Plant–Microbe–Metal (PMM) Interactions and Strategies for Remediating Metal Ions

  • Rahul Mahadev Shelake
  • Rajesh Ramdas Waghunde
  • Jae-Yean Kim


Sessility is a characteristic of plants. Hence, plants have evolved various mechanisms to interact with other organisms in the environment and to deal with biotic or abiotic stresses. One of the contributing factors of abiotic stress is metal ions in plants. Plants and microbes require certain metal ions to complete their life cycle, but all metal ions in excess are toxic. Plant microbiome comprises microbes from different kingdoms which have substantial effects on nutrient uptake, growth, and biotic and abiotic stress tolerance. At various bioavailable concentrations of metal ions, interactions between plant and microbes, generally known as plant–microbe–metal (PMM) interactions, are of interest due to their potential applications in higher crop productivity and metal remediation. Some of the PMM interactions are beneficial under metal stress which enhances uptake, trafficking, sequestration, and detoxification of toxic metal ions by microbe or plant or both the species. This chapter discusses metal homeostasis or metallostasis mechanisms in plants and microbes. Furthermore, the factors affecting PMM interactions, recent techniques for investigating the PMM interactions, metal toxicity and potential use of PMM interactions in metal remediation from the environment are thoroughly described.


Plant–microbe–metal interactions metal homeostasis metal pollution engineered plants hyperaccumulator plants bioremediation 



The authors gratefully acknowledge financial support from the National Research Foundation of Korea, Republic of Korea (Grant #2017R1A4A1015515).


  1. Ai TN, Naing AH, Yun BW et al (2018) Overexpression of RsMYB1 enhances anthocyanin accumulation and heavy metal stress tolerance in transgenic petunia. Front Plant Sci 9:1388PubMedPubMedCentralCrossRefGoogle Scholar
  2. Andresen E, Peiter E, Küpper H (2018) Trace metal metabolism in plants. J Expt Bot 69:909–954CrossRefGoogle Scholar
  3. Arunakumar KK, Walpola BC, Yoon MH (2013) Current status of heavy metal contamination in Asia’s rice lands. Rev Environ Sci and Bio/Technol 12:355–377CrossRefGoogle Scholar
  4. Banakar R, Alvarez Fernández Á, Abadía J, Capell T, Christou P (2017) The expression of heterologous Fe(III) phytosiderophore transporter HvYS1 in rice increases Fe uptake, translocation and seed loading and excludes heavy metals by selective Fe transport. Plant Biotechnol J 15:423–432PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bashir K, Rasheed S, Kobayashi T et al (2016) Regulating subcellular metal homeostasis: the key to crop improvement. Front Plant Sci 7:1192PubMedPubMedCentralCrossRefGoogle Scholar
  6. Basu S, Rabara RC, Negi S, Shukla P (2018) Engineering PGPMOs through gene editing and systems biology: a solution for phytoremediation. Trends Biotechnol 36:499–510PubMedCrossRefPubMedCentralGoogle Scholar
  7. Blindauer CA (2008) Zinc handling in cyanobacteria: an update. Chem Biodivers 5:1990–2013PubMedCrossRefPubMedCentralGoogle Scholar
  8. Brooks RR (1977) Copper and cobalt uptake by Haumaniastrum species. Plant Soil 48:541–544CrossRefGoogle Scholar
  9. Cai SY, Zhang Y et al (2017) HsfA1a upregulates melatonin biosynthesis to confer cadmium tolerance in tomato plants. J Pineal Res 62:e12387CrossRefGoogle Scholar
  10. Capdevila DA, Edmonds KA, Giedroc DP (2017) Metallochaperones and metalloregulation in bacteria. Essays Biochem 61(2):177–200PubMedPubMedCentralCrossRefGoogle Scholar
  11. Chandrangsu P, Rensing C, Helmann JD (2017) Metal homeostasis and resistance in bacteria. Nat Rev Microbiol 15(6):338PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chen B, Luo S, Wu Y et al (2017) The effects of the endophytic bacterium Pseudomonas fluorescens Sasm05 and IAA on the plant growth and cadmium uptake of Sedum alfredii Hance. Front Microbiol 8:2538PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chen H, Zhang C, Guo H, Hu Y, He Y, Jiang D (2018) Overexpression of a Miscanthus sacchariflorus yellow stripe-like transporter MsYSL1 enhances resistance of Arabidopsis to cadmium by mediating metal ion reallocation. Plant Growth Regul 85:101–111CrossRefGoogle Scholar
  14. Das A, Osborne JW (2018) Enhanced lead uptake by an association of plant and earthworm bioaugmented with bacteria. Pedosphere 28:311–322CrossRefGoogle Scholar
  15. Das J, Sarkar P (2018) Remediation of arsenic in mung bean (Vigna radiata) with growth enhancement by unique arsenic-resistant bacterium Acinetobacter lwoffii. Sci Total Environ 624:1106–1118PubMedCrossRefPubMedCentralGoogle Scholar
  16. De Araújo RP, de Almeida AAF, Pereira LS, Mangabeira PA, Souza JO (2017) Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil. Ecotoxicol Environ Saf 144:148–157Google Scholar
  17. Diep P, Mahadevan R, Yakunin A (2018) Heavy metal removal by bioaccumulation using genetically engineered microorganisms. Front Bioeng Biotechnol 6:157PubMedPubMedCentralCrossRefGoogle Scholar
  18. Doran PM (2009) Application of plant tissue cultures in phytoremediation research: Incentives and limitations. Biotechnology and Bioengineering 103:60–76PubMedCrossRefPubMedCentralGoogle Scholar
  19. El-Kady AA, Abdel-Wahhab MA (2018) Occurrence of trace metals in foodstuffs and their health impact. Trends Food Sci Technol 75:36–45CrossRefGoogle Scholar
  20. 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 147:175–191PubMedCrossRefPubMedCentralGoogle Scholar
  21. Fan M, Xiao X, Guo Y et al (2018a) Enhanced phytoremdiation of Robinia pseudoacacia in heavy metal-contaminated soils with rhizobia and the associated bacterial community structure and function. Chemosphere 197:729–740PubMedCrossRefPubMedCentralGoogle Scholar
  22. Fan W, Guo Q, Liu C et al (2018b) Two mulberry phytochelatin synthase genes confer zinc/cadmium tolerance and accumulation in transgenic Arabidopsis and tobacco. Gene 645:95–104PubMedCrossRefPubMedCentralGoogle Scholar
  23. Fasani E, Manara A, Martini F et al (2018) The potential of genetic engineering of plants for the remediation of soils contaminated with heavy metals. Plant Cell Environ 41:1201–1232PubMedCrossRefPubMedCentralGoogle Scholar
  24. Galeas ML, Zhang LH, Freeman JL et al (2006) Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related nonaccumulators. New Phytol 173:517–525CrossRefGoogle Scholar
  25. Gielen H, Vangronsveld J, Cuypers A (2017) Cd-induced Cu deficiency responses in Arabidopsis thaliana: are phytochelatins involved? Plant Cell Environ 40:390–400PubMedCrossRefPubMedCentralGoogle Scholar
  26. Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414CrossRefGoogle Scholar
  27. Gong B, Nie W, Yan Y, Gao Z, Shi Q (2017) Unravelling cadmium toxicity and nitric oxide induced tolerance in Cucumis sativus: Insight into regulatory mechanisms using proteomics. J Hazard Mater 336:202–213PubMedCrossRefPubMedCentralGoogle Scholar
  28. 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 reports 8:4860CrossRefGoogle Scholar
  29. Han Y, Du Y, Wang J, Wu T (2018) Overexpression of Chinese flowering cabbage BpPMSR3 enhances the tolerance of Arabidopsis thaliana to cadmium. J Plant Nutr Soil Sci 181:787–794CrossRefGoogle Scholar
  30. Hou D, Wang R, Gao X et al (2018) Cultivar-specific response of bacterial community to cadmium contamination in the rhizosphere of rice (Oryza sativa L.). Environ Pollut 241:63–73PubMedCrossRefPubMedCentralGoogle Scholar
  31. Hussain A, Kamran MA, Javed MT (2019) Individual and combinatorial application of Kocuria rhizophila and citric acid on phytoextraction of multi-metal contaminated soils by Glycine max L. Environ Exper Bot 159:23–33CrossRefGoogle Scholar
  32. Jaffré T (1979) Accumulation du manganèse par des espèces associées aux terrains ultrabasiques de Nouvelle Calédonie. Comptes Rendus de l'Académie des Sciences Série D: Sciences Naturelles 289:425–428Google Scholar
  33. Joshi R, Pareek A, Singla-Pareek SL (2016) Plant metallothioneins: classification, distribution, function, and regulation. In: Ahmad P (ed) Plant metal interaction: emerging remediation techniques. Elsevier, Amsterdam, pp 239–261CrossRefGoogle Scholar
  34. Kaur P, Singh S, Kumar V, Singh N, Singh J (2018) Effect of rhizobacteria on arsenic uptake by macrophyte Eichhornia crassipes (Mart.) Solms. Int J Phytoremediation 20:114–120PubMedCrossRefGoogle Scholar
  35. Kidwai M, Dhar YV, Gautam N et al (2019) Oryza sativa class III peroxidase (OsPRX38) overexpression in Arabidopsis thaliana reduces arsenic accumulation due to apoplastic lignification. J Hazard Mater 362:383–393PubMedCrossRefGoogle Scholar
  36. LaCoste C, Robinson BH, Brooks RR (1999) The phytoremediation potential of thallium-contaminated soils using Iberis and Biscutella species. Int J Phytoremediation 1:327–338CrossRefGoogle Scholar
  37. Liu H, Zhao H, Wu L et al (2017) Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol 215:687–698PubMedCrossRefGoogle Scholar
  38. Ma L, Komar K, Tu C et al (2001) A fern that hyperaccumulates arsenic. Nature 409:579PubMedCrossRefGoogle Scholar
  39. Ma Z, Jacobsen FE, Giedroc DP (2009) Coordination chemistry of bacterial metal transport and sensing. Chem Rev 109:4644–4681PubMedPubMedCentralCrossRefGoogle Scholar
  40. Mahadev SR, Hayashi H, Ikegami T, Abe S, Morita EH (2013) Improved protein overexpression and purification strategies for structural studies of cyanobacterial metal-responsive transcription factor, SmtB from marine Synechococcus sp. PCC 7002. The Protein J 32:626–634PubMedCrossRefGoogle Scholar
  41. Malaisse F, Grégoire J, Brooks RR et al (1978) Aeolanthus biformifolius De Wild.: a hyperaccumulator of copper from Zaire. Science 199:887–888PubMedCrossRefPubMedCentralGoogle Scholar
  42. Mayerová M, Petrová Š, Madaras M, Lipavský J, Šimon T (2017) Non-enhanced phytoextraction of cadmium, zinc, and lead by high-yielding crops. Environ Sci Pollut Res 24:14706–14716CrossRefGoogle Scholar
  43. Mesjasz-Przybyłowicz J, Nakonieczny M, Migula P et al (2004) Uptake of cadmium, lead nickel and zinc from soil and water solutions by the nickel hyperaccumulator Berkheya coddii. Acta Biol Cracov Series Bot 46:75–85Google Scholar
  44. Nath S, Deb B, Sharma I (2018) Isolation of toxic metal-tolerant bacteria from soil and examination of their bioaugmentation potentiality by pot studies in cadmium-and lead-contaminated soil. Int Microbiol 21:35–45PubMedCrossRefPubMedCentralGoogle Scholar
  45. Ojuederie O, Babalola O (2017) Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res and Public Health 14:1504CrossRefGoogle Scholar
  46. Olaniran A, Balgobind A, Pillay B (2013) Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. Int J Mol Sci 14:10197–10228PubMedPubMedCentralCrossRefGoogle Scholar
  47. Osman D, Cavet JS (2010) Bacterial metal-sensing proteins exemplified by ArsR–SmtB family repressors. Nat Prod Rep 27:668–680PubMedCrossRefPubMedCentralGoogle Scholar
  48. Pan W, Shen J, Zheng Z et al (2018) Overexpression of the Tibetan Plateau annual wild barley (Hordeum spontaneum) HsCIPKs enhances rice tolerance to heavy metal toxicities and other abiotic stresses. Rice 11:51PubMedPubMedCentralCrossRefGoogle Scholar
  49. Peng F, Wang C, Zhu J et al (2018) Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants. Planta 247:1395–1406PubMedCrossRefPubMedCentralGoogle Scholar
  50. Poschenrieder C, Cabot C, Martos S et al (2013) Do toxic ions induce hormesis in plants. Plant Sci 212:15–25PubMedCrossRefPubMedCentralGoogle Scholar
  51. Pourret O, Lange B, Bonhoure J et al (2016) Assessment of soil metal distribution and environmental impact of mining in Katanga (Democratic Republic of Congo). Appl Geochem 64:43–55CrossRefGoogle Scholar
  52. Prosser JI (2002) Molecular and functional diversity in soil microorganisms. Plant Soil 244:9–17CrossRefGoogle Scholar
  53. Rajkumar M, Sandhya S, Prasad MN, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574PubMedCrossRefPubMedCentralGoogle Scholar
  54. Raldugina GN, Maree M, Mattana M et al (2018) Expression of rice OsMyb4 transcription factor improves tolerance to copper or zinc in canola plants. Biol plantarum 62:511–520CrossRefGoogle Scholar
  55. Reboredo F, Simões M, Jorge C et al (2019) Metal content in edible crops and agricultural soils due to intensive use of fertilizers and pesticides in Terras da Costa de Caparica (Portugal). Environ Sci Pollut Res 26:2512–2522PubMedCrossRefPubMedCentralGoogle Scholar
  56. Reeves RD, Brooks RR (1983) Hyperaccumulation of lead and zinc by two metallophytes from mining areas of Central-Europe. Environ Pollut Ser A-Ecol Biol 31:277–285CrossRefGoogle Scholar
  57. Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediation 3:145–172CrossRefGoogle Scholar
  58. Reeves RD, Baker AJ, Jaffré T, Erskine PD, Echevarria G, van der Ent A. (2018) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytologist 218(2):407–411PubMedCrossRefPubMedCentralGoogle Scholar
  59. Rieuwerts JS, Thornton I, Farago ME, Ashmore MR (1998) Factors influencing metal bioavailability in soils: preliminary investigations for the development of a critical loads approach for metals. Chem Spec Bioavailab 10:61–75CrossRefGoogle Scholar
  60. Shan X, Wang H, Zhang S et al (2003) Accumulation and uptake of light rare earth elements in a hyperaccumulator Dicropteris dichotoma. Plant Sci 165:1343–1353CrossRefGoogle Scholar
  61. Shan S, Guo Z, Lei P et al (2019) Simultaneous mitigation of tissue cadmium and lead accumulation in rice via sulfate-reducing bacterium. Ecotoxicol Environ Saf 169:292–300PubMedCrossRefPubMedCentralGoogle Scholar
  62. Shelake RM, Hayashi H, Morita EH (2016) Structural analysis and homology modeling of members of smt-like operon from thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. J Proteins Proteomics 7:221–230Google Scholar
  63. Shelake RM, Waghunde RR, Morita EH, Hayashi H (2018) Plant-microbe-metal interactions: basics, recent advances, and future trends. In: Egamberdieva D, Ahmad P (eds) Plant microbiome: stress response. Microorganisms for sustainability, vol 5. Springer, Singapore, pp 1–5Google Scholar
  64. Shelake RM, Waghunde RR, Verma PP, Singh C, Kim J-Y (2019) Carbon sequestration for soil fertility management: microbiological perspective. In: Panpatte DG, Jhala YK (eds) Soil fertility management for sustainable development. Springer, Singapore. Scholar
  65. Shi X, Zhou G, Liao S, Shan S, Wang G, Guo Z (2018) Immobilization of cadmium by immobilized Alishewanella sp. WH16-1 with alginate-lotus seed pods in pot experiments of Cd-contaminated paddy soil. J Hazard Mater 357:431–439PubMedCrossRefPubMedCentralGoogle Scholar
  66. Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere–microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393PubMedCrossRefPubMedCentralGoogle Scholar
  67. Singh RP, Mishra S, Jha P, Raghuvanshi S, Jha PN (2018) Effect of inoculation of zinc-resistant bacterium Enterobacter ludwigii CDP-14 on growth, biochemical parameters and zinc uptake in wheat (Triticum aestivum L.) plant. Ecol Eng 116:163–173CrossRefGoogle Scholar
  68. Srivastava V, Sarkar A, Singh S et al (2017) Agroecological responses of heavy metal pollution with special emphasis on soil health and plant performances. Front Env Sci 5:64CrossRefGoogle Scholar
  69. Stein RJ, Höreth S, Melo JR et al (2017) Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis halleri. New Phytol 213:1274–1286PubMedCrossRefPubMedCentralGoogle Scholar
  70. Sun L, Ma Y, Wang H et al (2018) Overexpression of PtABCC1 contributes to mercury tolerance and accumulation in Arabidopsis and poplar. Biochem Biophys Res Commun 497:997–1002PubMedCrossRefPubMedCentralGoogle Scholar
  71. Van der Ent A, Baker AJ, Reeves RD et al (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 1:319–334Google Scholar
  72. Waghunde RR, Shelake RM, Shinde MS, Hayashi H (2017) Endophyte microbes: a weapon for plant health management. In: Panpatte D, Jhala Y, Vyas R, Shelat H (eds) Microorganisms for green revolution. Springer, Singapore, pp 303–325CrossRefGoogle Scholar
  73. Waldron KJ, Robinson NJ (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nat Rev Microbiol 7:25–35PubMedCrossRefPubMedCentralGoogle Scholar
  74. Wang XH, Wang Q, Nie ZW, He LY, Sheng XF (2018) Ralstonia eutropha Q2-8 reduces wheat plant above-ground tissue cadmium and arsenic uptake and increases the expression of the plant root cell wall organization and biosynthesis-related proteins. Environ Pollut 242:1488–1499PubMedCrossRefGoogle Scholar
  75. Wang M, Li S, Chen S et al (2019) Manipulation of the rhizosphere bacterial community by biofertilizers is associated with mitigation of cadmium phytotoxicity. Sci Total Environ 649:413–421PubMedCrossRefGoogle Scholar
  76. Wani W, Masoodi KZ, Zaid A et al (2018) Engineering plants for heavy metal stress tolerance. Rendiconti Lincei Scienze Fisiche e Naturali 29:709–723CrossRefGoogle Scholar
  77. Xia Y, Liu J, Wang Y et al (2018) Ectopic expression of Vicia sativa Caffeoyl-CoA O-methyltransferase (VsCCoAOMT) increases the uptake and tolerance of cadmium in Arabidopsis. Environ Exper Bot 145:47–53CrossRefGoogle Scholar
  78. Yadav KK, Gupta N, Kumar A et al (2018) Mechanistic understanding and holistic approach of phytoremediation: a review on application and future prospects. Ecol Eng 120:274–298CrossRefGoogle Scholar
  79. Zhang J, Martinoia E, Lee Y (2018a) Vacuolar transporters for cadmium and arsenic in plants and their applications in phytoremediation and crop development. Plant Cell Physiol 59:1317–1325PubMedGoogle Scholar
  80. Zhang X, Rui H, Zhang F, Hu Z, Xia Y, Shen Z (2018b) Overexpression of a functional Vicia sativa PCS1 homolog increases cadmium tolerance and phytochelatins synthesis in arabidopsis. Front Plant Sci 9:107PubMedPubMedCentralCrossRefGoogle Scholar
  81. Zhou T, Li L, Zhang X et al (2016) Changes in organic carbon and nitrogen in soil with metal pollution by Cd, Cu, Pb and Zn: a meta-analysis. Eur J Soil Sci 67:237–246CrossRefGoogle Scholar
  82. Zornoza R, Acosta JA, Bastida F et al (2015) Identification of sensitive indicators to assess the interrelationship between soil quality, management practices and human health. Soil 1:173–185CrossRefGoogle Scholar
  83. Zygiel EM, Nolan EM (2018) Transition metal sequestration by the host-defense protein calprotectin. Annu Rev Biochem 87:621–643PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Rahul Mahadev Shelake
    • 1
  • Rajesh Ramdas Waghunde
    • 2
  • Jae-Yean Kim
    • 1
  1. 1.Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research CenterGyeongsang National UniversityJinjuSouth Korea
  2. 2.Department of Plant PathologyCollege of Agriculture, Navsari Agricultural UniversityBharuchIndia

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