Advertisement

Symbiotic Microorganisms Enhance Antioxidant Defense in Plants Exposed to Metal/Metalloid-Contaminated Soils

  • Laíze A. F. Vilela
  • Anita F. S. Teixeira
  • Felipe M. O. Lourenço
  • Marta D. Souza
Chapter

Abstract

Symbiotic microorganisms increase plants resistance to metal(oid)s toxicity by various mechanisms, including changes in antioxidant defense system. Apparently, arbuscular mycorrhizal fungi (AMF) and diazotrophic bacteria modify the antioxidant system response to metal(oid)s contamination. There are positive results in enzymatic and non-enzymatic defense systems. AMF can accumulate ROS in your structures (arbuscules, apoplastic spaces of hyphae, fungal cytosol, intracellular hyphae, cell wall of hyphae and spores). These microorganisms up-regulate various antioxidant defense system enzymes such as SOD, CAT, POD, APX, and GR and regulate genes encoding proteins involved in ROS homeostasis. Higher concentrations of non-enzymatic antioxidants (glutathione, flavonoids, ascorbic acid, phenolic compounds, alkaloids, tocopherol, carotenoids) occur more frequently in colonized plants. Future research should prioritize physiological and molecular genetic approaches under metal(loid)s phytotoxicity in plants associated with these microorganisms. Moreover, advanced ultrastructural analysis techniques can support identification of ROS and antioxidant molecules and enzymes distribution in the structures of these microorganisms.

Keywords

Metal tolerance Mycorrhizal symbiosis AM fungi Nitrogen-fixing bacterial Glutathione Reactive oxygen species 

References

  1. Aguiar NO, Medici LO, Olivares FL, Dobbss LB, Torres-Netto A, Silva SF, Novotny EH, Canella LP (2016) Metabolic profile and antioxidant responses during drought stress recovery in sugarcane treated with humic acids and endophytic diazotrophic bacteria. Ann Appl Biol 168:203–213CrossRefGoogle Scholar
  2. Ahmed MMM, Mazen MBD, Nafady NA, Monsef OA (2017) Bioavailability of cadmium and nickel to Daucus carota L. and Corchorus olitorius L. treated by compost and microorganisms. Soil Environ 36:1–12CrossRefGoogle Scholar
  3. Al-Garni SMS (2006) Increased heavy metal tolerance of cowpea plants by dual inoculation of an arbuscular mycorrhizal fungi and nitrogen-fixer Rhizobium bacterium. Afr J Biotechnol 5:133–142Google Scholar
  4. Allah EFA, Hashem A, Alqarawi AA, Hend AA (2015) Alleviation of adverse impact of cadmium stress in sunflower (Helianthus annuus L.) by arbuscular mycorrhizal fungi. Pak J Bot 47:785–795Google Scholar
  5. Alloway BJ (2013) Sources of heavy metals and metalloids in soils. In: Alloway BJ (ed) Heavy metals in soils: trace metals and metalloids in soils and their bioavailability. Springer, New York, pp p11–p50CrossRefGoogle Scholar
  6. Almeida-Rodríguez AM, Gómes MP, Loubert-Hudon A, Joly S, Labrecque M (2015) Symbiotic association between Salix purpurea L. and Rhizophagus irregularis: modulation of plant responses under copper stress. Tree Physiol 36:407–420PubMedCrossRefPubMedCentralGoogle Scholar
  7. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341PubMedCrossRefPubMedCentralGoogle Scholar
  8. Angle JS, Chaney RL (1991) Heavy metal effects on soil populations and heavy metal tolerance of Rhizobium meliloti, nodulation, and growth of alfalfa. Water Air Soil Pollut 57:597–604CrossRefGoogle Scholar
  9. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  10. Awoyemi OM, Dzantor EK (2017) Toxicity of coal fly ash (CFA) and toxicological response of switchgrass in mycorrhiza-mediated CFA-soil admixtures. Ecotoxicol Environ Saf 144:438–444PubMedCrossRefPubMedCentralGoogle Scholar
  11. Balestrass KB, Gallego SM, Tomaro ML (2006) Oxidation of the enzymes involved in nitrogen assimilation plays an important role in the cadmium-induced toxicity in soybean plants. Plant Soil 284:187–194CrossRefGoogle Scholar
  12. Bamberg S, Carneiro MAC, Ramos SJ, Siqueira JO (2016) Selenium and mycorrhiza on grass yield and selenium content. In: Bañuelos G, Lin Z, Moraes M, Guilherme LRG, Reis A (eds) Global advances in selenium research from theory to application. CRC Press, London, pp 137–139Google Scholar
  13. Ban Y, Jiang Y, Li M, Zhang X, Zhang S, Wu Y, Xu Z (2017) Homogenous stands of a wetland grass living in heavy metal polluted wetlands harbor diverse consortia of arbuscular mycorrhizal fungi. Chemosphere 181:699–709PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bedini S, Turrini A, Rigo C, Argese E, Giovannetti M (2010) Molecular characterization and glomalin production of arbuscular mycorrhizal fungi colonizing a heavy metal polluted ash disposal island, downtown Venice. Soil Biol Biochem 42:758–765CrossRefGoogle Scholar
  15. Benabdellah K, Azcón Aguilar C, Valderas A, Speziga D, Fitzpatrick TB, Ferrol N (2009a) GintPDX1 encodes a protein involved in vitamin B6 biosynthesis that is up regulated by oxidative stress in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 184:682–693PubMedCrossRefPubMedCentralGoogle Scholar
  16. Benabdellah K, Merlos MA, Azcón-Aguilar C, Ferrol N (2009b) GintGRX1, the first characterized glomeromycotan glutaredoxin, is a multifunctional enzyme that responds to oxidative stress. Fungal Genet Biol 46:94–103PubMedCrossRefPubMedCentralGoogle Scholar
  17. Bhattacharjee S (2011) Sites of generation and physicochemical basis of formation of reactive oxygen species in plant cell. In: Gupta SD (ed) Reactive oxygen species and antioxidants in higher plants. CRC Press/Science Publishers, Boca Raton, pp 1–30Google Scholar
  18. Biro I, Nemeth T, Takács T (2009) Changes of parameters of infectivity and efficiency of different Glomus mosseae arbuscular mycorrhizal fungi strains in cadmium-loaded soils. Commun Soil Sci Plant Anal 40:227–239CrossRefGoogle Scholar
  19. Bohlool BB, Ladha JK, Garrity DP, George T (1992) Biological nitrogen fixation for sustainable agriculture: a perspective. Plant Soil 141:1–11CrossRefGoogle Scholar
  20. Brígido C, Glick BR, Oliveira S (2017) Survey of plant growth-promoting mechanisms in native portuguese chickpea Mesorhizobium isolates. Microb Ecol 73:900–915CrossRefGoogle Scholar
  21. Checcucci A, Bazzicalupo M, Mengoni A (2017) Exploiting nitrogen-fixing rhizobial symbionts genetic resources for improving phytoremediation of contaminated soils. In: Anjum NA, Gill SS, Tuteja N (eds) Enhancing cleanup of environmental pollutants. Springer, Cham, pp 275–288CrossRefGoogle Scholar
  22. Chen WM, Wu CH, James EK, Chang JS (2008) Metal biosorption capability of Cupriavidus taiwanensis and its effects on heavy metal removal by nodulated Mimosa pudica. J Hazard Mater 151:364–371PubMedCrossRefPubMedCentralGoogle Scholar
  23. Cicatelli A, Torrigiani P, Todeschini V, Biondi S, Castiglione S, Lingua G (2014) Arbuscular mycorrhizal fungi as a tool to ameliorate the phytoremediation potential of poplar: biochemical and molecular aspects. iForest-Biogeosci For 7:1–9CrossRefGoogle Scholar
  24. Davar R, Darvishzadeh R, Majd A (2013) Changes in antioxidant systems in sunflower partial resistant and susceptible lines as affected by Sclerotinia sclerotiorum. Biologia 68:821–829CrossRefGoogle Scholar
  25. Del Val C, Barea J, Ázcon-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65:718–723PubMedPubMedCentralGoogle Scholar
  26. Dhawi F, Datta R, Ramakrishna W (2015) Mycorrhiza and PGPB modulate maize biomass, nutrient uptake and metabolic pathways in maize grown in mining-impacted soil. Plant Physiol Biochem 97:390–399PubMedCrossRefPubMedCentralGoogle Scholar
  27. Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631PubMedCrossRefPubMedCentralGoogle Scholar
  28. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149CrossRefGoogle Scholar
  29. Döbereiner J (1991) The genera Azospirillum and Herbaspirillum. In: Ballows A, Trüper HG, Dworkin M, Harder W, Shleifer K (eds) The prokaryotes. Springer, New York, pp 2236–2253Google Scholar
  30. Dubey RS (2011) Metal toxiciy, oxidative stress and antioxidant defense system in plants. In: Gupta SD (ed) Reactive oxygen species and antioxidants in higher plants. CRC Press/Science Publishers, Boca Raton, pp 177–203Google Scholar
  31. Dutta SC, Neog B (2016) Accumulation of secondary metabolites in response to antioxidant activity of turmeric rhizomes co-inoculated with native arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria. Sci Hortic 204:179–184CrossRefGoogle Scholar
  32. Evelin H, Kapoor R (2014) Arbuscular mycorrhizal symbiosis modulates antioxidant response in salt-stressed Trigonella foenum-graecum plants. Mycorrhiza 24:197–208PubMedCrossRefPubMedCentralGoogle Scholar
  33. 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 338:241–254PubMedCrossRefPubMedCentralGoogle Scholar
  34. Figueira EM, Lima AL, Pereira SI (2005) Cadmium tolerance plasticity in Rhizobium leguminosarum bv. viciae: glutathione as a detoxifying agent. Can J Microbiol 51:7–14PubMedCrossRefPubMedCentralGoogle Scholar
  35. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875PubMedPubMedCentralCrossRefGoogle Scholar
  36. Garg N, Bhandari P (2013) Cadmium toxicity in crop plants and its alleviation by arbuscular mycorrhizal (AM) fungi: an overview. Plant Biosyst- Int J Dealing Asp Plant Biol 148:609–621Google Scholar
  37. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530PubMedCrossRefPubMedCentralGoogle Scholar
  38. Gill M (2014) Heavy metal stress in plants: a review. Springer, BerlinGoogle Scholar
  39. Gillis M, Van TV, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fernandez MP (1995) Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Bacteriol 45:274–289CrossRefGoogle Scholar
  40. González Chavez C, Harris P, Dodd J, Meharg A (2002) Arbuscular mycorrhizal fungi confer enhanced arsenate resistance on Holcus lanatus. New Phytol 155:163–171CrossRefGoogle Scholar
  41. González-Guerrero M, Cano C, Azcón-Aguilar C, Ferrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17:327–335PubMedCrossRefPubMedCentralGoogle Scholar
  42. Gourion B, Berrabah F, Ratet P, Stacey G (2015) Rhizobium–legume symbioses: the crucial role of plant immunity. Trend Plant Sci 20:186–194CrossRefGoogle Scholar
  43. Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  44. Gupta P, Diwan B (2017) Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep 13:58–71CrossRefGoogle Scholar
  45. Hajiboland R (2014) Reactive oxygen species and photosynthesis. In: Ahmad P (ed) Oxidative damage to plants. Academic, New York, pp 1–63Google Scholar
  46. Hall J (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11PubMedCrossRefPubMedCentralGoogle Scholar
  47. 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 16:179–202PubMedCrossRefPubMedCentralGoogle Scholar
  48. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42PubMedCrossRefPubMedCentralGoogle Scholar
  49. Hashem A, Abd_Allah E, Alqarawi A, Al Huqail AA, Egamberdieva D, Wirth S (2016) Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23:272–281PubMedCrossRefPubMedCentralGoogle Scholar
  50. Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Møller IS, White P (2012) Functions of macronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Elsevier, NewYork, pp 135–189CrossRefGoogle Scholar
  51. Heijden MG, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423PubMedCrossRefPubMedCentralGoogle Scholar
  52. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta analysis of context dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407PubMedCrossRefPubMedCentralGoogle Scholar
  53. Hossain MA, Hoque MA, Burritt DJ, Fujita M (2014) Proline protects plants against abiotic oxidative stress: biochemical and molecular mechanisms. In: Ahmad P (ed) Oxidative damage to plants. Academic, New York, pp 1–63Google Scholar
  54. Hristozkova M, Geneva M, Stancheva I, Boychinova M, Djonova E (2016) Contribution of arbuscular mycorrhizal fungi in attenuation of heavy metal impact on Calendula officinalis development. Appl Soil Ecol 101:57–63CrossRefGoogle Scholar
  55. Huang RH, Lub YM, Yanga HL, Huang W, Chena K (2016) Effects of arbuscular mycorrhizal fungi on caesium accumulation and the ascorbate-glutathione cycle of Sorghum halepense. Sci Asia 42:323–331CrossRefGoogle Scholar
  56. Ibiang YB, Mitsumoto H, Sakamoto K (2017) Bradyrhizobia and arbuscular mycorrhizal fungi modulate manganese, iron, phosphorus, and polyphenols in soybean (Glycine max (L.) Merr.) under excess zinc. Environ Exp Bot 137:1–13CrossRefGoogle Scholar
  57. Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2007) Bioremediation of cadmium contaminated soil using symbiosis between leguminous plant and recombinant rhizobia with the MTL4 and the PCS genes. Chemosphere 66:1670–1676PubMedCrossRefPubMedCentralGoogle Scholar
  58. Jacquart A, Brayner R, Chahine JH, Ha-Duong N (2017) Cd2+ and Pb2+ complexation by glutathione and the phytochelatins. Chemico-Biol Interact 267:2–10CrossRefGoogle Scholar
  59. Jiang QY, Tan SY, Zhuo F, Yang DJ, Ye ZH, Jing YX (2016a) Effect of Funneliformis mosseae on the growth, cadmium accumulation and antioxidant activities of Solanum nigrum. Appl Soil Ecol 98:112–120CrossRefGoogle Scholar
  60. Jiang QY, Zhuo F, Long SH, Zhao HD, Yang DJ, Ye ZH, Jing YZ (2016b) Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Sci Rep 6:1–9CrossRefGoogle Scholar
  61. Judy JD, Kirby JK, McLaughlin MJ, McNear D, Bertsch PM (2016) Symbiosis between nitrogen-fixing bacteria and Medicago truncatula is not significantly affected by silver and silver sulfide nanomaterials. Environ Pollut 214:731–736PubMedCrossRefPubMedCentralGoogle Scholar
  62. Kabata-Pendias A (2010) Trace elements in soils and plants. CRC Press, Boca RatonCrossRefGoogle Scholar
  63. Karthik C, Oves M, Sathya K, Ramkumar VS, Arulselvi PI (2017) Isolation and characterization of multi-potential Rhizobium strain ND2 and its plant growth-promoting activities under Cr(VI) stress. Arch Agron Soil Sci 63:1058–1069CrossRefGoogle Scholar
  64. Khade SW, Adholeya A (2009) Arbuscular mycorrhizal association in plants growing on metal-contaminated and noncontaminated soils adjoining Kanpur tanneries, Uttar Pradesh, India. Water Air Soil Pollut 202:45–56CrossRefGoogle Scholar
  65. 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 7:1–19CrossRefGoogle Scholar
  66. Klauberg-Filho O, Siqueira JO, Moreira FMS (2002) Fungos micorrízicos arbusculares em solos de área poluída com metais pesados. Rev Bras Ciênc Solo 26:125–134CrossRefGoogle Scholar
  67. Kong Z, Mohamad OA, Deng Z, Liu X, Glick BR, Wei G (2015) Rhizobial symbiosis effect on the growth, metal uptake, and antioxidant responses of Medicago lupulina under copper stress. Environ Sci Pollut Res 22:12479–12489CrossRefGoogle Scholar
  68. Konieczny A, Kowalska I (2016) The role of arbuscular mycorrhiza in zinc uptake by lettuce grown at two phosphorus levels in the substrate. Agric Food Sci 25:124–137CrossRefGoogle Scholar
  69. Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol 137:1319–1330PubMedPubMedCentralCrossRefGoogle Scholar
  70. Latef AAHA (2011) Influence of arbuscular mycorrhizal fungi and copper on growth, accumulation of osmolyte, mineral nutrition and antioxidant enzyme activity of pepper (Capsicum annuum L.). Mycorrhiza 21:495–503PubMedCrossRefPubMedCentralGoogle Scholar
  71. Latef AAHA (2013) Growth and some physiological activities of pepper (Capsicum annuum L.) in response to cadmium stress and mycorrhizal symbiosis. J Agric Sci Technol 15:1437–1448Google Scholar
  72. Latef AAHA, Hashem A, Rasool S, Abd_Allah EF, Alqarawi AA, Egamberdieva AD, Jan S, Anjum NA, Ahmad P (2016) Arbuscular mycorrhizal symbiosis and abiotic stress in plants: a review. J Plant Biol 59:407–426CrossRefGoogle Scholar
  73. Lea PJ, Miflin BJ (2003) Glutamate synthase and the synthesis of glutamate in plants. Plant Physiol Biochem 41:555–564CrossRefGoogle Scholar
  74. Lima AIG, Corticeiro SC, Figueira EMAP (2006) Glutathione-mediated cadmium sequestration in Rhizobium leguminosarum. Enzym Microb Technol 39:763–769CrossRefGoogle Scholar
  75. Long SR (2016) SnapShot: signaling in symbiosis. Cell 167:582–582PubMedCrossRefPubMedCentralGoogle Scholar
  76. Manjhi BK, Pal S, Meena SK, Yadav RS, Farooqui A, Singh H, Rakshit A (2016) Mycorrhizoremediation of nickel and cadmium: a promising technology. Nat Environ Pollut Technol 15:647–652Google Scholar
  77. MAPA – Ministério de Agricultura, Pecuária e Abastecimento (2011) Instrução normativa SDA n° 13, de 24 de março de 2011. Diário Oficial da República Federativa do Brasil, Poder Executivo, Brasília Available in: http://www.agricultura.gov.br/assuntos/insumos-agropecuarios/insumos-agricolas/fertilizantes/legislacao/in-sda-13-de-24-03-2011-inoculantes.pdf Google Scholar
  78. Maynaud G, Brunel B, Yashiro E, Mergeay M, Cleyet-Marel JC, Le Quéré A (2014) CadA of Mesorhizobium metallidurans isolated from a zinc-rich mining soil is a PIB-2-type ATPase involved in cadmium and zinc resistance. Res Microbiol 165:175–189PubMedCrossRefPubMedCentralGoogle Scholar
  79. Meier S, Borie F, Bolan N, Cornejo P (2012) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42:741–775CrossRefGoogle Scholar
  80. Meneses C, Gonçalves T, Alquéres S, Rouws L, Serrato R, Vidal M, Baldani J (2017) Gluconacetobacter diazotrophicus exopolysaccharide protects bacterial cells against oxidative stress in vitro and during rice plant colonization. Plant Soil 416:133–147CrossRefGoogle Scholar
  81. Merlos MA, Zitka O, Vojtech A, Azcón-Aguilar C, Ferrol N (2016) The arbuscular mycorrhizal fungus Rhizophagus irregularis differentially regulates the copper response of two maize cultivars differing in copper tolerance. Plant Sci 253:68–76PubMedCrossRefPubMedCentralGoogle Scholar
  82. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trend Plant Sci 7:405–410CrossRefGoogle Scholar
  83. Mohamad R, Maynaud G, Le Quéré A, Vidal AC, Klonowska A, Yashiro E, Cleyet-Marel JC, Brunel B (2017) Ancient heavy metal contamination in soils as a driver of tolerant Anthyllis vulneraria rhizobial communities. Appl Environ Microbiol 83:1–13CrossRefGoogle Scholar
  84. Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481PubMedCrossRefPubMedCentralGoogle Scholar
  85. Moore TC (1974) Symbiotic nitrogen fixation in legume nodules. In: Moore TC (ed) Research experiences in plant physiology. Springer, Berlin, pp 417–433CrossRefGoogle Scholar
  86. Moreira FMS, Silva K, Nóbrega RSS, Carvalho F (2010) Bactérias diazotróficas associativas: diversidade, ecologia e potencial de aplicações. Comun Sci 1:74–99Google Scholar
  87. Moreira FMS, Ferreira PAA, Vilela LAF, Carneiro MAC (2015) Symbioses of plants with rhizobia and mycorrhizal fungi in heavy metal-contaminated tropical soils. In: Sherameti I, Varma A (eds) Heavy metal contamination of soils. Springer, Cham, pp 215–243Google Scholar
  88. Nascimento JB, Barrigossi JAF (2014) O papel de enzimas antioxidantes na defesa das plantas contra insetos herbívoros e fitopatógenos. Agrar Acad 1:234–250CrossRefGoogle Scholar
  89. Nelson LM, Knowles R (1978) Effect of oxygen and nitrate on nitrogen fixation and denitrification by Azospirillum brasilense grown in continuous culture. Can J Microbiol 24:1395–1403PubMedCrossRefPubMedCentralGoogle Scholar
  90. Nonnoi F, Chinnaswamy AA, Torre VSG, Peña TC, Lucas MM, Pueyo JJ (2012) Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes (Medicago spp. and Trifolium spp.) growing in mercury-contaminated soils. Appl Soil Ecol 61:49–59CrossRefGoogle Scholar
  91. Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263PubMedCrossRefPubMedCentralGoogle Scholar
  92. Oliveira-Longatti SM, Marra LM, Soares BL, Bomfeti CA, Silva K, Ferreira PAA, Moreira FMS (2014) Bacteria isolated from soils of the western Amazon and from rehabilitated bauxite-mining areas have potential as plant growth promoters. World J Microbiol Biotechnol 30:1239–1250PubMedCrossRefPubMedCentralGoogle Scholar
  93. Pajuelo E, Dary M, Palomares AJ, Rodriguez-Llorente ID, Carrasco JA, Chamber MA (2008) Biorhizoremediation of heavy metals toxicity using rhizobium-legume symbioses. In: Dakora FD, SBM C, Valentine AJ, Elmerich C, Newton WE (eds) Biological nitrogen fixation: towards poverty alleviation through sustainable agriculture. Springer, Dordrecht, pp 101–104CrossRefGoogle Scholar
  94. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775PubMedCrossRefPubMedCentralGoogle Scholar
  95. Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2014) Bacterial associations with legumes. Crit Rev Plant Sci 34:17–42CrossRefGoogle Scholar
  96. Praburaman L, Park SH, Cho M, Lee KJ, Ko JA, Han SS, Lee SH, Kamala-Kannan S, Oh BT (2017) Significance of diazotrophic plant growth-promoting Herbaspirillum sp. GW103 on phytoextraction of Pb and Zn by Zea mays L. Environ Sci Pollut Res 24:3172–3180CrossRefGoogle Scholar
  97. Rangel WM, Schneider J, Souza CE, Sousa SC, Guimarães GL, Souza MF (2014) Phytoprotective effect of arbuscular mycorrhizal fungi species against arsenic toxicity in tropical leguminous species. Int J Phytoremediation 16:840–858CrossRefGoogle Scholar
  98. Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754CrossRefGoogle Scholar
  99. Rozpądek P, Wężowicz K, Stojakowska A, Malarz J, Surówka E, Sobczyk T, Anielska T, Wazny R, Miszalski Z, Turnau K (2014) Mycorrhizal fungi modulate phytochemical production and antioxidant activity of Cichorium intybus L.(Asteraceae) under metal toxicity. Chemosphere 112:217–224PubMedCrossRefPubMedCentralGoogle Scholar
  100. Sánchez-Pardo B, Zornoza P (2014) Mitigation of Cu stress by legume–Rhizobium symbiosis in white lupin and soybean plants. Ecotoxicol Environ Saf 102:1–5PubMedCrossRefPubMedCentralGoogle Scholar
  101. Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Annal Bot 111:743–767CrossRefGoogle Scholar
  102. Sarathambal C, Khankhane PJ, Gharde Y, Kumar B, Varun M, Arun S (2017) The effect of plant growth-promoting rhizobacteria on the growth, physiology, and Cd uptake of Arundo donax L. Int J Phytoremediation 19:360–370PubMedCrossRefPubMedCentralGoogle Scholar
  103. Sarkar A, Asaeda T, Wang Q, Kaneko Y, Rashid MH (2017) Response of Miscanthus sacchariflorus to zinc stress mediated by arbuscular mycorrhizal fungi. Flora 234:60–68CrossRefGoogle Scholar
  104. Scandalios JG (2002) The rise of ROS. Trend Biochem Sci 27:483–486PubMedCrossRefPubMedCentralGoogle Scholar
  105. Schneider J, Stürmer SL, Guilherme LRG, Moreira FMS, Soares CRFS (2013) Arbuscular mycorrhizal fungi in arsenic-contaminated areas in Brazil. J Hazard Mater 262:1105–1115PubMedCrossRefPubMedCentralGoogle Scholar
  106. Schneider J, Bundschuh J, Rangel WM, Guilherme LRG (2017) Potential of different AM fungi (native from As-contaminated and uncontaminated soils) for supporting Leucaena leucocephala growth in As-contaminated soil. Environ Pollut 224:125–135PubMedCrossRefPubMedCentralGoogle Scholar
  107. Shahabivand S, Aliloo AA, Maivan HZ (2016) Wheat biochemical response to cadmium toxicity under Funneliformis mosseae and Piriformospora indica symbiosis. Bot Lithuanica 22:169–177CrossRefGoogle Scholar
  108. Sharma V, Parmar P, Kumari N (2016) Differential cadmium stress tolerance in wheat genotypes under mycorrhizal association. J Plant Nutr 39:2025–2036CrossRefGoogle Scholar
  109. Sharma S, Anand G, Singh N, Kapoor R (2017) Arbuscular mycorrhiza augments arsenic tolerance in wheat (triticum aestivum l.) by strengthening antioxidant defense system and thiol metabolism. Front Plant Sci 8:1–21PubMedPubMedCentralGoogle Scholar
  110. Silva GA, Trufem SFB, Júnior OJS, Maia LC (2005) Arbuscular mycorrhizal fungi in a semiarid copper mining area in Brazil. Mycorrhiza 15:47–53PubMedCrossRefPubMedCentralGoogle Scholar
  111. Silva LR, Pereira MJ, Azevedo J, Mulas R, Velazquez E, González-Andrés F, Valentão P, Andrade PB (2013) Inoculation with Bradyrhizobium japonicum enhances the organic and fatty acids content of soybean (Glycine max (L.) Merrill) seeds. Food Chem 141:3636–3648PubMedCrossRefPubMedCentralGoogle Scholar
  112. Siqueira JO, Soares CRFR, Santos JD, Schneider J, Carneiro MAC (2007) Micorrizas e degradação do solo: caracterização, efeitos e ação recuperadora. In: Ceretta CA, Silva LS, Reichert JM (eds) Tópicos em ciência do solo. Sociedade Brasileira de Ciência do Solo, Viçosa, pp 219–305Google Scholar
  113. Souza T (2015) Handbook of arbuscular mycorrhizal fungi. Springer, New YorkCrossRefGoogle Scholar
  114. Spagnoletti FN, Balestrasse K, Lavado RS, Giacometti R (2016) Arbuscular mycorrhiza detoxifying response against arsenic and pathogenic fungus in soybean. Ecotoxicol Environ Saf 133:47–56PubMedCrossRefPubMedCentralGoogle Scholar
  115. Thirkell TJ, Charters MD, Elliott AJ, Sait SM, Field KJ (2017) Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security. J Ecol 105:921–929CrossRefGoogle Scholar
  116. Vilela LAF (2015) Cério, lantânio, neodímio e ítrio no crescimento de milho na presença e ausência de micorriza em casa de vegetação e da aplicação de mix desses elementos na produção de grãos em campo. Universidade Federal de Lavras, LavrasGoogle Scholar
  117. Wang L, Huang X, Ma F, Ho SH, Wu J, Zhu S (2017) Role of Rhizophagus irregularis in alleviating cadmium toxicity via improving the growth, micro and macroelements uptake in Phragmites australis. Environ Sci Pollut Res 24:3593–3607CrossRefGoogle Scholar
  118. Wani S, Chand S, Ali T (2013) Potential use of Azotobacter chroococcum in crop production: an overview. Curr Agric Res J 1:35–38CrossRefGoogle Scholar
  119. Wei Y, Chen Z, Wu F, Li J, ShangGuan Y, Li F, Zeng QR, Hou H (2015) Diversity of arbuscular mycorrhizal fungi associated with a Sb accumulator plant, ramie (Boehmeria nivea), in an active Sb mining. J Microbiol Biotechnol 25:1205–1215PubMedCrossRefPubMedCentralGoogle Scholar
  120. Weissenhorn I, Glashoff A, Leyval C, Berthelin J (1994) Differential tolerance to Cd and Zn of arbuscular mycorrhizal (AM) fungal spores isolated from heavy metal-polluted and unpolluted soils. Plant Soil 167:189–196CrossRefGoogle Scholar
  121. Wu QS, Zou YN, Abd_Allah EF (2014) Mycorrhizal association and ROS in plants. In: Ahmad (ed) Oxidative damage to plants. Academic, New York, pp 453–475CrossRefGoogle Scholar
  122. Xie P, Hao PX, Herzberg M, Luo Y, Nies DH, Wei G (2015) Genomic analyses of metal resistance genes in three plant growth promoting bacteria of legume plants in Northwest mine tailings, China. J Environ Sci 27:179–187CrossRefGoogle Scholar
  123. Zarei M, Saleh-Rastin N, Jouzani GS, Savaghebi G, Buscot F (2008) Arbuscular mycorrhizal abundance in contaminated soils around a zinc and lead deposit. Eur J Soil Biol 44:381–391CrossRefGoogle Scholar
  124. Zarei M, Hempel S, Wubet T, Schäfer T, Savaghebid G, Jouzanie GS, Nekoueie MK, Buscot F (2010) Molecular diversity of arbuscular mycorrhizal fungi in relation to soil chemical properties and heavy metal contamination. Environ Pollut 158:2757–2765PubMedCrossRefPubMedCentralGoogle Scholar
  125. Zhang J, Xu Y, Cao T, Chen J, Rosen BP, Zhao FJ (2017) Arsenic methylation by a genetically engineered Rhizobium-legume symbiont. Plant Soil 416:259–269PubMedPubMedCentralCrossRefGoogle Scholar
  126. Zou YN, Huang YM, Wu QS, He XH (2015) Mycorrhiza-induced lower oxidative burst is related with higher antioxidant enzyme activities, net H2O2 effluxes, and Ca2+ influxes in trifoliate orange roots under drought stress. Mycorrhiza 25:143–152PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Laíze A. F. Vilela
    • 1
  • Anita F. S. Teixeira
    • 2
  • Felipe M. O. Lourenço
    • 1
  • Marta D. Souza
    • 1
  1. 1.Nature Science CenterFederal University of São CarlosBuriBrazil
  2. 2.Soil Science DepartmentFederal University of LavrasLavrasBrazil

Personalised recommendations