525
Views
4
CrossRef citations to date
0
Altmetric
Articles

Microbe-Assisted Alleviation of Heavy Metal Toxicity in Plants: A Review

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 416-425 | Received 24 Jul 2021, Accepted 07 Sep 2021, Published online: 11 Oct 2021

References

  • Adediran GA, Ngwenya BT, Mosselmans JFW, Heal KV, Harvie BA. 2015. Mechanisms behind bacteria induced plant growth promotion and Zn accumulation in Brassica juncea. J Hazard Mater 283:490–499.
  • Ahmad I, Akhtar MJ, Asghar HN, Ghafoor U, Shahid M. 2016. Differential effects of plant growth-promoting rhizobacteria on maize growth and cadmium uptake. J Plant Growth Regul 35(2):303–315.
  • Alonso MJC, Ortiz CEL, Perez SOG, Narayanasamy R, Miguel G, Hernández HH, Balagurusamy N. 2018. Improved strength and durability of concrete through metabolic activity of ureolytic bacteria. Environ Sci Pollut Res Int 25(22):21451–21458.
  • Amstaetter K, Borch T, Larese-Casanova P, Kappler A. 2010. Redox transformation of arsenic by Fe(II)-activated goethite (alpha-FeOOH)). Environ Sci Technol 44(1):102–108.
  • Atlas RM, Hazen TC. 2011. Oil biodegradation and bioremediation: a tale of the two worst spills in U.S. history. Environ Sci Technol 45(16):6709–6715.
  • Azevedo R, Rodriguez E. 2012. Phytotoxicity of mercury in plants: a review. J Bot 2012:1–6.
  • Barkay T, Schaefer J. 2001. Metal and radionuclide bioremediation: issues, considerations and potentials. Curr Opin Microbiol 4(3):318–323.
  • 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(2):241–250.
  • Bielen A, Remans T, Vangronsveld J, Cuypers A. 2013. The influence of metal stress on the availability and redox state of ascorbate, and possible interference with its cellular functions. Int J Mol Sci 14(3):6382–6413.
  • Costerton JW. 1995. Overview of microbial biofilms. J Ind Microbiol 15:137–140.
  • Chibuike GU, Obiora SC. 2014. Heavy metal polluted soils: effect on plants and bioremediation methods. Appl Environ Soil Sci 2014:1–12.
  • Chuo SC, Mohamed SF, Setaper SHM, Ahmad A, Jawaid M, Wani WA, Yaqoob AA, Ibrahim MNM. 2020. Insights into the current trends in the utilization of bacteria for microbially induced calcium carbonate precipitation. Materials 13:4993.
  • Clemens S, Ma JF. 2016. Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512.
  • Cong W, Miao Y, Xu L, Zhang Y, Yuan C, Wang J, Zhuang T, Lin X, Jiang L, Wang N, et al. 2019. Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.). BMC Plant Biol 19(1):282.
  • Dąbrowska G, Hrynkiewicz K, Trejgell A, Baum C. 2017. The effect of plant growth-promoting rhizobacteria on the phytoextraction of Cd and Zn by Brassica Napus L. Int J Phytoremediation 19(7):597–604.
  • De J, Ramaiah N, Vardanyan L. 2008. Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Mar Biotechnol 10(4):471–477.
  • Dixit P, Mukherjee PK, Ramachandran V, Eapen S. 2011. Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS One 6:e16360.
  • Dutta P, Karmakar A, Majumdar S, Roy S. 2018. Klebsiella pneumoniae (HR1) assisted alleviation of Cd(II) toxicity in Vigna mungo: a case study of biosorption of heavy metal by an endophytic bacterium coupled with plant growth promotion. Euro-Mediterranean J Environ Integr 3:27.
  • Edwards SJ, Kjellerup BV. 2013. Applications of biofilms in bioremediation and biotransformation of persistent organic pollutants, pharmaceuticals/personal care products, and heavy metals. Appl Microbiol Biotechnol 97(23):9909–9921.
  • El-Masry MH, El-Bestawy E, El-Adl NI. 2004. Bioremediation of vegetable oil and grease from polluted wastewater using a sand biofilm system. World J Microbiol Biotechnol 20(6):551–557.
  • Fomina M, Gadd GM. 2014. Biosorption: current perspectives on concept, definition and application. Bioresour Technol 160:3–14.
  • Franchi E, Rolli E, Marasco R, Agazzi G, Borin S, Cosmina P, Pedron F, Rosellini I, Barbafieri M, Petruzzelli G, et al. 2017. Phytoremediation of a multi contaminated soil: mercury and arsenic phytoextraction assisted by mobilizing agent and plant growth promoting bacteria. J Soils Sediments 17(5):1224–1236.
  • Funes Pinter I, Salomon MV, Berli F, Bottini R, Piccoli P. 2017. Characterization of the As(III) tolerance conferred by plant growth promoting rhizobacteria to in vitro-grown grapevine. Appl Soil Ecol 109:60–68.
  • Gao Y, Miao C, Mao L, Zhou P, Jin Z, Shi W. 2010. Improvement of phytoextraction and antioxidative defense in Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid. J Hazard Mater 181(1–3):771–777.
  • Gavrilescu M. 2004. Removal of heavy metals from the environment by biosorption. Eng Life Sci 4(3):219–232.
  • Ghosh S, Bal B, Das AP. 2018. Enhancing manganese recovery from low grade ores by using mixed culture of indigenously isolated bacterial strains. Geomicrobiol J 35(3):242–246.
  • Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930.
  • 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 Growth Regul 35(4):1000–1012.
  • Gorospe CM, Han SH, Kim SG, Park JY, Kang CH, Jeong JH, So JS. 2013. Effects of different calcium salts on calcium carbonate crystal formation by Sporosarcina pasteurii KCTC 3558. Biotechnol Bioproc E 18(5):903–908.
  • Grujić S, Vasić S, Radojević I, Čomić L, Ostojić A. 2017. Comparison of the Rhodotorula mucilaginosa biofilm and planktonic culture on heavy metal susceptibility and removal potential. Water Air Soil Pollut 228(2):73.
  • Guiné V, Spadini L, Sarret G, Muris M, Delolme C, Gaudet J-P, Martins JMF. 2006. Zinc sorption to three gram-negative bacteria: combined titration, modeling, and EXAFS study. Environ Sci Technol 40(6):1806–1813.
  • Gupta DK, Chatterjee S, Datta S, Veer V, Walther C. 2014. Role of phosphate fertilizers in heavy metal uptake and detoxification of toxic metals. Chemosphere 108:134–144.
  • Gutiérrez-Corona JF, Romo-Rodríguez P, Santos-Escobar F, Espino-Saldaña AE, Hernández-Escoto H. 2016. Microbial interactions with chromium: basic biological processes and applications in environmental biotechnology. World J Microbiol Biotechnol 32:191.
  • Han H, Sheng X, Hu J, He L, Wang Q. 2018. Metal-immobilizing Serratia liquefaciens CL-1 and Bacillus thuringiensis X30 increase biomass and reduce heavy metal accumulation of radish under field conditions. Ecotoxicol Environ Saf 161:526–533.
  • 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(7):1119–1128.
  • Hao X, Taghavi S, Xie P, Orbach MJ, Alwathnani HA, Rensing C, Wei G. 2014. Phytoremediation of heavy and transition metals aided by legume-rhizobia symbiosis. Int J Phytoremediation 16(2):179–202.
  • 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 Phytoremediation 19(6):522–529.
  • He HJ, Xiang ZH, Chen XJ, Chen H, Huang H, Wen M, Yang CP. 2018. Biosorption of Cd(II) from synthetic wastewater using dry biofilms from biotrickling filters. Int J Environ Sci Technol 15(7):1491–1500.
  • He H, Ye Z, Yang D, Yan J, Xiao L, Zhong T, Yuan M, Cai X, Fang Z, Jing Y, et al. 2013. Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere 90(6):1960–1965.
  • 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(2):114–122.
  • Hu J, Wu S, Wu F, Leung HM, Lin X, Wong MH. 2013. Arbuscular mycorrhizal fungi enhance both absorption and stabilization of Cd by Alfred stonecrop (Sedum alfredii Hance) and perennial ryegrass (Lolium perenne L.) in a Cd-contaminated acidic soil. Chemosphere 93(7):1359–1365.
  • Ibuot A, Dean AP, McIntosh OA, Pittman JK. 2017. Metal bioremediation by CrMTP4 over-expressing Chlamydomonas reinhardtii in comparison to natural wastewatertolerant microalgae strains. Algal Res 24:89–96.
  • Igiri BE, Okoduwa SIR, Idoko GO, Akabuogu EP, Adeyi AO, Ejiogu IK. 2018. Toxicity and bioremediation of heavy metals contaminated ecosystem from tannery wastewater: a review. J Toxicol 2018:2568038.
  • Jagodzik P, Tajdel-Zielinska M, Ciesla A, Marczak M, Ludwikow A. 2018. Mitogen-activated protein kinase cascades in plant hormone signaling. Front Plant Sci 9:1387.
  • Jain D, Kour R, Bhojiya AA, Meena RH, Singh A, Mohanty SR, Rajpurohit D, Ameta KD. 2020. Zinc tolerant plant growth promoting bacteria alleviates phytotoxic effects of zinc on maize through zinc immobilization. Sci Rep 10:13865.
  • Jalilvand N, Akhgar A, Alikhani HA, Rahmani HA, Rejali F. 2020. Removal of heavy metals zinc, lead, and cadmium by biomineralization of urease-producing bacteria isolated from Iranian mine calcareous soils. J Soil Sci Plant Nutr 20(1):206–219.
  • Jiang J, Pan C, Xiao A, Yang X, Zhang G. 2017. Isolation, identification, and environmental adaptability of heavy-metal-resistant bacteria from ramie rhizosphere soil around mine refinery. 3 Biotech 7(1):5.
  • Jin Y, Luan Y, Ning Y, Wang L. 2018. Effect and mechanism of microbial remediation of heavy metals in soil: a critical review. Appl Sci 8(8):1336.
  • Karn SK, Duan J, Jenkinson IR. 2017. Book review: role of biofilms in bioremediation. Front Environ Sci 5:22.
  • Khanna K, Jamwal VL, Gandhi SG, Ohri P, Bhardwaj R. 2019. Metal resistant PGPR lowered Cd uptake and expression of metal transporter genes with improved growth and photosynthetic pigments in Lycopersicon esculentum under metal toxicity. Sci Rep 9:5855.
  • Kumar S, Dubey RS, Tripathi RD, Chakrabarty D, Trivedi PK. 2015. Omics and biotechnology of arsenic stress and detoxification in plants: current updates and prospective. Environ Int 74:221–230.
  • Kumar S, Trivedi PK. 2016. Heavy metal stress signaling in plants. In: Ahmad, P, editor. Plant Metal Interaction. Amsterdam: Elsevier, p585–603.
  • Lermen C, Morelli F, Gazim ZC, Silva A. P d, Gonçalves JE, Dragunski DC, Alberton O. 2015. Essential oil content and chemical composition of Cymbopogon citratus inoculated with arbuscular mycorrhizal fungi under different levels of lead. Ind Crops Prod 76:734–738.
  • Li R, Wu H, Ding J, Fu W, Gan L, Li Y. 2017. Mercury pollution in vegetables, grains and soils from areas surrounding coal-fired power plants. Sci Rep 7:46545.
  • Li J, Zhang M, Sun J, Mao X, Wang J, Liu H, Zheng H, Li X, Zhao H, Zou D, et al. 2020. Heavy metal stress-associated proteins in rice and arabidopsis: genome-wide identification, phylogenetics, duplication, and expression profiles analysis. Front Genet 11:477.
  • Lin CC, Lin HL. 2005. Remediation of soil contaminated with the heavy metal (Cd2+). J Hazard Mater 122(1–2):7–15.
  • Liu J, Wang F, Wu W, Wan J, Yang J, Xiang S, Wu Y. 2018. Biosorption of high-concentration Cu (II) by periphytic biofilms and the development of a fiber periphyton bioreactor (FPBR). Bioresour Technol 248(Pt B):127–134.
  • Lloyd JR, Gadd GM. 2011. The geomicrobiology of radionuclides. Geomicrobiol J 28(5–6):383–386.
  • Luo Q, Wang S, Sun LN, Wang H. 2017. Metabolic profiling of root exudates from two ecotypes of Sedum alfredii treated with Pb based on GC-MS. Sci Rep 7:39878.
  • Ma Y, Oliveira RS, Freitas H, Zhang C. 2016. Biochemical and molecular mechanisms of plant-microbe-metal interactions: relevance for phytoremediation. Front Plant Sci 7:918.
  • 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 A 78(13–14):931–944.
  • Ma Y, Prasad MNV, Rajkumar M, Freitas H. 2011. Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29(2):248–258.
  • Ma L, Wang F, Yu Y, Liu J, Wu Y. 2018. Cu removal and response mechanisms of periphytic biofilms in a tubular bioreactor. Bioresour Technol 248(Pt B):61–67.
  • Malik A. 2004. Metal bioremediation through growing cells. Environ Int 30(2):261–278.
  • Mallick I, Bhattacharyya C, Mukherji S, Dey D, Sarkar SC, Mukhopadhyay UK, Ghosh A. 2018. Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: a step towards arsenic rhizoremediation. Sci Total Environ 610–611:1239–1250.
  • Mateos LM, Villadangos AF, de la Rubia AG, Mourenza A, Marcos-Pascual L, Letek M, Pedre B, Messens J, Gil JA. 2017. The arsenic detoxification system in corynebacteria: basis and application for bioremediation and redox control. Adv Appl Microbiol 99:103–137.
  • Miransari M. 2011. Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol Adv 29(6):645–653.
  • 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.
  • Mohanty S, Ghosh S, Nayak S, Das AP. 2017. Isolation, identification and screening of manganese solubilizing fungi from low-grade manganese ore deposits. Geomicrobiol J 34(4):309–316.
  • Mondal NK, Das C, Datta JK. 2015. Effect of mercury on seedling growth, nodulation and ultrastructural deformation of Vigna radiata (L) Wilczek. Environ Monit Assess 187(5):241.
  • Montero-Palmero MB, Ortega-Villasante C, Escobar C, HernáNdez LE. 2014. Are plant endogenous factors like ethylene modulators of the early oxidative stress induced by mercury? Front Environ Sci 2:34.
  • Mosa KA, Saadoun I, Kumar K, Helmy M, Dhankher OP. 2016. Potential biotechnological strategies for the cleanup of heavy metals and metalloids. Front Plant Sci 7:303.
  • Nanda S, Nayak S, Joshi RK. 2014. Molecular cloning and expression analysis of four turmeric MAP kinase genes in response to abiotic stresses and phytohormones. Biol Plant 58:479–490. https://doi.org/10.1007/s10535-014-0429-2
  • Neumann RB, Ashfaque KN, Badruzzaman ABM, Ashraf Ali M, Shoemaker JK, Harvey CF. 2010. Anthropogenic influences on groundwater arsenic concentrations in Bangladesh. Nature Geosci 3(1):46–52.
  • Niedoba T, Hołda A, Kisielowska E. 2010. Removal of heavy metals from coal medium with application of biotechnological methods. Górnictwo i Geoinżynieria 34:93–104.
  • Pandey S, Ghosh PK, Ghosh S, De TK, Maiti TK. 2013. Role of heavy metal resistant Ochrobactrum sp. and Bacillus spp. strains in bioremediation of a rice cultivar and their PGPR like activities. J Microbiol 51(1):11–17.
  • Pokethitiyook P, Poolpak T. 2016. Biosorption of heavy metal from aqueous solutions. In: Ansari, AA, Gill, SS, Gill, R, Lanza, GR, Newman, L, editors. Phytoremediation. Cham: Springer International Publishing, p113–141.
  • 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 726(2):123–128.
  • Pramanik K, Mitra S, Sarkar A, Soren T, Maiti TK. 2017. Characterization of cadmium-resistant Klebsiella pneumoniae MCC 3091 promoted rice seedling growth by alleviating phytotoxicity of cadmium. Environ Sci Pollut Res 24(31):24419–24437.
  • Rai KK, Pandey N, Meena RP, Rai SP. 2021. Biotechnological strategies for enhancing heavy metal tolerance in neglected and underutilized legume crops: a comprehensive review. Ecotoxicol Environ Saf 208:111750.
  • Rangel WM, Thijs S, Janssen J, Oliveira Longatti SM, Bonaldi DS, Ribeiro PRA, Jambon I, Eevers N, Weyens N, Vangronsveld J, et al. 2017. Native rhizobia from Zn mining soil promote the growth of Leucaena leucocephala on contaminated soil. Int J Phytoremediation 19(2):142–156.
  • Ruscitti M, Arango M, Beltrano J. 2017. Improvement of copper stress tolerance in pepper plants (Capsicum annuum L.) by inoculation with arbuscular mycorrhizal fungi. Theor Exp Plant Physiol 29(1):37–49.
  • Sanket AS, Ghosh S, Sahoo R, Nayak S, Das AP. 2017. Identification of acidophilic manganese (Mn) solubilizing bacteria from mining effluents and their application in mineral beneficiation. Geomicrobiol J 34(1):71–80.
  • Sarma H, Islam NF, Prasad R, Prasad MNV, Ma LQ, Rinklebe J. 2021. Enhancing phytoremediation of hazardous metal(loid)s using genome engineering CRISPR-Cas9 technology. J Hazard Mater 414:125493.
  • Sharma PK, Balkwill DL, Frenkel A, Vairavamurthy MA. 2000. A new Klebsiella planticola strain (Cd-1) grows anaerobically at high cadmium concentrations and precipitates cadmium sulfide. Appl Environ Microbiol 66(7):3083–3087.
  • Shi L, Dong H, Reguera G, Beyenal H, Lu A, Liu J, Yu H-Q, Fredrickson JK. 2016. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol 14(10):651–662.
  • Shin M-N, Shim J, You Y, Myung H, Bang K-S, Cho M, Kamala-Kannan S, Oh B-T. 2012. Characterization of lead resistant endophytic Bacillus sp. MN3-4 and its potential for promoting lead accumulation in metal hyperaccumulator Alnus firma. J Hazard Mater 199–200:314–320.
  • Siddiquee S, Rovina K, Azad SA. 2015. Heavy metal contaminants removal from wastewater using the potential filamentous fungi biomass: a review. J Microb Biochem Technol 7:6.
  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM. 2015. Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143.
  • Steinhorst L, Kudla J. 2014. Signaling in cells and organisms – calcium holds the line . Curr Opin Plant Biol 22:14–21.
  • Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV. 2013. Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35(4):985–999.
  • 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 2011:1–31.
  • Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ. 2012. Heavy metal toxicity and the environment. Mol Clin Environ Toxicol 101:133–164.
  • Tiwari S, Lata C. 2018. Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview. Front Plant Sci 9:452.
  • Verma S, Verma PK, Meher AK, Bansiwal AK, Tripathi RD, Chakrabarty D. 2018. A novel fungal arsenic methyltransferase, WaarsM reduces grain arsenic accumulation in transgenic rice (Oryza sativa L.). J Hazard Mater 344:626–634.
  • Verma PK, Verma S, Pande V. 2016. Overexpression of rice glutaredoxin OsGrx_C7 and OsGrx_C2.1 reduces intracellular arsenic accumulation and increases tolerance in Arabidopsis thaliana. Front Plant Sci 7:740.
  • Wang Q, Chen L, He LY, Sheng XF. 2016. Increased biomass and reduced heavy metal accumulation of edible tissues of vegetable crops in the presence of plant growth-promoting Neorhizobium huautlense T1-17 and biochar. Agric Ecosyst Environ 228:9–18.
  • Wang Q, Zhang WJ, He LY, Sheng XF. 2018. Increased biomass and quality and reduced heavy metal accumulation of edible tissues of vegetables in the presence of Cd-tolerant and immobilizing Bacillus megaterium H3. Ecotoxicol Environ Saf 148:269–274.
  • Wu G, Kang H, Zhang X, Shao H, Chu L, Ruan C. 2010. A critical review on the bio-removal of hazardous heavy metals from contaminated soils: issues, progress, eco-environmental concerns and opportunities. J Hazard Mater 174(1–3):1–8.
  • Wuana RA, Okieimen FE. 2011. Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol 2011:1–20.
  • Xu M, Liu Y, Deng Y, Zhang S, Hao X, Zhu P, Zhou J, Yin H, Liang Y, Liu H, et al. 2020. Bioremediation of cadmium-contaminated paddy soil using an autotrophic and heterotrophic mixture. RSC Adv 10(44):26090–26101.
  • Zaidi S, Usmani S, Singh BR, Musarrat J. 2006. Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64(6):991–997.
  • Zhang M, Chiang Y-H, Toruño TY, Lee D, Ma M, Liang X, Lal NK, Lemos M, Lu Y-J, Ma S, et al. 2018. The MAP4 kinase SIK1 ensures robust extracellular ROS burst and antibacterial immunity in plants. Cell Host Microbe 24(3):379–391.e5.
  • Zhang X, Xia H, Li Z, Zhuang P, Gao B. 2011. Identification of a new potential Cd-hyperaccumulator Solanum photeinocarpum by soil seed bank-metal concentration gradient method. J Hazard Mater 189(1–2):414–419.
  • Zhang K, Xue Y, Xu H, Yao Y. 2019. Lead removal by phosphate solubilizing bacteria isolated from soil through biomineralization. Chemosphere 224:272–279.
  • Zhou ZS, Wang SJ, Yang ZM. 2008. Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere 70(8):1500–1509.
  • Zhuang P, Lu H, Li Z, Zou B, McBride MB. 2014. Multiple exposure and effects assessment of heavy metals in the population near mining area in South China. PLoS One 9(4):e94484.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.