter

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References

  • Abbas G, Murtaza B, Bibi I, Shahid M, Niazi N, Khan M, Amjad M, Hussain M (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59. https://doi.org/10.3390/ijerph15010059

    Article  PubMed Central  CAS  Google Scholar 

  • Amstaetter K, Borch T, Larese-Casanova P, Kappler A (2009) Redox transformation of arsenic by Fe (II)-activated goethite (α-FeOOH). Environ Sci Technol 44:102–108

    Article  CAS  Google Scholar 

  • Anderson AJ, Meyer DR, Mayer FK (1973) Heavy metal toxicities: levels of nickel, cobalt and chromium in the soil and plants associated with visual symptoms and variation in growth of an oat crop. Aust J Agric Res 24:557–571

    Article  CAS  Google Scholar 

  • Ashfaque F, Inam A, Sahay S, Iqbal S (2016) Influence of Heavy metal toxicity on plant growth, metabolism and its alleviation by phytoremediation- A promising technology. J Agri Ecol Res Int 6:1–19

    Article  Google Scholar 

  • 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 198:132–143

    Article  CAS  Google Scholar 

  • Ayangbenro A, Babalola O (2018) A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Environ Res Public Health 14:94. https://doi.org/10.3390/ijerph14010094

    Article  PubMed Central  CAS  Google Scholar 

  • Baldiris R, Acosta-Tapia N, Montes A, Hernández J, Vivas-Reyes R (2018) Reduction of hexavalent chromium and detection of chromate reductase (ChrR) in Stenotrophomonas maltophilia. Molecules 23:406. https://doi.org/10.3390/molecules23020406

    Article  CAS  PubMed Central  Google Scholar 

  • Bati CB, Santilli E, Lombardo L (2015 Feb 1) Effect of arbuscular mycorrhizal fungi on growth and on micronutrient and macronutrient uptake and allocation in olive plantlets growing under high total Mn levels. Mycorrhiza 25:97–108

    Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    Article  CAS  Google Scholar 

  • Blazka ME, Shaikh ZA (1992) Cadmium and mercury accumulation in rat hepatocytes: interactions with other metal ions. Toxicol Appl Pharmacol 113:118–125

    Article  CAS  PubMed  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Bradham KD, Dayton EA, Basta NT, Schroder J, Payton M, Lanno RP (2006) Effect of soil properties on lead bioavailability and toxicity to earthworms. Environ Toxicol Chem 25:769–775

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee S, Sau GB, Mukherjee SK (2009) Plant growth promotion by a hexavalent chromium reducing bacterial strain, Cellulosimicrobium cellulans KUCr3. World J Microbiol Biotechnol 25:1829–1836. https://doi.org/10.1007/s11274-009-0084-5

    Article  CAS  Google Scholar 

  • Clarkson TW, Magos L (2006) The toxicology of mercury and its chemical compounds. Crit Rev Toxicol 36:609–662

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512

    Article  CAS  PubMed  Google Scholar 

  • Coreño-Alonso A, Solé A, Diestra E, Esteve I, Gutiérrez-Corona JF, López GR, Fernández FJ, Tomasini A (2014 Apr 1) Mechanisms of interaction of chromium with Aspergillus Niger var tubingensis strain Ed8. Bioresour Technol 158:188–192

    Article  PubMed  CAS  Google Scholar 

  • Dary M, Chamber-Pérez MA, Palomares AJ, Pajuelo E (2010) “In situ” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177:323–330

    Article  CAS  PubMed  Google Scholar 

  • De Abreu CA, De Abreu MF, De Andrade JC (1998) Distribution of lead in the soil profile evaluated by DTPA and Mehlich-3 solutions. Bragantia 57:185–192

    Article  Google Scholar 

  • de Andrade SA, da Silveira AP (2008 Mar) Mycorrhiza influence on maize development under cd stress and P supply. Braz J Plant Physiol 20(1):39–50

    Article  Google Scholar 

  • Delhaize E, Ryan PR (1995 Feb) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315-321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Vries W, Lofts S, Tipping E, Meili M, Groenenberg JE, Schütze G (2007) Impact of soil properties on critical concentrations of cadmium, lead, copper, zinc, and mercury in soil and soil solution in view of ecotoxicological effects. Rev Environ Contam Toxicol 191:47–89

    PubMed  Google Scholar 

  • Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E (2009) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162

    Article  CAS  Google Scholar 

  • Ebbs SD, Kochian LV (1992) Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J Environ Qual 26:776–781

    Article  Google Scholar 

  • Ehrlich HL (1997) Microbes and metals. Appl Microbiol Biotechnol 48:687–692

    Article  CAS  Google Scholar 

  • Eick MJ, Peak JD, Brady PV, Pesek JD (1999) Kinetics of lead adsorption/desorption on goethite: residence time effect. Soil Sci 164:28–39

    Article  CAS  Google Scholar 

  • Etesami H (2018) Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicol Environ Saf 147:175–191

    Article  CAS  PubMed  Google Scholar 

  • Farid M, Shakoor MB, Ehsan S, Ali S, Zubair M, Hanif MS (2013) Morphological, physiological and biochemical responses of different plant species to Cd stress. Intl J Chem Biochem Sci 3:53–60

    Google Scholar 

  • Finnegan P, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 63:182. https://doi.org/10.3389/fphys.2012.00182

    Article  CAS  Google Scholar 

  • Franchi E, Rolli E, Marasco R, Agazzi G, Borin S, Cosmina P, Pedron F, Rosellini I, Barbafieri M, Petruzzelli G (2017) Phytoremediation of a multi-contaminated soil: mercury and arsenic phytoextraction assisted by mobilizing agent and plant growth promoting bacteria. J Soils Sediments 17:1224–1236

    Article  CAS  Google Scholar 

  • Gadd GM, Bahri-Esfahani J, Li Q, Rhee YJ, Wei Z, Fomina M, Liang X (2014 Oct 1) Oxalate production by fungi: significance in geomycology, biodeterioration and bioremediation. Fungal Biol Rev 28:36–55

    Article  Google Scholar 

  • Garbisu C, Alkorta I (2001) Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresour Technol 77:229–236

    Article  CAS  PubMed  Google Scholar 

  • Gavrilescu M (2004) Removal of heavy metals from the environment by biosorption. Eng Life Sci 4:219–232

    Article  CAS  Google Scholar 

  • Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68

    Article  CAS  PubMed  Google Scholar 

  • Gupta SK, Rai AK, Kanwar SS, Sharma TR (2012) Comparative analysis of zinc finger proteins involved in plant disease resistance. PLoS One 7:e42578. https://doi.org/10.1371/journal.pone.0042578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta P, Rani R, Chandra A, Kumar V (2018) Potential applications of Pseudomonas sp. (strain CPSB21) to ameliorate Cr6+ stress and phytoremediation of tannery effluent contaminated agricultural soils. Sci Rep 8:4860

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  PubMed  Google Scholar 

  • Haridasan M, Paviani TI, Schiavini I (1986) Localization of aluminium in the leaves of some aluminium-accumulating species. Plant Soil 94:435–437

    Article  Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    Article  CAS  PubMed  Google Scholar 

  • Hassan TU, Bano A, Naz I (2017) Alleviation of heavy metals toxicity by the application of plant growth promoting rhizobacteria and effects on wheat grown in saline sodic field. Int J Phytoremed 19:522–529

    Article  CAS  Google Scholar 

  • Helleday T, Nilsson R, Jenssen D (2000) Arsenic [III] and heavy metal ions induce intrachromosomal homologous recombination in the hprt gene of V79 Chinese hamster cells. Environ Mol Mutagen 35:114–122

    Article  CAS  PubMed  Google Scholar 

  • Islam F, Yasmeen T, Ali Q, Mubin M, Ali S, Arif MS, Hussain S, Riaz M, Abbas F (2016) Copper-resistant bacteria reduces oxidative stress and uptake of copper in lentil plants: potential for bacterial bioremediation. Environ Sci Pollut Res 23:220–233

    Article  CAS  Google Scholar 

  • Jarvis MD, Leung DW (2002) Chelated lead transport in Pinus radiata: an ultrastructural study. Environ Exp Bot 48:21–32

    Article  CAS  Google Scholar 

  • Joner E, Leyval C (2001) Time-course of heavy metal uptake in maize and clover as affected by root density and different mycorrhizal inoculation regimes. Biol Fertil Soils 33:351–357

    Google Scholar 

  • Kaewdoung B, Sutjaritvorakul T, Gadd GM, Whalley AJ, Sihanonth P (2016) Heavy metal tolerance and biotransformation of toxic metal compounds by new isolates of wood-rotting fungi from Thailand. Geomicrobiol J 33:283–288

    Article  CAS  Google Scholar 

  • Khan AG, Kuek C, Chaudhary TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197–207

    Article  CAS  PubMed  Google Scholar 

  • Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–9

    Article  CAS  Google Scholar 

  • Koyro HW, Ahmad P, Geissler N (2012) Abiotic stress responses in plants: an overview. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, Cham, pp 1–28

    Google Scholar 

  • Kumar B, Smita K, Flores LC (2017) Plant mediated detoxification of mercury and lead. Arab J Chem 10:2335–2342

    Article  CAS  Google Scholar 

  • Leyval C, Joner EJ, Del Val C, Haselwandter K (2002) Potential of arbuscular mycorrhizal fungi for bioremediation. In: Mycorrhizal technology in agriculture. Birkhäuser, Basel, pp 175–186

    Chapter  Google Scholar 

  • Liu D, Wang X, Chen Z, Xu H, Wang Y (2010) Influence of mercury on chlorophyll content in winter wheat and mercury bioaccumulation. Plant Soil Environ 56:139–143

    Article  CAS  Google Scholar 

  • Lloyd JR (2003) Microbial reduction of metals and radionuclides. FEMS Microbiol Rev 27:411–425

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Prasad MN, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258

    Article  CAS  PubMed  Google Scholar 

  • 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 69:220–228

    Article  CAS  PubMed  Google Scholar 

  • Majumder A, Bhattacharyya K, Bhattacharyya S, Kole SC (2013) Arsenic-tolerant, arsenite-oxidising bacterial strains in the contaminated soils of West Bengal, India. Sci Total Environ 463:1006–1014. https://doi.org/10.1016/j.scitotenv.2013.06.068

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto H (1988) Inhibition of proton transport activity of microsomal membrane vesicles of barley roots by aluminium. Soil Sci Plant Nutr 34:499–506

    Article  CAS  Google Scholar 

  • May HM, Nordstrom DK (1991) Assessing the solubilities and reaction kinetics of aluminous minerals in soils. In: Ulrich B, Sumner E (eds) Soil acidity. Springer, Berlin, pp 125–148

    Chapter  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mishra J, Singh R, Arora NK (2017) Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front Microbiol 8:1706

    Article  PubMed  PubMed Central  Google Scholar 

  • Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448

    Article  PubMed  Google Scholar 

  • Naguib MM, El-Gendy AO, Khairalla AS (2018) Microbial diversity of mer operon genes and their potential rules in mercury bioremediation and resistance. Open Biotechnol J 12:56–77

    Article  CAS  Google Scholar 

  • Ong GH, Ho XH, Shamkeeva S, Manasha Savithri Fernando AS, Wong LS (2017) Biosorption study of potential fungi for copper remediation from Peninsular Malaysia. Remediat J 27:59–63

    Article  Google Scholar 

  • Ortega-Villasante C, Rellán-Alvarez R, Del Campo FF, Carpena-Ruiz RO, Hernández LE (2005) Cellular damage induced by cadmium and mercury in Medicago sativa. J Exp Bot 56:2239–2251

    Article  CAS  PubMed  Google Scholar 

  • Panda SK, Patra HK (2000) Nitrate and ammonium ions effect on the chromium toxicity in developing wheat seedlings. Proc Natl Acad Sci India B 70:75–80

    Google Scholar 

  • Panda SK, Yamamoto Y, Kondo H, Matsumoto H (2008) Mitochondrial alterations related to programmed cell death in tobacco cells under aluminium stress. Crit Rev Biol 331:597–610

    CAS  Google Scholar 

  • 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 52:199–223

    Article  CAS  Google Scholar 

  • Pehlivan E, Özkan AM, Dinç S, Parlayici S (2009) Adsorption of Cu2+ and Pb2+ ion on dolomite powder. J Hazard Mater 167:1044–1049

    Article  CAS  PubMed  Google Scholar 

  • Pourrut B, Jean S, Silvestre J, Pinelli E (2011) Lead-induced DNA damage in Vicia faba root cells: potential involvement of oxidative stress. Mutat Res Gen Toxicol Enivron 726:123–128

    Article  CAS  Google Scholar 

  • Richardson JB, Blossey B, Dobson AM (2018) Earthworm impacts on trace metal (Al, Fe, Mo, Cu, Zn, Pb) exchangeability and uptake by young Acer saccharum and Polystichum acrostichoides. Biogeochemistry 138:103–119

    Article  CAS  Google Scholar 

  • Rout GR, Samantaray S, Das P (2000) Effects of chromium and nickel on germination and growth in tolerant and non-tolerant populations of Echinochloa colona (L.) Link. Chemosphere 40:855–859

    Article  CAS  PubMed  Google Scholar 

  • Sagardoy RU, Morales FE, López-Millán AF, Abadía AN, Abadía JA (2009) Effects of zinc toxicity on sugar beet (Beta vulgaris L.) plants grown in hydroponics. Plant Biol 11:339–350

    Article  CAS  PubMed  Google Scholar 

  • Salla V, Hardaway CJ, Sneddon J (2011) Preliminary investigation of Spartina alterniflora for phytoextraction of selected heavy metals in soils from Southwest Louisiana. Microchem J 97:207–212

    Article  CAS  Google Scholar 

  • Saxena S, Kaur H, Verma P, Petla BP, Andugula VR, Majee M (2013) Osmoprotectants: Potential for crop improvement under adverse conditions. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer, New York, pp 197–232

    Chapter  Google Scholar 

  • Schnoor J (1997) Phytoremediation. Technology evaluation report TE-98-01. Ground-Water Remediation Technologies Analysis Center, Pittsburgh, PA, USA

    Google Scholar 

  • Shahid M, Dumat C, Aslam M, Pinelli E (2012) Assessment of lead speciation by organic ligands using speciation models. Chem Speciat Bioavailab 24:248–252

    Article  CAS  Google Scholar 

  • Shanker AK, Djanaguiraman M, Sudhagar R, Chandrashekar CN, Pathmanabhan G (2004) Differential antioxidative response of ascorbate glutathione pathway enzymes and metabolites to chromium speciation stress in green gram (Vigna radiata (L.) R. Wilczek. cv CO4) roots. Plant Sci 166:1035–1043

    Article  CAS  Google Scholar 

  • Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753

    Article  CAS  PubMed  Google Scholar 

  • Sharma I (2012) Arsenic induced oxidative stress in plants. Biologia 67:447–453

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sharma DC, Sharma CP (1993) Chromium uptake and its effects on growth and biological yield of wheat. Cereal Res Commun 21:317–322

    CAS  Google Scholar 

  • Sharma DC, Sharma CP, Tripathi RD (2003) Phytotoxic lesions of chromium in maize. Chemosphere 51:63–68

    Article  CAS  PubMed  Google Scholar 

  • Sharma I, Singh R, Tripathi BN (2007) Biochemistry of arsenic toxicity and tolerance in plants. Biochem Cell Arch 7:165–170

    CAS  Google Scholar 

  • Sha Valli Khan PS, Nagamallaiah GV, Dhanunjay Rao M, Sergeant K, Hausman JF (2014) Emerging technologies and Management of Crop Stress Tolerance. In: Ahmad P, Rasool S (eds) Abiotic stress tolerance in plants: insights from proteomics. Academic Press, pp 23–68. https://doi.org/10.1016/B978-0-12-800875-1.00002-8

    Chapter  Google Scholar 

  • Shi L, Dong H, Reguera G, Beyenal H, Lu A, Liu J, Yu HQ, Fredrickson JK (2016 Oct) Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol 14(10):651

    Article  CAS  PubMed  Google Scholar 

  • Solano BR, Maicas JB, Monero FJG (2008) Physiological and molecular mechanisms of plant growth promoting rhizobacteria (PGPR). In: Ahmad I, Pichtel J, Hayat S (eds) Plant–bacteria interactions. Wiley-VCH, Weinheim, pp 41–52

    Chapter  Google Scholar 

  • Skeffington RA, Shewry PR, Peterson PJ (1976) Chromium uptake and transport in barley seedlings (Hordeum vulgare L.). Planta 132:209–214

    Article  CAS  PubMed  Google Scholar 

  • Stambulska UY, Bayliak MM, Lushchak VI (2018) Chromium (VI) toxicity in legume plants: modulation effects of rhizobial symbiosis. Biomed Res Int. https://doi.org/10.1155/2018/8031213

    Article  CAS  Google Scholar 

  • Suseela MR, Sinha S, Singh S, Saxena R (2002) Accumulation of chromium and scanning electron microscopic studies in Scirpus lacustris L. treated with metal and tannery effluent. Bull Environ Contam Toxicol 68:540–548

    Article  CAS  PubMed  Google Scholar 

  • Talaat NB, Shawky BT (2017) Microbe-mediated induced abiotic stress tolerance responses in plants. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 101–133

    Google Scholar 

  • Tiwari S, Lata C (2018) Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview. Front Plant Sci 9:452

    Article  PubMed  PubMed Central  Google Scholar 

  • Tobin JM (2001) Fungal metal biosorption. Br Mycol Soc Symp Ser 23:424–444

    CAS  Google Scholar 

  • 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 25:158–165. https://doi.org/10.1016/j.tibtech.2007.02.003

    Article  CAS  PubMed  Google Scholar 

  • Tripathi P, Singh PC, Mishra A, Chaudhry V, Mishra S, Tripathi RD, Nautiyal CS (2013) Trichoderma inoculation ameliorates arsenic induced phytotoxic changes in gene expression and stem anatomy of chickpea (Cicer arietinum). Ecotoxicol Environ Saf 89:8–14. https://doi.org/10.1016/j.ecoenv.2012.10.017

    Article  CAS  PubMed  Google Scholar 

  • Tripathi P, Singh PC, Mishra A, Srivastava S, Chauhan R, Awasthi S,  Mishra S, Dwivedi S, Tripathi P, Kalra A, Tripathi RD, Nautiyal CS (2017) Arsenic tolerant Trichoderma sp. reduces arsenic induced stress in chickpea (Cicer arietinum). Environ Pollut 223:137–145. https://doi.org/10.1016/j.envpol.2016.12.073

    Article  CAS  PubMed  Google Scholar 

  • Ullah A, Heng S, Munis MF, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40

    Article  CAS  Google Scholar 

  • Van Assche F, Clijsters H (1986) Inhibition of photosynthesis in Phaseolus vulgaris by treatment with toxic concentrations of zinc: effects on electron transport and photophosphorylation. Physiol Plant 66:717–721

    Article  Google Scholar 

  • Verma S, Verma PK, Meher AK, Dwivedi S, Bansiwal AK, Pande V, Srivastava PK, Verma PC, Tripathi RD, Chakrabarty D (2016) A novel arsenic methyltransferase gene of Westerdykellaaurantiaca isolated from arsenic contaminated soil: phylogenetic, physiological, and biochemical studies and its role in arsenic bioremediation. Metallomics 8:344–353

    Article  CAS  PubMed  Google Scholar 

  • Vivas A, Azcón R, Biró B, Barea JM, Ruiz-Lozano JM (2003) Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense L. under lead toxicity. Can J Microbiol 49:577–588

    Article  CAS  PubMed  Google Scholar 

  • Wannaz ED, Carreras HA, Rodriguez JH, Pignata ML (2012) Use of biomonitors for the identification of heavy metals emission sources. Ecol Indic 20:248–252

    Article  CAS  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol 2011:402647. https://doi.org/10.5402/2011/402647

    Article  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signalling during cold, drought and salt stress. Plant Cell 14:S165–S183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 76:167–179

    Article  CAS  Google Scholar 

  • Yang Y, Yin J, Liu J, Xu Q, Lan T, Ren F, Hao Y (2017) The copper homeostasis transcription factor CopR is involved in H2O2 stress in Lactobacillus plantarum CAUH2. Front Microbiol 8:2015. https://doi.org/10.3389/fmicb.2017.02015

    Article  PubMed  PubMed Central  Google Scholar 

  • Zahir F, Rizwi SJ, Haq SK, Khan RH (2005) Low dose mercury toxicity and human health. Environ Toxicol Pharmacol 20:351–360

    Article  CAS  PubMed  Google Scholar 

  • Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997

    Article  CAS  PubMed  Google Scholar 

  • Zengin FK, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean seedlings. Acta Biol Cracov Ser Bot 47:157–164

    Google Scholar 

  • Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413

    Article  PubMed  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Swamy, M.K., Nalina, N., Nalina, D., Akhtar, M.S., Purushotham, B. (2019). Heavy Metal Stress and Tolerance in Plants Mediated by Rhizospheric Microbes. In: Akhtar, M. (eds) Salt Stress, Microbes, and Plant Interactions: Causes and Solution. Springer, Singapore. https://doi.org/10.1007/978-981-13-8801-9_8

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