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Cadmium Stress Tolerance in Plants and Role of Beneficial Soil Microorganisms

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Phyto and Rhizo Remediation

Abstract

Heavy metal stress triggers anomalies in the plant metabolic activity thereby reducing the yield potential of the crop plants. Cadmium (Cd) is one of the toxic heavy metals that is continuously added to the soil through natural as well as anthropogenic means and once taken up by plants can inhibit plant growth and development. Cd toxicity causes problem in uptake and metabolism of essential mineral elements as a result of reduced enzyme activity and protein synthesis. It has been observed that essential mineral nutrients and the available soil Cd show direct competition for the transport proteins. In addition, Cd alters with the sulfhydryl group of proteins resulting in reduced enzyme activity. Soilborne microorganisms include all actively metabolizing organisms directly or indirectly associated with the improvement of soil health and the existing flora. Among the soilborne beneficial microorganisms, arbuscular mycorrhizal fungi (AMF) and plant growth-promoting rhizobacteria (PGPR) have been widely accepted for their growth-promoting role. Optimization of important physiological and biochemical processes in plants can be achieved by the soilborne microorganisms. Hence exploiting their unique properties including stress tolerance via synthesis of compatible solutes and phytohormones, biocontrol agents, etc. should be exploited. The present review discusses the role of beneficial soil microorganisms in alleviating the effects of Cd stress in crop plants.

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References

  • Abd_Allah EF, Hashem A, Alqarawi AA, Alwathnani HA (2015) Alleviation of adverse impact of cadmium stress in sunflower (Helianthus annuus L.) by arbuscular mycorrhizal fungi. Pak J Bot 47(2):785–795

    CAS  Google Scholar 

  • Abd_Allah EF, Hashem A, Alqarawi AA, Wirth S, Egamberdieva D (2017) Calcium application enhances growth and alleviates the damaging effects induced by Cd stress in sesame (Sesamum indicum L.). J Plant Interact 12(1):237–243

    Article  CAS  Google Scholar 

  • Ahanger MA, Hashem A, Abd_Allah EF, Ahmad P (2014) Arbuscular mycorrhiza in crop improvement under environmental stress. In: Ahmad P, Rasool S (eds) Emerging technologies and management of crop stress tolerance, vol 2. Academic, San Diego, pp 69–95

    Chapter  Google Scholar 

  • Ahemad M, Khan MS (2011a) Response of green gram [Vigna radiata (L.) Wilczek] grown in herbicide-amended soil to quizalafop-p-ethyl and clodinafop tolerant plant growth promoting Bradyrhizobium sp. (vigna) MRM6. J Agric Sci Technol 13:1209–1222

    CAS  Google Scholar 

  • Ahemad M, Khan MS (2011b) Pseudomonas aeruginosa strain PS1 enhances growth parameters of green gram [Vigna radiata (L.) Wilczek] in insecticide-stressed soils. J Pest Sci 84:123–131

    Article  Google Scholar 

  • Ahemad M, Khan MS (2012a) Effect of fungicides on plant growth promoting activities of phosphate solubilizing Pseudomonas putida isolated from mustard (Brassica compestris) rhizosphere. Chemosphere 86:945–950

    Article  CAS  Google Scholar 

  • Ahemad M, Khan MS (2012b) Productivity of greengram in tebuconazole-stressed soil, by using a tolerant and plant growth promoting Bradyrhizobium sp. MRM6 strain. Acta Physiol Plant 34:245–254

    Article  CAS  Google Scholar 

  • Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [(Brassica juncea L.) Czern. & Coss.] plants can be alleviated by salicylic acid. S Afr J Bot 77:36–44

    Article  CAS  Google Scholar 

  • Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran LS (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS One 10(1):e0114571

    Article  CAS  Google Scholar 

  • Ahmad P, Ahanger MA, Egamberdieva D, Alam P, Alyemeni MN, Ashraf M (2018) Modification of osmolytes and antioxidant enzymes by 24-epibrassinolide in chickpea seedlings under mercury (Hg) toxicity. J Plant Growth Regul 37:309–322

    Article  CAS  Google Scholar 

  • Aina R, Labra M, Fumagalli P, Vannini C, Marsoni M, Cucchi U, Bracale M, Sgorbati S, Citterio S (2007) Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots. Environ Exp Bot 59(3):381–392

    Article  CAS  Google Scholar 

  • Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269

    Article  Google Scholar 

  • Alqarawi AA, Abd_Allah EF, Hashem A (2014) Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J Plant Interact 9(1):802–810

    Article  CAS  Google Scholar 

  • Alwhibi MS, Hashem A, Abd_Allah EF, Alqarawi AA, DWK S, Wirth S, Egamberdieva D (2017) Increased resistance of drought by Trichoderma harzianum fungal treatment correlates with increased secondary metabolites and proline content. J Integr Agric 16(8):1751–1757

    Article  Google Scholar 

  • Alyemeni MN, Ahanger MA, Wijaya L, Alam P, Ahmad P (2017) Contrasting tolerance among soybean genotypes subjected to different levels of cadmium stress. Pak J Bot 49(3):903–911

    CAS  Google Scholar 

  • Asgher M, Khan NA, Khan MIR, Fatma M, Masood A (2014) Ethylene production is associated with alleviation of cadmium-induced oxidative stress by sulfur in mustard types differing in ethylene sensitivity. Ecotoxicol Environ Saf 106:54–61

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–221

    Article  CAS  Google Scholar 

  • Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19(2):90–98

    Article  CAS  Google Scholar 

  • Bak JC, Gzyl J, Sobkowiak RR, Jelonek MA, Deckert J (2014) The new insights into cadmium sensing. Front Plant Sci 5:245

    Google Scholar 

  • Bharti N, Yadav D, Barnawal D, Maji D, Kalra A (2013) Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J Microbiol Biotechnol 29:379–387

    Article  CAS  Google Scholar 

  • Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep 6:34768

    Article  CAS  Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350

    Article  CAS  Google Scholar 

  • Blanvillain R, Kim JH, Wu S, Lima A, Ow DW (2009) OXIDATIVE STRESS 3 is a chromatin-associated factor involved in tolerance to heavy metals and oxidative stress. Plant J 57(4):654–665

    Article  CAS  Google Scholar 

  • Candido VC, Campanelli G, D’Addabbo T, Castronuovo D, Perniola M, Camele I (2015) Growth and yield promoting effect of artificial mycorrhization on field tomato at different irrigation regimes. Sci Hortic 187:35–43

    Article  Google Scholar 

  • Chen YX, He YF, Yang Y, Yu YL, Zheng SJ, Tian GM, Luo YM, Wong MH (2003) Effect of cadmium on nodulation and N2-fixation of soybean in contaminated soils. Chemosphere 50(6):781–787

    Article  CAS  Google Scholar 

  • Chen Z, Ma S, Liu LL (2008) Studies on phosphorus solubilizing activity of a strain of phosphobacteria isolated from chestnut type soil in China. Bioresour Technol 99:6702–6707

    Article  CAS  Google Scholar 

  • Cheng J, Qiu H, Chang Z, Jiang Z, Yin W (2016) The effect of cadmium on the growth and antioxidant response for freshwater algae Chlorella vulgaris. Springerplus 5(1):1290

    Article  CAS  Google Scholar 

  • Chetty KN, Drummond L, Desaiah D (1980) Effect of cadmium on ATPase activities in rats fed on iron-deficient and sufficient diets. J Environ Sci Health B 15(4):379–393

    Article  CAS  Google Scholar 

  • Chiboub M, Jebara SH, Saadani O, Fatnassi IC, Abdelkerim S, Jebara M (2018) Physiological responses and antioxidant enzyme changes in Sulla coronaria inoculated by cadmium resistant bacteria. J Plant Res 131(1):99–110

    Article  CAS  Google Scholar 

  • Chibuike GU, Obiora SC (2014) Heavy metal polluted soils: effect on plants and bioremediation methods. Appl Environ Soil Sci. Article ID 752708, 12 pages

    Google Scholar 

  • De Sousa CAF, Sodek L (2003) Alanine metabolism and alanine aminotransferase activity in soybean (Glycine max) during hypoxia of the root system and sub-sequent return to Normoxia. Environ Exp Bot 50(1):1–8

    Article  CAS  Google Scholar 

  • Dimkpa C, Weinand T, ASch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694

    Article  CAS  Google Scholar 

  • Djebali W, Zarrouk M, Brouquisse R, El Kahoui S, Limam F, Ghorbel MH, Chaibi W (2005) Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes. Plant Biol 7:358–368

    Article  CAS  Google Scholar 

  • Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci. World J 2015. Article ID 756120, 18 pages

    Google Scholar 

  • Fatnassi IC, Chiboub M, Saadani O, Jebara M, Jebara SH (2015) Impact of dual inoculation with rhizobium and PGPR on growth and antioxidant status of Vicia faba L. under copper stress. C R Biol 338(4):241–254

    Article  Google Scholar 

  • Feng J, Shi Q, Wang X, Wei M, Yang F, Xu H (2010) Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic 123(4):521–530

    Article  CAS  Google Scholar 

  • Gamalero E, Lingua G, Berta G, Glick BR (2009) Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress. Can J Microbiol 55:501–514

    Article  CAS  Google Scholar 

  • Garg N, Chandel S (2011) The effects of salinity on nitrogen fixation and trehalose metabolism in mycorrhizal Cajanus cajan (L.) Millsp plants. J Plant Growth Regul 30:490–503

    Article  CAS  Google Scholar 

  • Garg N, Singla P (2012) The role of Glomus mosseae on key physiological and biochemical parameters of pea plants grown in arsenic contaminated soil. Sci Hortic 14:92–101

    Article  CAS  Google Scholar 

  • Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A (2013) Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 117:106–114

    Article  Google Scholar 

  • Giri J (2011) Glycine betaine and abiotic stress tolerance in plants. Plant Signal Behav 6(11):1746–1751

    Article  CAS  Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

    Article  CAS  Google Scholar 

  • Hameed A, Wu QS, Abd_Allah EF, Hashem A, Kumar A, Lone HA, Ahmad P (2014) Role of AM fungi in alleviating drought stress in plants. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses. Springer Science+Business Media, New York

    Google Scholar 

  • Haneef I, Faizan S, Perveen R, Kausar S (2014) Impact of bio-fertilizers and different levels of cadmium on the growth, biochemical contents and lipid peroxidation of Plantago ovata Forsk. Saudi J Biol Sci 21:305–310

    Article  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  Google Scholar 

  • Hashem A, Abd_Allah EF, Alqarawi AA, El-Didamony G, Alwhibi Mona S, Egamberdieva D, Ahmad P (2014) Alleviation of adverse impact of salinity on faba bean (Vicia faba L.) by arbuscular mycorrhizal fungi. Pak J Bot 46(6):2003–2013

    Google Scholar 

  • Hashem A, Abd_Allah EF, Alqarawi AA, Aldubise A, Egamberdieva D (2015) Arbuscular mycorrhizal fungi enhances salinity tolerance of Panicum turgidum Forssk by altering photosynthetic and antioxidant pathways. J Plant Interact 10(1):230–242

    Article  Google Scholar 

  • Hashem A, Abd_Allah EF, Alqarawi AA, Al Huqail AA, Wirth S, Egamberdieva D (2016a) Alleviation of cadmium stress in Solanum lycopersicum L by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23(2):272–281

    Article  CAS  Google Scholar 

  • Hashem A, Abd_Allah EF, Alqarawi AA, Al-Huqail AA, Shah MA (2016b) Induction of osmoregulation and modulation of salt stress in Acacia gerrardii Benth. by arbuscular mycorrhizal fungi and Bacillus subtilis (BERA 71). Bio Med Res Int 2016:1–11

    Google Scholar 

  • Hashem A, Abd_Allah EF, Alqarawi AA, Al-Huqail AA, Wirth S, Egamberdieva D (2016c) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol 7:1089

    Article  Google Scholar 

  • Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598

    Article  Google Scholar 

  • Hinsinger P, Plassard C, Jaillard B (2006) Rhizosphere: a new frontier for soil biogeochemistry. J Geochem Explor 88(1–3):210–213

    Article  CAS  Google Scholar 

  • Hossain Z, Mandal AKA, Datta SK, Biswas AK (2006) Isolation of a NaCl tolerant mutant of Chrysanthemum morifolium by gamma radiation: in vitro mutagenesis and selection by salt stress. Funct Plant Biol 33:91–101

    Article  CAS  Google Scholar 

  • Janicka-Russak M, Kabała K, Burzyński M (2012) Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. J Exp Bot 63(11):4133–4142

    Article  CAS  Google Scholar 

  • Jha Y, Subramanian RB, Patel S (2011) Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol Plant 33:797–802

    Article  Google Scholar 

  • Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants. 3rd ed. CRC Press, Boca Raton. https://www.crcpress.com/Trace-Elements-in-Soils-and-Plants-Third-Edition/Kabata-Pendias/p/book/9780849315756

    Book  Google Scholar 

  • Kamran MA, Syed JH, Eqani SAMAS, Munis MFH, Chaudhary HJ (2015) Effect of plant growth-promoting rhizobacteria inoculation on cadmium (Cd) uptake by Eruca sativa. Environ Sci Pollut Res 22(12):9275–9283

    Article  CAS  Google Scholar 

  • Kamran MA, Eqani SAMAS, Bibi S, Xu R, Amna MMFH, Katsoyiannis A, Bokhari H, Chaudhary JH (2016) Bioaccumulation of nickel by E. sativa and role of plant growth promoting rhizobacteria (PGPRs) under nickel stress. Ecotoxicol Environ Saf 126:256–263

    Article  CAS  Google Scholar 

  • Kang BG, Kim WT, Yun HS, Chang SC (2010) Use of plant growth-promoting rhizobacteria to control stress responses of plant roots. Plant Biotechnol Rep 4:179–183

    Article  Google Scholar 

  • Kathuria H, Giri J, Nataraja KN, Murata N, Udayakumar M, Tyagi AK (2009) Glycine betaine induced water stress tolerance in cod A-expressing transgenic rice is associated with up regulation of several stress responsive genes. Plant Biotechnol J 7:512–526

    Article  CAS  Google Scholar 

  • Khan MIR, Khan NA (2014) Ethylene reverses photosynthetic inhibition by nickel and zinc in mustard through changes in PS II activity, photosynthetic nitrogen use efficiency, and antioxidant metabolism. Protoplasma 251:1007–1019

    Article  CAS  Google Scholar 

  • Khan MS, Zaidi A, Wani PA (2006) Role of phosphate solubilizing microorganisms in sustainable agriculture – a review. Agron Sustain Dev 27:29–43

    Article  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 7:1–19

    Article  CAS  Google Scholar 

  • Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

    Article  CAS  Google Scholar 

  • Khan WU, Yasin NA, Ahmad SR, Ali A, Amad A, Akram W, Faisal M (2018) Role of Burkholderia cepacia CS8 in Cd-stress alleviation and phytoremediation by Catharanthus roseus. Int J Phytoremediation 20:581–592

    Article  CAS  Google Scholar 

  • Kim J, Rees DC (1994) Nitrogenase and biological nitrogen fixation. Biochemist 33:389–397

    Article  CAS  Google Scholar 

  • Kim JH, Rhee JS, Lee JS, Dahms HU, Lee J, Han KN, Lee JS (2010) Effect of cadmium exposure on expression of antioxidant gene transcripts in the river pufferfish, Takifugu obscurus (Tetraodontiformes). Comp Biochem Physiol C Toxicol Pharma 152(4):473–479

    Article  CAS  Google Scholar 

  • Kloepper JW, Zablotowick RM, Tipping EM, Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister DL, Cregan PB (eds) The Rhizosphere and plant growth. Kluwer Academic Publishers, Dordrecht, pp 315–326

    Google Scholar 

  • Korenkov V, Hirschi K, Weld JDC, Wagner GJ (2007) Enhancing Tonoplast Cd/H Antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L. Planta 226(6):1379–1387

    Article  CAS  Google Scholar 

  • Korir H, Mungai NW, Thuita M, Hamba Y, Masso C (2017) Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil. Front Plant Sci 8:141

    Article  Google Scholar 

  • Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40(1):37–44

    Article  CAS  Google Scholar 

  • Kotoky R, Nath S, Maheshwari DK, Pandey P (2019) Cadmium resistant plant growth promoting rhizobacteria Serratia marcescens S2I7 associated with the growth promotion of rice plant. Environ Sustain 2:135–144. https://doi.org/10.1007/s42398-019-00055-3

    Article  CAS  Google Scholar 

  • Kramer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581(12):2263–2272

    Article  CAS  Google Scholar 

  • Kruger M, Kruger C, Walker C, Stockinger H, Schubler A (2012) Phylogenetic reference data for systematic and phytotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984

    Article  Google Scholar 

  • Kuo C, Kao H (2004) Antioxidant enzyme activities are up regulated in response to cadmium in sensitive, but not in tolerant, rice (Oryza sativa) seedlings. Bot Bull Acad Sin 45:291–299

    CAS  Google Scholar 

  • Li Y, Liu X, Hao T, Chen S (2017) Colonization and maize growth promotion induced by phosphate solubilizing bacterial isolates. Int J Mol Sci 18:1253

    Article  CAS  Google Scholar 

  • Llamas A, Ullrich CI, Sanz A (2000) Cd2+ effects on transmembrane electrical potential difference, respiration and membrane permeability of rice (Oryza sativa L.) roots. Plant Soil 219(1–2):21–28

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Luo Y, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants-effects on plant growth and Ni uptake. J Hazard Mater 195:230–237

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25

    Article  CAS  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572

    Article  CAS  Google Scholar 

  • Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Singh DP, Prabha R, Sahu PK, Gupta VK, Singh HB, Krishanani KK, Minhas PS (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:172

    Article  Google Scholar 

  • Mitra S, Pramanik K, Sarkar A, Ghosh PK, Soren T, Maiti TK (2018a) Bioaccumulation of cadmium by Enterobacter sp and enhancement of rice seedling growth under cadmium stress. Ecotoxicol Environ Safe 156:183–196

    Article  CAS  Google Scholar 

  • Mitra S, Pramanik K, Ghosh PK, Soren T, Sarkar A, Dey RS, Pandey S, Maiti TK (2018b) Characterization of Cd-resistant Klebsiella michiganensis MCC3089 and its potential for rice seedling growth promotion under Cd stress. Microbiol Res 210:12–25

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  Google Scholar 

  • Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164(5):601–610

    Article  CAS  Google Scholar 

  • Montanini B, Blaudez D, Jeandroz S, Sanders D, Chalot M (2007) Phylogenetic and functional analysis of the cation diffusion facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 8:107. https://doi.org/10.1186/1471-2164-8-107

    Article  CAS  Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can J Microbiol 53:1141–1149

    Article  CAS  Google Scholar 

  • Nadeem S, Maqshoof A, Zahir Z, 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  Google Scholar 

  • Nardi S, Concheri G, Pizzeghello D, Sturaro A, Rella R, Parvoli G (2000) Soil organic matter mobilization by root exudates. Chemosphere 5:653–658

    Article  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Khan MIR, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489

    Article  CAS  Google Scholar 

  • Neumann G, Bott S, Ohler MA, Mock HP, Lippmann R, Grosch R, Smalla K (2014) Root exudation and root development of lettuce (Lactuca sativa L. cv. Tizian) as affected by different soils. Front Microbiol 5:2

    CAS  Google Scholar 

  • Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta 1763(7):609–620

    Article  CAS  Google Scholar 

  • Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745

    Article  Google Scholar 

  • Ouariti O, Boussama N, Zarrouk M, Cherif A, Ghorbal MH (1997) Cadmium and copper induced changes in tomato membrane lipids. Phytorochemistry 45(7):1343–1350

    Article  CAS  Google Scholar 

  • Pantazis V, Kalavrouziotis I, Deligiannakis I (2007) Cu-Zn accumulation on soil plant system irrigated with wastewater. Proceedings in IWA facing sludge diversities: challenges, risks and opportunities. Antalya, Turkey, pp 673–680

    Google Scholar 

  • Papageorgiou GC, Murata N (1995) The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynth Res 44:243–252

    Article  CAS  Google Scholar 

  • Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136(3):3814–3823

    Article  CAS  Google Scholar 

  • Per TS, Khan NA, Masood A, Fatma M (2016) Methyl jasmonate alleviates cadmium-induced photosynthetic damages through increased S-assimilation and glutathione production in mustard. Front Plant Sci 7:1933

    Article  Google Scholar 

  • Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32(4):539–548

    Article  CAS  Google Scholar 

  • Poonguzhali S, Madhaiyan M, Sa T (2008) Isolation and identification of phosphate solubilizing bacteria from chinese cabbage and their effect on growth and phosphorus utilization of plants. J Microbiol Biotechnol 18:773–777

    CAS  Google Scholar 

  • Pramanik K, Mitra S, Sarkar A, Maiti TK (2018) Alleviation of phytotoxic effects of cadmium on rice seedlings by cadmium resistant PGPR strain Enterobacter aerogenes MCC 3092. J Hazard Mater 351:317–329

    Article  CAS  Google Scholar 

  • Rangel WM, Thijs S, Janssen J, Oliveira Longatti SM, Bonaldi DS, Ribeiro PR, Jambon I, Eevers N, Weyens N, Vangronsveld J, Moreira FM (2017) Native rhizobia from Zn mining soil promote the growth of Leucaena leucocephala on contaminated soil. Int J Phytoremediation 19(2):142–156

    Article  CAS  Google Scholar 

  • Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554

    Article  CAS  Google Scholar 

  • Santoyo G, Moreno-Hagelsieb G, del Carmen O-MM, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  CAS  Google Scholar 

  • Sarwar N, Saifullah S, Malhi S, Zia MH, Naeem A, Bibi S, Farida G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90(6):925–937

    CAS  Google Scholar 

  • Scagel CF, Bryla DR (2017) Salt exclusion and mycorrhizal symbiosis increase tolerance to NaCl and CaCl2 salinity in ‘Siam Queen’ Basil. Hortic Sci 52(2):278–287

    CAS  Google Scholar 

  • Shaharoona B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Appl Microbiol Biotechnol 79:147–155

    Article  CAS  Google Scholar 

  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2015a) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143

    Google Scholar 

  • Singh RR, Pathak B, Fulekar MH (2015b) Characterization of PGP traits by heavy metals tolerant Pseudomonas putida and Bacillus safensis strain isolated from rhizospheric zone of weed (Phyllanthus urinaria) and its efficiency in cd and Pb. Int J Curr Microbiol App Sci 4(7):954–975

    CAS  Google Scholar 

  • Singh RP, Shelke GM, Kumar A, Jha PN (2015c) Biochemistry and genetics of ACC deaminase: a weapon to “stress ethylene” produced in plants. Front Microbiol 6:937

    Google Scholar 

  • Sirhindi G, Mir MA, Abd_Allah EF, Ahmad P, Gucel S (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in Glycine max under nickel toxicity. Front Plant Sci 7:591

    Article  Google Scholar 

  • Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3(4):a001438

    Article  CAS  Google Scholar 

  • Stefan M, Munteanu N, Stoleru V, Mihasan M (2013) Effects of inoculation with plant growth promoting rhizobacteria on photosynthesis, antioxidant status and yield of runner bean. Rom Biotechnol Lett 18(2):8132–8143

    CAS  Google Scholar 

  • Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  Google Scholar 

  • Tamas L, Dudíková J, Ďurčeková K, Haluškov L, Huttová J, Mistrík I (2009) Effect of cadmium and temperature on the lipoxygenase activity in barley root tip. Protoplasma 235:17

    Article  CAS  Google Scholar 

  • Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5:51–58

    Article  CAS  Google Scholar 

  • Tao GC, Tian SJ, Cai MY, Xie GH (2008) Phosphate solubilizing and -mineralizing abilities of bacteria isolated from. Pedosphere 18:515–523

    Article  CAS  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  Google Scholar 

  • Thomine S, Lelievre F, Debarbieux F, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34(5):685–695

    Article  CAS  Google Scholar 

  • Tian F, Wang W, Liang C, Wang X, Wang G, Wang W (2017) Over-accumulation of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress. Crop J 5:73–82

    Article  Google Scholar 

  • Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. Mutat Res 681:134–149

    Article  CAS  Google Scholar 

  • Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma JF (2009) A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol 182(3):644–653

    Article  CAS  Google Scholar 

  • Unyayar S, Değer AG, Çelik A, Çekiç FÖ, Çevik S (2010) Cadmium-induced antioxidant status and sister-chromatid exchanges in Vicia faba L. Turk J Biol 34(4):413–422

    CAS  Google Scholar 

  • Upadhyay SK, Singh JS, Saxena AK, Singh DP (2012) Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol 14:605–611

    Article  CAS  Google Scholar 

  • Vahter M, Berglund M, Slorach S, Friberg L, Saric M, Zheng XQ, Fujita M (1991) Methods for integrated exposure monitoring of lead and cadmium. Environ Res 56(1):78–89

    Article  CAS  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181(4):759–776

    Article  CAS  Google Scholar 

  • Verdoy D, Coba De La Pena T, Redondo FJ, Lucas MM, Pueyo JJ (2006) Transgenic Medicago truncatula plants that accumulate proline display nitrogen-fixing activity with enhanced tolerance to osmotic stress. Plant Cell Environ 29(10):1913–1923

    Article  CAS  Google Scholar 

  • Vurukonda SSKP, Vardharajula S, Shrivastava M, Sk ZA (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24

    Article  Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS (2010) Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem Toxicol 48:3262–3267

    Article  CAS  Google Scholar 

  • Wei T, Lv X, Jia HL, Hua L, Xu HH, Zhou R, Zhao J, Ren XH, Guo JK (2018) Effects of salicylic acid, Fe (II) and plant growth-promoting bacteria on Cd accumulation and toxicity alleviation of Cd tolerant and sensitive tomato genotypes. J Environ Manag 214:164–171

    Article  CAS  Google Scholar 

  • Wong CKE, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181(1):71–78

    Article  CAS  Google Scholar 

  • Wood JL, Liu W, Tang C, Franks AE (2016) Microorganisms in heavy metal bioremediation: strategies for applying microbial-community engineering to remediate soils. AIMS Bioeng 3(2):211–229. https://doi.org/10.3934/bioeng.2016.2.211

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN (2017) Arbuscular mycorrhizal fungi and tolerance of drought stress in plants. In: Wu QS (ed) Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore. https://doi.org/10.1007/978-981-10-4115-0_2

    Chapter  Google Scholar 

  • Wu H, Chen C, Du J, Liu H, Cui Y, Zhang Y, He Y, Wang Y, Chu C, Feng Z, Li J, Ling HQ (2012) Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis-enhanced cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiol 158:790–800

    Article  CAS  Google Scholar 

  • Yang Y, Han X, Liang Y, Ghosh A, Chen J, Tang M (2015) The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS One 10(12):e0145726

    Article  CAS  Google Scholar 

  • Yedidia I, Srivastva AK, Kapulnik Y, Chet I (2001) Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil 235:235–242

    Article  CAS  Google Scholar 

  • Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J 30:529–539

    Article  CAS  Google Scholar 

  • Yoshihara T, Hodoshima H, Miyano Y, Shoji K, Shimada H, Goto F (2006) Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants. Plant Cell Rep 25(4):365–373

    Article  CAS  Google Scholar 

  • Zafar-Ul-Hye M, Shahjahan A, Danish S, Abid M, Qayyum M (2018) Mitigation of cadmium toxicity induced stress in wheat by acc-deaminase containing pgpr isolated from cadmium polluted wheat rhizosphere. Pak J Bot 50:1727–1734

    CAS  Google Scholar 

  • Zahir ZA, Munir A, Asghar HN, Shaharoona B, Arshad M (2008) Effectiveness of rhizobacteria containing ACC-deaminase for growth promotion of pea (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18:958–963

    CAS  Google Scholar 

  • Zaidi A, Khan MS (2005) Interactive effect of rhizospheric microorganisms on growth, yield and nutrient uptake of wheat. J Plant Nutr 28:2079–2092

    Article  CAS  Google Scholar 

  • Zaidi A, Khan MS, Ahemad M, Oves M (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Immunol Hung 56:263–284

    Article  CAS  Google Scholar 

  • Zhai Z, Gayomba ZR, Jung H, Vimalakumari NK, Pineros M, Craft E, Rutzke MA, Danku J, Lahner B, Punshon T, Guerinot ML, Salt ME, Kochian LV, Vatamaniuk OK (2016) OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis. Plant Cell 29(7):1–16

    Google Scholar 

  • Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Zak JC, Dowd SE, Paré PW (2010) Choline and osmotic stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant-Microbe Interact 23:1097–1104

    Article  CAS  Google Scholar 

  • Zhang F, Wan X, Zheng Y, Sun L, Chen Q, Zhu X, Guo Y, Liu M (2014) Effects of nitrogen on the activity of antioxidant enzymes and gene expression in leaves of Populus plants subjected to cadmium stress. J Plant Interact 9(1):599–609

    Article  CAS  Google Scholar 

  • Zhifang G, Loescher WH (2003) Expression of a celery mannose 6-phosphate reductase in Arabidopsis thaliana enhances salt tolerance and induces biosynthesis of both mannitol and a glucosyl-mannitol dimmer. Plant Cell Environ 26:275–283

    Article  CAS  Google Scholar 

  • Zhou C, Zhu L, Ma Z, Wang J (2017) Bacillus amyloliquefaciens SAY09 increases cadmium resistance in plants by activation of auxin-mediated signaling pathways. Genes 8:173

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for its funding to the Research Group number (RG-1435-014).

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Correspondence to Elsayed Fathi Abd_Allah .

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Hashem, A., Alqarawi, A.A., Al-Hazzani, A.A., Egamberdieva, D., Tabassum, B., Abd_Allah, E.F. (2019). Cadmium Stress Tolerance in Plants and Role of Beneficial Soil Microorganisms. In: Arora, N., Kumar, N. (eds) Phyto and Rhizo Remediation. Microorganisms for Sustainability, vol 9. Springer, Singapore. https://doi.org/10.1007/978-981-32-9664-0_9

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