Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes, and Effects of Heavy Metals

  • Uliana Ya. StambulskaEmail author
  • Maria M. BayliakEmail author
Reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)


Leguminous plants are able to establish symbiosis with a group of nitrogen-fixing soil bacteria called collectively rhizobia. This symbiosis leads to the formation of root nodules, specialized structures within which bacteria carry out nitrogen fixation. Both rhizobia and host legumes exhibit a strong specificity, which can be a result of their coevolution. Symbiotic specificity is provided by the complex exchange of signals between both symbiotic partners. To initiate symbiosis, legumes produce a cocktail of flavonoids that trigger synthesis and secretion of bacterial lipochgitooligosaccharide molecules called Nod factors. Nod factors together with surface polysaccharides and secreted proteins are proposed to be major rhizobial determinants of host specificity. Much evidence suggests that reactive oxygen species (ROS) play a key role in the formation and functioning of legume-rhizobium symbiosis. Elevated levels of heavy metals in soils can affect rhizobial growth and host legumes as well as impair legume-rhizobium symbiosis, in particular due to enhanced ROS production. On the other hand, if plants form symbiosis with rhizobia, heavy metals are accumulated preferentially in nodules that can be one of the possible ways to reduce toxic effects of heavy metals to legumes.


Rhizobium Chemotaxis Nodule development, Nod factors Surface polysaccharides Phytohormones ROS Oxidative stress Bioremediation 



Extracellular polysaccharide


Indole-3-acetic acid






Reactive nitrogen species


Reactive oxygen species


  1. 1.
    Gibson KE, Kobayashi H, Walker GC (2008) Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42:413–441. Scholar
  2. 2.
    Dos Santos P, Fang Z, Mason SW, Setubal JC, Dixon R (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13:1–12. Scholar
  3. 3.
    Mus F, Crook MB, Garcia K, Garcia Costas A, Geddes BA, Kouri ED, Paramasivan P, Ryu M-H, Oldroyd GED, Poole PS, Udvardi MK, Voigt CA, Ané J-M, Peters JW (2016) Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microbiol 82:3698–3710. Scholar
  4. 4.
    Martinez-Romero E (2009) Controversies in science coevolution in Rhizobium-legume symbiosis? DNA Cell Biol 28:361–370. Scholar
  5. 5.
    Coba de la Peña T, Fedorova E, Pueyo JJ, Lucas MM (2018) The symbiosome: legume and rhizobia co-evolution toward a nitrogen-fixing organelle? Front Plant Sci 8:1–26. Scholar
  6. 6.
    Halbleib CM, Ludden PW (2000) Regulation of biological nitrogen fixation. J Nutr 130:1081–1084. Scholar
  7. 7.
    Dupont L, Alloing G, Pierre O, El S, Hopkins J, Hrouart D, Frendo P (2012) The legume root nodule: from symbiotic nitrogen fixation to senescence. In: Nagata T (ed) Senescence. IntechOpen. Scholar
  8. 8.
    Clúa J, Roda C, Zanetti ME, Blanco FA (2018) Compatibility between legumes and rhizobia for the establishment of a successful nitrogen-fixing symbiosis. Genes (Basel):9.
  9. 9.
    Yang C, Bueckert R, Schoenau J, Diederichsen A, Zakeri H, Warkentin T (2017) Symbiosis of selected Rhizobium leguminosarum bv. viciae strains with diverse pea genotypes: effects on biological nitrogen fixation. Can J Microbiol 63:909–919. Scholar
  10. 10.
    Silveira JAG, Figueiredo MDVB, Cavalvcanti FR, Ferreira-Silva SL (2011) Legume nodule oxidative stress and N2 fixation efficiency. In: de Araújo ASF, Figueiredo MVB (eds) Microbial ecology of tropical soils. Nova Science Pub Inc, UK, pp 49–78Google Scholar
  11. 11.
    Brencic A, Winans SC (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 69:155–194. Scholar
  12. 12.
    Wang Q, Liu J, Zhu H (2018) Genetic and molecular mechanisms underlying symbiotic specificity in legume-rhizobium interactions. Front Plant Sci 9:1–8. Scholar
  13. 13.
    Li B, Li Y-Y, Wu H-M, Zhang F-F, Li C-J, Li X-X, Lambers H, Li L (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proc Natl Acad Sci 113:6496–6501. Scholar
  14. 14.
    Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. Scholar
  15. 15.
    Stambul’s’ka UI, Lushchak VI (2009) Chemotaxis of Rhizobium leguminosarum bv. viciae to organic substances. Mikrobiol Z 71:47–54PubMedGoogle Scholar
  16. 16.
    Liu Y, Jiang X, Guan D, Zhou W, Ma M, Zhao B, Cao F, Li L, Li J (2017) Transcriptional analysis of genes involved in competitive nodulation in Bradyrhizobium diazoefficiens at the presence of soybean root exudates. Sci Rep 7:1–11. Scholar
  17. 17.
    Liu C-W, Murray J (2016) The role of flavonoids in nodulation host-range specificity: an update. Plants 5:33. Scholar
  18. 18.
    Cooper JE (2004) Multiple responses of rhizobia to flavonoids during legume root infection. In: Incorporating advances in plant pathology. Academic, Amsterdam, pp 1–62Google Scholar
  19. 19.
    Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular. Dialogue 103:1355–1365. Scholar
  20. 20.
    Janczarek M, Rachwał K, Marzec A, Grzadziel J, Palusińska-Szysz M (2014) Signal molecules and cell-surface components involved in early stages of the legume-rhizobium interactions. Appl Soil Ecol 85:94–113. Scholar
  21. 21.
    Long SR (2001) Genes and signals in the rhizobium-legume symbiosis. Plant Physiol 125:69–72. Scholar
  22. 22.
    Debellé F, Moulin L, Mangin B, Dénarié J, Boivin C (2001) Nod genes and Nod signals and the evolution of the rhizobium legume symbiosis. Acta Biochim Pol 48:359–365PubMedCrossRefGoogle Scholar
  23. 23.
    Nelson MS, Sadowsky MJ (2015) Secretion systems and signal exchange between nitrogen-fixing rhizobia and legumes. Front Plant Sci 6:1–11. Scholar
  24. 24.
    Ferguson BJ, Mathesius U (2014) Phytohormone regulation of legume-rhizobia interactions. J Chem Ecol 40:770–790. Scholar
  25. 25.
    Miri M, Janakirama P, Held M, Ross L, Szczyglowski K (2016) Into the root: how cytokinin controls rhizobial infection. Trends Plant Sci 21:178–186. Scholar
  26. 26.
    Foo E, McAdam EL, Weller JL, Reid JB (2016) Interactions between ethylene, gibberellins, and brassinosteroids in the development of rhizobial and mycorrhizal symbioses of pea. J Exp Bot 67:2413–2424. Scholar
  27. 27.
    Kohlen W, Ng JLP, Deinum EE, Mathesius U (2018) Auxin transport, metabolism, and signalling during nodule initiation: indeterminate and determinate nodules. J Exp Bot 69:229–244. Scholar
  28. 28.
    Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Factories 5:1–19. Scholar
  29. 29.
    Rinaudi LV, Gonzalez JE (2009) The low-molecular-weight fraction of exopolysaccharide II from Sinorhizobium meliloti is a crucial determinant of biofilm formation. J Bacteriol 191:7216–7224. Scholar
  30. 30.
    Carlson RW, Forsberg LS, Kannenberg EL (2010) Lipopolysaccharides in rhizobium-legume symbioses. In: Wang X, Quinn PJ (eds) Endotoxins: structure, function and recognition. Springer, Dordrecht, pp 339–386CrossRefGoogle Scholar
  31. 31.
    Marczak M, Mazur A, Koper P, Żebracki K, Skorupska A (2017) Synthesis of rhizobial exopolysaccharides and their importance for symbiosis with legume plants. Genes (Basel) 8:10–12. Scholar
  32. 32.
    Lohar DP, Haridas S, Gantt JS, VandenBosch KA (2007) A transient decrease in reactive oxygen species in roots leads to root hair deformation in the legume-rhizobia symbiosis. New Phytol 173:39–49. Scholar
  33. 33.
    Glian’ko AK, Akimova GP, Makarova LE, Sokolova MG, Vasil’eva GG (2007) Oxidation processes at initial stages of interaction of root nodule bacteria (Rhizobium leguminosarum) and pea (Pisum sativum L.): a review. Prikl Biokhim Mikrobiol 43:576–582PubMedGoogle Scholar
  34. 34.
    Glian’ko AK, Vasil’eva GG (2010) Reactive oxygen and nitrogen species in legume-rhizobial symbiosis: a review. Prikl Biokhim Mikrobiol 46:21–28PubMedGoogle Scholar
  35. 35.
    Cardenas L, Martinez A, Sanchez F, Quinto C (2008) Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). Plant J 56:802–813. Scholar
  36. 36.
    Chang C, Damiani I, Puppo A, Frendo P (2009) Redox changes during the legume-rhizobium symbiosis. Mol Plant 2:370–377. Scholar
  37. 37.
    Munoz V, Ibanez F, Tordable M, Megias M, Fabra A (2015) Role of reactive oxygen species generation and Nod factors during the early symbiotic interaction between bradyrhizobia and peanut, a legume infected by crack entry. J Appl Microbiol 118:182–192. Scholar
  38. 38.
    Santos R, Hérouart D, Puppo A, Touati D (2000) Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis. Mol Microbiol 38:750–759. Scholar
  39. 39.
    Matamoros MA, Dalton DA, Ramos J, Clemente MR, Rubio MC, Becana M (2003) Update on plant antioxidants biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis 1, 2. Society 133:499–509. Scholar
  40. 40.
    Matamoros MA, Saiz A, Peñuelas M, Bustos-Sanmamed P, Mulet JM, Barja MV, Rouhier N, Moore M, James EK, Dietz KJ, Becana M (2015) Function of glutathione peroxidases in legume root nodules. J Exp Bot 66:2979–2990. Scholar
  41. 41.
    Pauly N, Pucciariello C, Mandon K, Innocenti G, Jamet A, Baudouin E, Hérouart D, Frendo P, Puppo A (2006) Reactive oxygen and nitrogen species and glutathione: key players in the legume-Rhizobium symbiosis. J Exp Bot 57:1769–1776. Scholar
  42. 42.
    Becana M, Dalton DA, Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC (2000) Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381CrossRefGoogle Scholar
  43. 43.
    Andrio E, Marino D, Marmeys A, de Segonzac MD, Damiani I, Genre A, Huguet S, Frendo P, Puppo A, Pauly N (2013) Hydrogen peroxide-regulated genes in the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 198:179–189. Scholar
  44. 44.
    Puppo A, Pauly N, Boscari A, Mandon K, Brouquisse R (2013) Hydrogen peroxide and nitric oxide: key regulators of the Legume-Rhizobium and mycorrhizal symbioses. Antioxid Redox Signal 18:2202–2219. Scholar
  45. 45.
    Hichri I, Boscari A, Castella C, Rovere M, Puppo A, Brouquisse R (2015) Nitric oxide: a multifaceted regulator of the nitrogen-fixing symbiosis. J Exp Bot 66:2877–2887. Scholar
  46. 46.
    Damiani I, Pauly N, Puppo A, Brouquisse R, Boscari A (2016) Reactive oxygen species and nitric oxide control early steps of the Legume – Rhizobium symbiotic interaction. Front Plant Sci 7:1–8. Scholar
  47. 47.
    Montiel J, Arthikala MK, Cardenas L, Quinto C (2016) Legume NADPH oxidases have crucial roles at different stages of nodulation. Int J Mol Sci 17:1–12. Scholar
  48. 48.
    Stambulska UY, Bayliak MM, Lushchak VI (2018) Chromium (VI) toxicity in legume plants: modulation effects of rhizobial symbiosis. Biomed Res Int 2018:8031213. Scholar
  49. 49.
    Zahran HH (1999) Rhizobium -legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Johnston AW, Yeoman KH, Wexler M (2001) Metals and the rhizobial-legume symbiosis – uptake, utilization and signalling. Adv Microb Physiol 45:113–156PubMedCrossRefGoogle Scholar
  51. 51.
    Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Loza-Tavera H, Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347. Scholar
  52. 52.
    Broos K, Mertens J, Smolders E (2005) Toxicity of heavy metals in soil assessed with various soil microbial and plant growth assays: a comparative study. Environ Toxicol Chem 24:634–640PubMedCrossRefGoogle Scholar
  53. 53.
    Arora NK, Khare E, Singh S, Maheshwari DK (2010) Effect of Al and heavy metals on enzymes of nitrogen metabolism of fast and slow growing rhizobia under explanta conditions. World J Microbiol Biotechnol 26:811–816CrossRefGoogle Scholar
  54. 54.
    Ahmad E, Oves M (2012) Heavy metal toxicity to symbiotic nitrogen-fixing microorganism and host legumes. In: Zaidi A, Wani PA, Khan NS (eds) Toxicity of heavy metals to Legumes and bioremediation. Springer, Wien, pp 29–44. Scholar
  55. 55.
    DalCorso G (2012) Heavy metal toxicity in plants. In: Furini A (ed) Plants and heavy metals. Springer, Netherlands, Dordrecht, pp 1–25Google Scholar
  56. 56.
    Sangwan P, Kumar V, Joshi UN (2014) Effect of Chromium(VI) toxicity on enzymes of nitrogen metabolism in clusterbean (Cyamopsis tetragonoloba L.). Enzyme Res 2014:1–9. Scholar
  57. 57.
    Chaudhary P, Dudeja SS, Kapoor KK (2004) Effectivity of host- Rhizobium leguminosarum symbiosis in soils receiving sewage water containing heavy metals. Microbiol Res 159:121–127. Scholar
  58. 58.
    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 66:1670–1676. Scholar
  59. 59.
    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 22:12479–12489. Scholar
  60. 60.
    Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ – Sci 26:1–20. Scholar
  61. 61.
    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 16:179–202. Scholar
  62. 62.
    Gomez-Sagasti MT, Marino D (2015) PGPRs and nitrogen-fixing legumes: a perfect team for efficient Cd phytoremediation? Front Plant Sci 6:1–9. Scholar
  63. 63.
    Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546. Scholar
  64. 64.
    Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol Lett 285:1–9. Scholar
  65. 65.
    Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144. Scholar
  66. 66.
    Gresshoff PM, Lohar D, Chan PK, Biswas B, Jiang Q, Reid D, Ferguson B, Stacey G (2009) Genetic analysis of ethylene regulation of legume nodulation. Plant Signal Behav 4:818–823PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Bonaldi K, Gourion B, Fardoux J, Hannibal L, Cartieaux F, Boursot M, Vallenet D, Chaintreuil C, Prin Y, Nouwen N, Giraud E (2010) Large-scale transposon mutagenesis of photosynthetic Bradyrhizobium sp. strain ORS278 reveals new genetic loci putatively important for nod-independent symbiosis with Aeschynomene indica. Mol Plant-Microbe Interact 23:760–770. Scholar
  68. 68.
    Tominaga A, Nagata M, Futsuki K, Abe H, Uchiumi T, Abe M, Kucho K, Hashiguchi M, Akashi R, Hirsch AM, Arima S, Suzuki A (2009) Enhanced nodulation and nitrogen fixation in the abscisic acid low-sensitive mutant enhanced nitrogen fixation of Lotus japonicas. Plant Physiol 151:1965–1976. Scholar
  69. 69.
    Wang D, Yang S, Tang F, Zhu H (2012) Symbiosis specificity in the legume – rhizobial mutualism. Cell Microbiol 14:334–342. Scholar
  70. 70.
    Karunakaran R, Ramachandran VK, Seaman JC, East AK, Mouhsine B, Mauchline TH, Prell J, Skeffington A, Poole PS (2009) Transcriptomic analysis of Rhizobium leguminosarum biovar viciae in symbiosis with host plants Pisum sativum and Vicia cracca. J Bacteriol 191:4002–4014. Scholar
  71. 71.
    Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59. Scholar
  72. 72.
    Giles ED, Oldroyd GE, Harrison MJ, Udvardi M (2005) Peace talks and trade deals. Keys to long-term harmony in legume-microbe symbioses. Plant Physiol 137:1205–1220. Scholar
  73. 73.
    Kiss E, Oláh B, Kaló P, Morales M, Heckmann AB, Borbola A, Lózsa A, Kontár K, Middleton P, Downie JA, Oldroyd GE, Endre G (2009) LIN, a novel type of U-box/WD40 protein, controls early infection by rhizobia in legumes. Plant Physiol 151:1239–1249. Scholar
  74. 74.
    Poole P, Ramachandran V, Terpolilli J (2018) Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol 16:291–303. Scholar
  75. 75.
    Reddy P, Rendón-Anaya M, Soto del Río M, Khandual S (2007) Flavonoids as signaling molecules and regulators of root nodule development. Dyn Soil Dyn Plant 1:83–94Google Scholar
  76. 76.
    Wheatley RM, Poole PS (2018) Mechanisms of bacterial attachment to roots. FEMS Microbiol Rev 42:448–461. Scholar
  77. 77.
    Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, Osbourn A, Grant A, Poole PS (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J7:2248–2258. Scholar
  78. 78.
    Van Egeraat AWSM (1975) The possible role of homoserine in the development of Rhizobium leguminosarumin the rhizosphere of pea seedlings. Plant Soil 42:381–386. Scholar
  79. 79.
    Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273. Scholar
  80. 80.
    Zhang J, Subramanian S, Stacey G, Yu O (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant J 57:171–183. Scholar
  81. 81.
    Lee S, Seo D-H, Park H-L, Choi Y, Jung S (2003) Solubility enhancement of a hydrophobic flavonoid, luteolin by the complexation with cyclosophoraoses isolated from Rhizobium meliloti. Antonie Van Leeuwenhoek 84:201–207PubMedCrossRefGoogle Scholar
  82. 82.
    Lawson CGR, Rolfe BG, Djordjevic MA (1996) Rhizobium inoculation induces condition-dependent changes in the flavonoid composition of root exudates from Trifolium subterraneum. Funct Plant Biol 23:93–101CrossRefGoogle Scholar
  83. 83.
    Dakora FD, Joseph CM, Phillips DA (1993) Common bean root exudates contain elevated levels of daidzein and coumestrol in response to Rhizobium inoculation. Mol Plant-Microbe Interact 6:665–668CrossRefGoogle Scholar
  84. 84.
    Bolanos-Vasquez MC, Werner D (1997) Effects of Rhizobium tropici, R. etli, and R. leguminosarum bv. phaseoli on nod gene-inducing flavonoids in root exudates of Phaseolus vulgaris. Mol Plant-Microbe Interact 10:339–346CrossRefGoogle Scholar
  85. 85.
    Estabrook EM, Sengupta-Gopalan C (1991) Differential expression of phenylalanine ammonia-lyase and chalcone synthase during soybean nodule development. Plant Cell 3:299–308. Scholar
  86. 86.
    Begum AA, Leibovitch S, Migner P, Zhang F (2001) Specific flavonoids induced nod gene expression and pre-activated nod genes of Rhizobium leguminosarum increased pea (Pisum sativum L.) and lentil (Lens culinaris L.) nodulation in controlled growth chamber environments. J Exp Bot 52:1537–1543PubMedCrossRefGoogle Scholar
  87. 87.
    Novak K, Chovanec P, Skrdleta V, Kropacova M, Lisa L, Nemcova M (2002) Effect of exogenous flavonoids on nodulation of pea (Pisum sativum L.). J Exp Bot 53:1735–1174PubMedCrossRefGoogle Scholar
  88. 88.
    Kelly S, Sullivan JT, Kawaharada Y, Radutoiu S, Ronson CW, Stougaard J (2018) Regulation of Nod factor biosynthesis by alternative NodD proteins at distinct stages of symbiosis provides additional compatibility scrutiny. Environ Microbiol 20:97–110. Scholar
  89. 89.
    Fisher RF, Long SR (1993) Interactions of NodD at the nod Box: NodD binds to two distinct sites on the same face of the helix and induces a bend in the DNA. J Mol Biol 233:336–348PubMedCrossRefGoogle Scholar
  90. 90.
    Peck MC, Fisher RF, Long SR (2006) Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J Bacteriol 188:5417–5427. Scholar
  91. 91.
    Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170. Scholar
  92. 92.
    Phillips DA, Joseph CM, Maxwell CA (1992) Trigonelline and Stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol 99:1526–1533PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Ribeiro CW, Alloing G, Mandon K, Frendo P (2015) Redox regulation of differentiation in symbiotic nitrogen fixation. Biochim Biophys Acta, Gen Subj 1850:1469–1478. Scholar
  94. 94.
    Gourion B, Berrabah F, Ratet P, Stacey G (2015) Rhizobium-legume symbioses: the crucial role of plant immunity. Trends Plant Sci 20:186–194. Scholar
  95. 95.
    Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630–633. Scholar
  96. 96.
    Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, Maolanon N, Vinther M, Lorentzen A, Madsen EB, Jensen KJ, Roepstorff P, Thirup S, Ronson CW, Thygesen MB, Stougaard J (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci U S A 109:13859–13864. Scholar
  97. 97.
    Vedam V, Haynes JG, Kannenberg EL, Carlson RW, Sherrier DJ (2004) A Rhizobium leguminosarum lipopolysaccharide lipid-A mutant induces nitrogen-fixing nodules with delayed and defective bacteroid formation. Mol Plant-Microbe Interact 17:283–291PubMedCrossRefGoogle Scholar
  98. 98.
    Jones KM, Sharopova N, Lohar DP, Zhang JQ, VandenBosch KA, Walker GC (2008) Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc Natl Acad Sci U S A 105:704–709. Scholar
  99. 99.
    Jones KM (2012) Increased production of the exopolysaccharide succinoglycan enhances Sinorhizobium meliloti 1021 symbiosis with the host plant Medicago truncatula. J Bacteriol 194:4322–4331. Scholar
  100. 100.
    D’Haeze W, Holsters M (2004) Surface polysaccharides enable bacteria to evade plant immunity. Trends Microbiol 12:555–561PubMedCrossRefGoogle Scholar
  101. 101.
    de Vasconcelos MA, Cunha CO, Arruda FVS, Carneiro VA, Bastos RM, Mercante FM, do Nascimento KS, Cavada BS, dos Santos RP, Teixeira EH (2013) Effect of leguminous lectins on the growth of Rhizobium tropici CIAT899. Molecules 18:5792–5803. Scholar
  102. 102.
    Wang LX, Wang Y, Pellock B, Walker GC (1999) Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J Bacteriol 181:6788–6796PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Kelly SJ, Muszynski A, Kawaharada Y, Hubber AM, Sullivan JT, Sandal N, Carlson RW, Stougaard J, Ronson CW (2013) Conditional requirement for exopolysaccharide in the Mesorhizobium-Lotus symbiosis. Mol Plant-Microbe Interact 26:319–329. Scholar
  104. 104.
    Reuhs BL, Geller DP, Kim JS, Fox JE, Kolli VS, Pueppke SG (1998) Sinorhizobium fredii and Sinorhizobium meliloti produce structurally conserved lipopolysaccharides and strain-specific K antigens. Appl Environ Microbiol 64:4930–4938PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Raetz CRH, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76:295–329. Scholar
  106. 106.
    Gore RS, Miller KJ (1993) Cyclic [beta]-1,6 -1,3 Glucans are synthesized by Bradyrhizobium japonicum bacteroids within soybean (Glycine max) root nodules. Plant Physiol 102:191–194PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Koronakis V, Eswaran J, Hughes C (2004) Structure and function of TolC: the bacterial exit duct for proteins and drugs. Annu Rev Biochem 73:467–489PubMedCrossRefGoogle Scholar
  108. 108.
    Mongiardini EJ, Ausmees N, Pérez-Giménez J, Julia Althabegoiti M, Ignacio Quelas J, López-García SL, Lodeiro AR (2008) The rhizobial adhesion protein RapA1 is involved in adsorption of rhizobia to plant roots but not in nodulation. FEMS Microbiol Ecol 65:279–288. Scholar
  109. 109.
    Krishnan HB, Lorio J, Kim WS, Jiang G, Kim KY, DeBoer M, Pueppke SG (2003) Extracellular proteins involved in soybean cultivar-specific nodulation are associated with pilus-like surface appendages and exported by a type III protein secretion system in Sinorhizobium fredii USDA257. Mol Plant-Microbe Interact 16:617–625PubMedCrossRefGoogle Scholar
  110. 110.
    Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat Rev Microbiol 7:312–320. Scholar
  111. 111.
    Liu H, Zhang C, Yang J, Yu N, Wang E (2018) Hormone modulation of legume-rhizobial symbiosis. J Integr Plant Biol 60:632–648. Scholar
  112. 112.
    Maheshwari DK (2012) Bacteria in agrobiology: plant probiotics. Springer Science & Business Media, pp 201–211. Scholar
  113. 113.
    Imada EL, Rolla Dos Santos AADP, de Oliveira ALM, Hungria M, Rodrigues EP (2017) Indole-3-acetic acid production via the indole-3-pyruvate pathway by plant growth promoter Rhizobium tropici CIAT 899 is strongly inhibited by ammonium. Res Microbiol 168:283–292. Scholar
  114. 114.
    Timmers AC, Soupene E, Auriac MC, de Billy F, Vasse J, Boistard P, Truchet G (2000) Saprophytic intracellular rhizobia in alfalfa nodules. Mol Plant-Microbe Interact 13:1204–1213. Scholar
  115. 115.
    White JP, Prell J, Ramachandran VK, Poole PS (2009) Characterization of a {gamma}-aminobutyric acid transport system of Rhizobium leguminosarum bv. viciae 3841. J Bacteriol 191:1547–5155. Scholar
  116. 116.
    Blokhina O, Fagerstedt KV (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol Plant 138:447–462. Scholar
  117. 117.
    Lushchak VI (2011) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Physiol Part C Toxicol Pharmacol 153:175–190. Scholar
  118. 118.
    Lushchak VI (2014) Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact 224:164–175. Scholar
  119. 119.
    Lushchak VI (2016) Contaminant-induced oxidative stress in fish: a mechanistic approach. Fish Physiol Biochem 42:711–747. Scholar
  120. 120.
    Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364CrossRefGoogle Scholar
  121. 121.
    Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15. Scholar
  122. 122.
    Besson-Bard A, Courtois C, Gauthier A, Dahan J, Dobrowolska G, Jeandroz S, Pugin A, Wendehenne D (2008) Nitric oxide in plants: production and cross-talk with Ca2+ signaling. Mol Plant 1:218–228. Scholar
  123. 123.
    Becana M, Matamoros A, Udvardi M, Dalton DA (2010) Recent insights into antioxidant defenses of legume root nodules. New Phytol 188:960–976. Scholar
  124. 124.
    Kolupaev YE, Karpets YV, Musatenko LI (2007) Participation of active forms of oxygen in induction of salt tolerance of seedlings of wheat with salicylic acid. Rep Natl Acad Sci Ukraine 6:154–158Google Scholar
  125. 125.
    Shaw SL, Long SR (2003) Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiol 132:2196–2204PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Peleg-Grossman S, Volpin H, Levine A (2007) Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. J Exp Bot 58:1637–1649. Scholar
  127. 127.
    Wisniewski JP, Rathbun EA, Knox JP, Brewin NJ (2000) Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum. Mol Plant-Microbe Interact 13:413–420. Scholar
  128. 128.
    Davies MJ, Puppo A (1992) Direct detection of a globin-derived radical in leghaemoglobin treated with peroxides. Biochem J 281:197–201PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Ferrarini A, De Stefano M, Baudouin E, Pucciariello C, Polverari A, Puppo A, Delledonne M (2008) Expression of Medicago truncatula genes responsive to nitric oxide in pathogenic and symbiotic conditions. Mol Plant-Microbe Interact 21:781–790. Scholar
  130. 130.
    Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, de Felipe MR, Harrison J, Vanacker H, Foyer CH (2005) Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 165:683–701. Scholar
  131. 131.
    Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M (1999) Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol 121:879–888PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Cam Y, Pierre O, Boncompagni E, Hérouart D, Meilhoc E, Bruand C (2012) Nitric oxide (NO): a key player in the senescence of Medicago truncatula root nodules. New Phytol 196:548–560. Scholar
  133. 133.
    Alesandrini F, Mathis R, Van de Sype G, Herouart D, Puppo A (2003) Possible roles for a cysteine protease and hydrogen peroxide in soybean nodule development and senescence. New Phytol 158:131–138.–8137.2003.00720.xCrossRefGoogle Scholar
  134. 134.
    Marwa EM, Meharg AA, Rice CM (2012) Risk assessment of potentially toxic elements in agricultural soils and maize tissues from selected districts in Tanzania. Sci Total Environ 416:180–186. Scholar
  135. 135.
    Uddin MK (2017) A review on the adsorption of heavy metals by clay minerals, with special focus on the past decade. Chem Eng J 308:438–462. Scholar
  136. 136.
    Lu K, Yang X, Gielen G, Bolan N, Ok YS, Niazi NK, Xu S, Yuan G, Chen X, Zhang X, Liu D, Song Z, Liu X, Wang H (2017) Effect of bamboo and rice straw biochars on the mobility and redistribution of heavy metals (Cd, Cu, Pb and Zn) in contaminated soil. J Environ Manag 186:285–292. Scholar
  137. 137.
    Maheswari M, Yadav SK, Shanker AK, Kumar MA, Venkateswarlu B (2012) Overview of plant stresses: mechanisms, adaptations and research pursuit. In: Venkateswarlu B, Shanker AK, Shanker C, Maheswari M (eds) Crop stress and its management: perspectives and strategies. Springer, DordrechtGoogle Scholar
  138. 138.
    Khan A, Khan S, Khan MA, Qamar Z, Waqas M (2015) The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: a: review. Environ Sci Pollut Res Int 22:13772–13799. Scholar
  139. 139.
    Ahmed W, Ahmad M, Rauf A, Shah F, Khan S, Kamal S, Shah S, Khan A (2015) Evaluations of some trace metal levels from the leaves of Salix nigra in Hayatabad industrial estate Peshawar, Khyber Pakhtunkhwa Pakistan. Amer J Biomed Life Sci 3:21–24. Scholar
  140. 140.
    Bibi M, Hussain M (2005) Effect of copper and lead on photosynthesis and plant pigments in black gram Vigna mungo (L.) Hepper. Bull Environ Contam Toxicol 74:1126–1133PubMedCrossRefGoogle Scholar
  141. 141.
    Ma J, Lv C, Xu M, Chen G, Lv C, Gao Z (2016) Photosynthesis performance, antioxidant enzymes and ultrastructural analyses of rice seedlings under chromium stress. Environ Sci Pollut Res Int 23:1768–1778. Scholar
  142. 142.
    Xue Z, Gao H, Zhao S (2014) Effects of cadmium on the photosynthetic activity in mature and young leaves of soybean plants. Environ Sci Pollut Res Int 21:4656–4664. Scholar
  143. 143.
    Maiti S, Ghosh N, Mandal C, Das K, Dey N, Adak MK (2012) Responses of the maize plant to chromium stress with reference to antioxidation activity. Braz J Plant Physiol 24:203–212. Scholar
  144. 144.
    Rai V, Vajpayee P, Singh SN, Mehrotra S (2004) Effect of chromium accumulation on photosynthetic pigments, oxidative stress defense system, nitrate reduction, proline level and eugenol content of Ocimum tenuiflorum L. Plant Sci 167:1159–1169. Scholar
  145. 145.
    Dixit V, Pandey V, Shyam R (2002) Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L. cv. Azad) root mitochondria. Plant Cell Environ 25:687–693. Scholar
  146. 146.
    Panda SK, Choudhury S (2005) Chromium stress in plants. Braz J Plant Physiol 17:95–102CrossRefGoogle Scholar
  147. 147.
    Zou J, Yu K, Zhang Z, Jiang W, Liu D (2009) Antioxidant response system and chlorophyll fluorescence in chromium (VI)-treated Zea mays L. seedlings. Acta Biol Cracov Ser Bot 51:23–33Google Scholar
  148. 148.
    Barton LL, Johnson GV, O'Nan AG, Wagener BM (2000) Inhibition of ferric chelate reductase in alfalfa roots by cobalt, nickel, chromium, and copper. J Plant Nutr 23:1833–1845. Scholar
  149. 149.
    Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254. Scholar
  150. 150.
    Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179. Scholar
  151. 151.
    Kubrak OI, Husak VV, Rovenko BM, Poigner H, Kriews M, Abele D, Lushchak VI (2013) Antioxidant system efficiently protects goldfish gills from Ni2+-induced oxidative stress. Chemosphere 90:971–976. Scholar
  152. 152.
    Lushchak OV, Kubrak OI, Torous IM, Nazarchuk TY, Storey KB, Lushchak VI (2009) Trivalent chromium induces oxidative stress in goldfish brain. Chemosphere 75:56–62. Scholar
  153. 153.
    Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30. Scholar
  154. 154.
    Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208PubMedCrossRefGoogle Scholar
  155. 155.
    Semchuk NM, Lushchak OV, Falk J, Krupinska K, Lushchak VI (2009) Inactivation of genes, encoding tocopherol biosynthetic pathway enzymes, results in oxidative stress in outdoor grown Arabidopsis thaliana. Plant Physiol Biochem 47:384–390. Scholar
  156. 156.
    Khan MS, Zaidi A, Wani PA, Oves M (2009a) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19CrossRefGoogle Scholar
  157. 157.
    Rother JA, Millbank JW, Thornton I (1983) Nitrogen fixation by white clover (Trifolium repens) in grasslands on soils contaminated with cadmium, lead and zinc. J Soil Sci 34:127–136CrossRefGoogle Scholar
  158. 158.
    Khan M, Scullion J (2002) Effects of metal (Cd, Cu, Ni, Pb or Zn) enrichment of sewage-sludge on soil microorganisms and their activities. Appl Soil Ecol 20:145–155. Scholar
  159. 159.
    Shi W, Bischoff M, Turco R, Konopka A (2002) Long-term effects of chromium and lead upon the activity of soil microbial communities. Appl Soil Ecol 21:169–177CrossRefGoogle Scholar
  160. 160.
    Lakzian A, Murphy P, Turner A, Beynon JL, Giller KE (2002) Rhizobium leguminosarum bv. viciae populations in soils with increasing heavy metal contamination: abundance, plasmid profiles, diversity and metal tolerance. Soil Biol Biochem 34:519–529. Scholar
  161. 161.
    Bianucci E, Fabra A, Castro S (2011) Cadmium accumulation and tolerance in Bradyrhizobium spp. (Peanut Microsymbionts). Curr Microbiol 62:96–100. Scholar
  162. 162.
    Hirsch PR, Jones MJ, McGrath SP, Giller KE (1993) Heavy metals from past applications of sewage sludge decrease the genetic diversity of Rhizobium leguminosarum biovar trifolii populations. Soil Biol Biochem 25:1485–1490CrossRefGoogle Scholar
  163. 163.
    Khan MS, Zaidi A, Oves M, Wani PA (2008) Heavy metal toxicity to legumes. In: Samuel EB, William CW (eds) Heavy metal pollution. Nova Science Publishers, HauppaugeGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Biochemistry and BiotechnologyVasyl Stefanyk Precarpathian National UniversityIvano-FrankivskUkraine

Personalised recommendations