, Volume 77, Issue 3, pp 191–205 | Cite as

Opportunities for improved legume inoculants: enhanced stress tolerance of rhizobia and benefits to agroecosystems

  • Mary Atieno
  • Didier LesueurEmail author


Environmental stress conditions influence the growth and survival of rhizobia by affecting the signalling and infection process, nodule development and function. Stress factors such as osmotic stress, extremes of temperature and pH and accumulation of heavy metals result in reduced nodulation, leading to low levels of nitrogen fixation and crop yield. Some species of rhizobia are known to be tolerant to biotic and abiotic stresses and utilization of these stress-tolerant rhizobia strains as inoculants, can greatly improve biological nitrogen fixation. This review highlights the main environmental stresses known to cause cause rhizobial cell damage and death, including temperature, desiccation, drought, salinity, pH and heavy metal stresses. An understanding of the key physiological and molecular factors of how these stress responses affect the survival of rhizobia is crucial in the development of strains with high potential in symbiotic nitrogen fixation. Key responses range from expression of stress-linked genes and proteins which aid in cell repair and protection, accumulation of compatible solutes such as sugars and polymers, carbon enrichment in drought stress, to extrusion of heavy metals. Biological nitrogen fixation can be improved by the selection of nitrogen-fixing endosymbionts that are well-adapted and tolerant to a broad range of environmental stresses is important in alleviating the effects of adverse conditions, potentially increasing the chances of success of legume inoculation with rhizobia thus improving the contribution of atmospheric nitrogen fixation in agroecosystems.


Rhizobia Environmental stress Legumes adaptation Stress tolerance 



Authors wish to thank Dr. Lambert Brau for editing this manuscript and for his useful comments to improve its content.


  1. Abd-Alla M, Vuong T, Harper J (1998) Genotypic differences in dinitrogen fixation response to NaCl stress in intact and grafted soybean. Crop Sci 38:72–77CrossRefGoogle Scholar
  2. Acebrón S, Martín I, del Castillo U, Moro F, Muga A (2009) DnaK-mediated association of ClpB to protein aggregates. A bichaperone network at the aggregate surface. FEBS Lett 583:2991–2996CrossRefPubMedGoogle Scholar
  3. Alexandre A, Oliveira S (2011) Most heat-tolerant rhizobia show high induction of major chaperone genes upon stress. FEMS Microbiol Ecol 75:28–36CrossRefPubMedGoogle Scholar
  4. Alexandre A, Laranjo M, Oliveira S (2013) Global transcriptional response to heat shock of the legume symbiont Mesorhizobium loti MAFF303099 comprises extensive gene downregulation. DNA Res 21:195–206CrossRefPubMedPubMedCentralGoogle Scholar
  5. Alloing G, Travers I, Sagot B, Le Rudulier D, Dupont L (2006) Proline betaine uptake in Sinorhizobium meliloti: characterization of Prb, an Opp-like ABC transporter regulated by both proline betaine and salinity stress. J Bacteriol 188:6308–6317CrossRefPubMedPubMedCentralGoogle Scholar
  6. Alves BJR, Boddey RM, Urquiaga S (2003) The success of BNF in soybean in Brazil. Plant Soil 252:1–9. CrossRefGoogle Scholar
  7. Anyango B, Wilson KJ, Beynon JL, Giller KE (1995) Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. Appl Environ Microbiol 61:4016–4021PubMedPubMedCentralGoogle Scholar
  8. Arora N, Khare E, Singh S, Maheshwari D (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
  9. Atieno M, Herrmann L, Okalebo R, Lesueur D (2012) Efficiency of different formulations of Bradyrhizobium japonicum and effect of co-inoculation of Bacillus subtilis with two different strains of Bradyrhizobium japonicum. World J Microbiol Biotechnol 28:2541–2550CrossRefPubMedGoogle Scholar
  10. Atieno M, Wilson N, Casteriano A, Crossett B, Lesueur D, Deaker R (2018) Aqueous peat extract exposes rhizobia to sub-lethal stress which may prime cells for improved desiccation tolerance. Appl Microbiol Biotechnol 102:7521–7539CrossRefPubMedGoogle Scholar
  11. Bååth E, Díaz-Raviña M, Frostegård Å, Campbell CD (1998) Effect of metal-rich sludge amendments on the soil microbial community. Appl Microbiol Biotechnol 64:238–245Google Scholar
  12. Baldani JI, Weaver R, Hynes M, Eardly B (1992) Utilization of carbon substrates, electrophoretic enzyme patterns, and symbiotic performance of plasmid-cured clover rhizobia. Appl Environ Microbiol 58:2308–2314PubMedPubMedCentralGoogle Scholar
  13. Barra L, Pica N, Gouffi K, Walker GC, Blanco C, Trautwetter A (2003) Glucose 6-phosphate dehydrogenase is required for sucrose and trehalose to be efficient osmoprotectants in Sinorhizobium meliloti. FEMS Microbiol Lett 229:183–188CrossRefPubMedGoogle Scholar
  14. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. CRC Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  15. Bashan Y, de-Bashan LE, Prabhu S, Hernandez J-P (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33CrossRefGoogle Scholar
  16. Beltra R, Del Solar G, Sanchez-Serrano J, Alonso E (1988) Mutants of Rhizobium phaseoli HM Mel− obtained by means of elevated temperatures. Zentralbl Mikrobiol 143:529–532CrossRefGoogle Scholar
  17. Biter AB, Lee S, Sung N, Tsai FT (2012) Structural basis for intersubunit signaling in a protein disaggregating machine. Proc Natl Acad Sci U S A 109:12515–12520CrossRefPubMedPubMedCentralGoogle Scholar
  18. Bontemps C et al (2010) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19:44–52CrossRefPubMedGoogle Scholar
  19. Boscari A, Van de Sype G, Le Rudulier D, Mandon K (2006) Overexpression of BetS, a Sinorhizobium meliloti high-affinity betaine transporter, in bacteroids from Medicago sativa nodules sustains nitrogen fixation during early salt stress adaptation. Mol Plant-Microbe Interact 19:896–903CrossRefPubMedGoogle Scholar
  20. Botsford JL, Lewis TA (1990) Osmoregulation in Rhizobium meliloti: production of glutamic acid in response to osmotic stress. Appl Environ Microbiol 56:488–494PubMedPubMedCentralGoogle Scholar
  21. Brígido C, Robledo M, Menéndez E, Mateos PF, Oliveira S (2012) A ClpB chaperone knockout mutant of Mesorhizobium ciceri shows a delay in the root nodulation of chickpea plants. Mol Plant-Microbe Interact 25:1594–1604CrossRefPubMedGoogle Scholar
  22. Bryant G, Koster KL, Wolfe J (2001) Membrane behaviour in seeds and other systems at low water content: the various effects of solutes. Seed Sci Res 11:17–25CrossRefGoogle Scholar
  23. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220CrossRefPubMedGoogle Scholar
  24. Bushby H, Marshall K (1977) Some factors affecting the survival of root-nodule bacteria on desiccation. Soil Biol Biochem 9:143–147CrossRefGoogle Scholar
  25. Carrasco JA et al (2005) Isolation and characterisation of symbiotically effective Rhizobium resistant to arsenic and heavy metals after the toxic spill at the Aznalcollar pyrite mine. Soil Biol Biochem 37:1131–1140CrossRefGoogle Scholar
  26. Casteriano A (2013) Physiological mechanisms of desiccation tolerance in rhizobia. University of SydneyGoogle Scholar
  27. Casteriano A, Wilkes MA, Deaker R (2013) Physiological changes in rhizobia after growth in peat extract may be related to improved desiccation tolerance. Appl Environ Microbiol 79:3998–4007CrossRefPubMedPubMedCentralGoogle Scholar
  28. Catroux G, Hartmann A, Revellin C (2001) Trends in rhizobial inoculant production and use. Plant Soil 230:21–30CrossRefGoogle Scholar
  29. Charlson DV, Bhatnagar S, King CA, Ray JD, Sneller CH, Carter TE, Purcell LC (2009) Polygenic inheritance of canopy wilting in soybean [Glycine max (L.) Merr.]. Theor Appl Genet 119:587–594CrossRefPubMedGoogle Scholar
  30. Chaudri AM, Allain CM, Barbosa-Jefferson VL, Nicholson FA, Chambers BJ, McGrath SP (2000) A study of the impacts of Zn and Cu on two rhizobial species in soils of a long-term field experiment. Plant Soil 221:167–179CrossRefGoogle Scholar
  31. Chen L, Figueredo A, Villani H, Michajluk J, Hungria M (2002a) Diversity and symbiotic effectiveness of rhizobia isolated from field-grown soybean nodules in Paraguay. Biol Fertil Soils 35:448–457CrossRefGoogle Scholar
  32. Chen R, Bhagwat AA, Yaklich R, Keister DL (2002b) Characterization of ndvD, the third gene involved in the synthesis of cyclic β-(1 3),(1 6)-d-glucans in Bradyrhizobium japonicum. Can J Microbiol 48:1008–1016CrossRefPubMedGoogle Scholar
  33. Cheung K, Gu J-D (2007) Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior Biodegrad 59:8–15CrossRefGoogle Scholar
  34. Chien C-T, Maundu J, Cavaness J, Dandurand L-M, Orser CS (1992) Characterization of salt-tolerant and salt-sensitive mutants of Rhizobium leguminosarum biovar viciae strain C1204b. FEMS Microbiol Lett 90:135–140CrossRefGoogle Scholar
  35. Cloutier J, Prévost D, Nadeau P, Antoun H (1992) Heat and cold shock protein synthesis in arctic and temperate strains of rhizobia. Appl Environ Microbiol 58:2846–2853PubMedPubMedCentralGoogle Scholar
  36. Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678CrossRefGoogle Scholar
  37. Crockford AJ, Behncke C, Williams HD (1996) The adaptation of Rhizobium leguminosarum bv. phaseoli to oxidative stress and its overlap with other environmental stress responses. Microbiology 142:331–336CrossRefGoogle Scholar
  38. Crowe JH, Crowe LM, Oliver AE, Tsvetkova N, Wolkers W, Tablin F (2001) The trehalose myth revisited: introduction to a symposium on stabilization of cells in the dry state. Cryobiol 43:89–105CrossRefGoogle Scholar
  39. Cytryn EJ et al (2007) Transcriptional and physiological responses of Bradyrhizobium japonicum to desiccation-induced stress. J Bacteriol 189:6751–6762CrossRefPubMedPubMedCentralGoogle Scholar
  40. da Costa MS, Santos H, Galinski EA (1998) An overview of the role and diversity of compatible solutes in Bacteria and archaea. In: Antranikian G (ed) Biotechnology of extremophiles. Springer Berlin Heidelberg, Berlin, pp 117–153CrossRefGoogle Scholar
  41. da Silva Batista JS, Hungria M (2012) Proteomics reveals differential expression of proteins related to a variety of metabolic pathways by genistein-induced Bradyrhizobium japonicum strains. J Proteome 75:1211–1219CrossRefGoogle Scholar
  42. Das H, Mitra AK, Sengupta P, Hossain A, Islam F, Rabbani G (2004) Arsenic concentrations in rice, vegetables, and fish in Bangladesh: a preliminary study. Environ Int 30:383–387CrossRefPubMedGoogle Scholar
  43. da-Silva JR, Alexandre A, Brígido C, Oliveira S (2017) Can stress response genes be used to improve the symbiotic performance of rhizobia? AIMS Microbiol 3:365–382CrossRefGoogle Scholar
  44. de Castro PR, dos Reis Junior FB, Zilli JE, Fischer D, Hofmann A, James EK, Simon MF (2018) Soil characteristics determine the rhizobia in association with different species of Mimosa in Central Brazil. Plant Soil 423:411–428CrossRefGoogle Scholar
  45. de Lucena DK, Pühler A, Weidner S (2010) The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti. BMC Microbiol 10:265. CrossRefPubMedPubMedCentralGoogle Scholar
  46. De Meyer SE et al (2016) Symbiotic Burkholderia species show diverse arrangements of nif/fix and nod genes and lack typical high-affinity cytochrome cbb3 oxidase genes. Mol Plant-Microbe Interact 29:609–619CrossRefPubMedGoogle Scholar
  47. Deaker R, Roughley RJ, Kennedy IR (2004) Legume seed inoculation technology: a review. Soil Biol Biochem 36:1275–1288CrossRefGoogle Scholar
  48. Deaker R, Hartley E, Gemell G (2012) Conditions affecting shelf-life of inoculated legume seed. Agric J 2:38–51Google Scholar
  49. Deepika KV, Raghuram M, Kariali E, Bramhachari PV (2016) Biological responses of symbiotic Rhizobium radiobacter strain VBCK1062 to the arsenic contaminated rhizosphere soils of mung bean. Ecotoxicol Environ Saf 134(Part 1):1–10CrossRefGoogle Scholar
  50. Defez R, Esposito R, Angelini C, Bianco C (2016) Overproduction of indole-3-acetic acid in free-living rhizobia induces transcriptional changes resembling those occurring in nodule bacteroids. Mol Plant-Microbe Interact 29:484–495CrossRefPubMedGoogle Scholar
  51. Delmotte N et al (2010) An integrated proteomics and transcriptomics reference data set provides new insights into the Bradyrhizobium japonicum bacteroid metabolism in soybean root nodules. Proteomics 10:1391–1400CrossRefPubMedGoogle Scholar
  52. Donati AJ, Jeon J-M, Sangurdekar D, So J-S, Chang W-S (2011) The genome-wide transcriptional and physiological responses of Bradyrhizobium japonicum to paraquat-mediated oxidative stress. Appl Environ Microbiol:AEM. 00047–00011Google Scholar
  53. dos Reis Jr FB et al (2010) Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 186:934–946CrossRefGoogle Scholar
  54. Drouin P, Prëvost D, Antoun H (2000) Physiological adaptation to low temperatures of strains of Rhizobium leguminosarum bv. viciae associated with Lathyrus spp. FEMS Microbiol Lett 32:111–120Google Scholar
  55. Duzan HM, Mabood F, Souleimanov A, Smith DL (2006) Nod Bj-V (C 18: 1, MeFuc) production by Bradyrhizobium japonicum (USDA110, 532C) at suboptimal growth temperatures. J Plant Physiol 163:107–111CrossRefPubMedGoogle Scholar
  56. Eaglesham A, Ayanaba A (1984) Tropical stress ecology of rhizobia, rootnodulation and legume fixation. Curr Dev Biol N Fix:1–35Google Scholar
  57. Encarnación S, Guzmán Y, Dunn MF, Hernández M, del Vargas M, Mora J (2003) Proteome analysis of aerobic and fermentative metabolism in Rhizobium etli CE3. Proteomics 3:1077–1085CrossRefPubMedGoogle Scholar
  58. Estrada-De Los Santos P, Rojas-Rojas FU, Tapia-García EY, Vásquez-Murrieta MS, Hirsch AM (2016) To split or not to split: an opinion on dividing the genus. Burkholderia Ann Microbiol 66:1303–1314CrossRefGoogle Scholar
  59. Fonseca MB et al (2012) Nodulation in Dimorphandra wilsonii Rizz.(Caesalpinioideae), a threatened species native to the Brazilian Cerrado. PLoS One 7:e49520CrossRefPubMedPubMedCentralGoogle Scholar
  60. Garau G, Yates RJ, Deiana P, Howieson JG (2009) Novel strains of nodulating Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soils. Soil Biol Biochem 41:125–134CrossRefGoogle Scholar
  61. Gehlot HS et al (2012) Nodulation of legumes from the Thar desert of India and molecular characterization of their rhizobia. Plant Soil 357:227–243CrossRefGoogle Scholar
  62. Gemell L, Hartley E, Herridge D (2005) Point-of-sale evaluation of preinoculated and custom-inoculated pasture legume seed. Anim Prod Sci 45:161–169CrossRefGoogle Scholar
  63. Gilbert KB, Vanderlinde EM, Yost CK (2007) Mutagenesis of the carboxy terminal protease CtpA decreases desiccation tolerance in Rhizobium leguminosarum. FEMS Microbiol Lett 272:65–74CrossRefPubMedGoogle Scholar
  64. 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
  65. González E, Gálvez L, Royuela M, Aparicio-Tejo P, Arrese-Igor C (2001) Insights into the regulation of nitrogen fixation in pea nodules: lessons from drought, abscisic acid and increased photoassimilate availability. Agron 21:607–613CrossRefGoogle Scholar
  66. Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities 3. Biotech 5:355–377Google Scholar
  67. Gouffi K, Pica N, Pichereau V, Blanco C (1999) Disaccharides as a new class of nonaccumulated osmoprotectants for Sinorhizobium meliloti. Appl Environ Microbiol 65:1491–1500PubMedPubMedCentralGoogle Scholar
  68. Graham PH (1992) Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soil conditions. Can J Microbiol 38:475–484CrossRefGoogle Scholar
  69. Graham PH et al (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Can J Microbiol 40:198–207CrossRefGoogle Scholar
  70. Guan D-w et al (2012) Analysis of two Bradyrhizobium japonicum strains with different symbiotic matching for nodulation by primary proteomic. J Integr Agric 11:1377–1383CrossRefGoogle Scholar
  71. Gutnick D, Bach H (2000) Engineering bacterial biopolymers for the biosorption of heavy metals; new products and novel formulations. Appl Microbiol Biotechnol 54:451–460CrossRefPubMedGoogle Scholar
  72. Gyaneshwar P et al (2011) Legume-Nodulating Betaproteobacteria: diversity, host range, and future prospects. Mol Plant-Microbe Interact 24:1276–1288. CrossRefPubMedGoogle Scholar
  73. Hartl FU, Hayer-Hartl M (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 16:574CrossRefPubMedGoogle Scholar
  74. Hartley EJ, Gemell LG, Deaker R (2012) Some factors that contribute to poor survival of rhizobia on preinoculated legume seed. Crop Pasture Sci 63:858–865CrossRefGoogle Scholar
  75. Hellweg C, Pühler A, Weidner S (2009) The time course of the transcriptomic response of Sinorhizobium meliloti 1021 following a shift to acidic pH. BMC Microbiol 9:37CrossRefPubMedPubMedCentralGoogle Scholar
  76. Herrmann L, Atieno M, Brau L, Lesueur D (2015) Microbial quality of commercial inoculants to increase BNF and nutrient use efficiency. In: Biological nitrogen fixation. John Wiley & Sons, Inc, pp 1031–1040Google Scholar
  77. Hoelzle I, Streeter JG (1990) Increased accumulation of trehalose in rhizobia cultured under 1% oxygen. Appl Environ Microbiol 56:3213–3215PubMedPubMedCentralGoogle Scholar
  78. Humann JL, Kahn ML (2015) Genes involved in desiccation resistance of rhizobia and other bacteria. In: Biological nitrogen fixation. John Wiley & Sons, Inc, pp 397–404Google Scholar
  79. Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L. Plant Soil 149:95–102CrossRefGoogle Scholar
  80. Hungria M, Vargas MA (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crop Res 65:151–164CrossRefGoogle Scholar
  81. Hussain MB, Zahir ZA, Asghar HN, Asgher M (2014) Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat? Int J Agric Biol 16:3–13Google Scholar
  82. James EK et al (1998) Photosynthetic oxygen evolution within Sesbania rostrata stem nodules. Plant J 13:29–38CrossRefGoogle Scholar
  83. Jensen JB, Peters NK, Bhuvaneswari T (2002) Redundancy in periplasmic binding protein-dependent transport systems for trehalose, sucrose, and maltose in Sinorhizobium meliloti. J Bacteriol 184:2978–2986CrossRefPubMedPubMedCentralGoogle Scholar
  84. Jeon J-M, Lee H-I, Donati AJ, So J-S, Emerich DW, Chang W-S (2011) Whole-genome expression profiling of Bradyrhizobium japonicum in response to hydrogen peroxide. Mol Plant-Microbe Interact 24:1472–1481CrossRefPubMedGoogle Scholar
  85. Jiang JQ, Wei W, Du BH, Li XH, Wang L, Yang SS (2004) Salt-tolerance genes involved in cation efflux and osmoregulation of Sinorhizobium fredii RT19 detected by isolation and characterization of Tn5 mutants. FEMS Microbiol Lett 239:139–146CrossRefPubMedGoogle Scholar
  86. Johansen C, Krishnamurthy L, Saxena N, Sethi S (1994) Genotypic variation in moisture response of chickpea grown under line-source sprinklers in a semi-arid tropical environment. Field Crop Res 37:103–112CrossRefGoogle Scholar
  87. Kala T, Christi R, Bai N (2011) Effect of Rhizobium inoculation on the growth and yield of horsegram (Dolichos biflorus Linn). Plant Arch 11:97–99Google Scholar
  88. Karanja NK, Wood M (1988) Selecting Rhizobium phaseoli strains for use with beans (Phaseolus vulgaris L.) in Kenya: tolerance of high temperature and antibiotic resistance. Plant Soil 112:15–22CrossRefGoogle Scholar
  89. Kaya MD, Okçu G, Atak M, Çıkılı Y, Kolsarıcı Ö (2006) Seed treatments to overcome salt and drought stress during germination in sunflower (Helianthus annuus L.). Eur J Agron 24:291–295CrossRefGoogle Scholar
  90. Kedzierska S, Matuszewska E (2001) The effect of co-overproduction of DnaK/DnaJ/GrpE and ClpB proteins on the removal of heat-aggregated proteins from Escherichia coli ΔclpB mutant cells–new insight into the role of Hsp70 in a functional cooperation with Hsp100. FEMS Microbiol Lett 204:355–360PubMedGoogle Scholar
  91. Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolarity environments. Arch Microbiol 170:319–330CrossRefPubMedGoogle Scholar
  92. Khan M, Scullion J (2002) Effects of metal (Cd, Cu, Ni, Pb or Zn) enrichment of sewage-sludge on soil micro-organisms and their activities. Appl Soil Ecol 20:145–155CrossRefGoogle Scholar
  93. 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
  94. Kobayashi R, Suzuki T, Yoshida M (2007) Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol Microbiol 66:100–109CrossRefPubMedGoogle Scholar
  95. Krujatz F, Haarstrick A, Nörtemann B, Greis T (2012) Assessing the toxic effects of nickel, cadmium and EDTA on growth of the plant growth-promoting Rhizobacterium Pseudomonas brassicacearum. Water Air Soil Pollut 223:1281–1293CrossRefGoogle Scholar
  96. Lafay B, Burdon JJ (1998) Molecular diversity of rhizobia occurring on native shrubby legumes in southeastern Australia. Appl Environ Microbiol 64:3989–3997PubMedPubMedCentralGoogle Scholar
  97. 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 34:519–529CrossRefGoogle Scholar
  98. Latrach L, Farissi M, Mouradi M, Makoudi B, Bouizgaren A, Ghoulam C (2014) Growth and nodulation of alfalfa-rhizobia symbiosis under salinity: electrolyte leakage, stomatal conductance, and chlorophyll fluorescence. Turk J Agric For 38:320–326CrossRefGoogle Scholar
  99. Lebrazi S, Benbrahim KF (2014) Environmental stress conditions affecting the N2 fixing Rhizobium-legume symbiosis and adaptation mechanisms. Afr J Microbiol Res 8:4053–4061Google Scholar
  100. Lee M-Y et al (2005) Induction of thioredoxin is required for nodule development to reduce reactive oxygen species levels in soybean roots. Plant Physiol 139:1881–1889CrossRefPubMedPubMedCentralGoogle Scholar
  101. Lemaire B, Van Cauwenberghe J, Chimphango S, Stirton C, Honnay O, Smets E, Muasya AM (2015) Recombination and horizontal transfer of nodulation and ACC deaminase (acdS) genes within alpha-and Betaproteobacteria nodulating legumes of the cape fynbos biome. FEMS Microbiol Ecol 91Google Scholar
  102. Leprince O, Buitink J (2010) Desiccation tolerance: from genomics to the field. Plant Sci 179:554–564CrossRefGoogle Scholar
  103. Lesueur D, Founoune H, Lebonvallet S, Sarr A (2009) Effect of rhizobial inoculation on growth of Calliandra tree species under nursery conditions. New For 39:129–137CrossRefGoogle Scholar
  104. Lesueur D, Deaker R, Herrmann L, Bräu L, Jansa J (2016) The production and potential of biofertilizers to improve crop yields. In: Arora NK, Mehnaz, S., Balestrini, R. (ed) Bioformulations: for sustainable agriculture. pp 71-92Google Scholar
  105. Li J et al (2011) Proteomic study on two Bradyrhizobium japonicum strains with different competitivenesses for nodulation. Agric Sci China 10:1072–1079CrossRefGoogle Scholar
  106. Lima AIG, Corticeiro SC, Figueira EMdAP (2006) Glutathione-mediated cadmium sequestration in Rhizobium leguminosarum. Enzym Microb Technol 39:763–769CrossRefGoogle Scholar
  107. Lira Junior MA, Lima AST, Arruda JRF, Smith DL (2005) Effect of root temperature on nodule development of bean, lentil and pea. Soil Biol Biochem 37:235–239CrossRefGoogle Scholar
  108. Manchanda G, Garg N (2008) Salinity and its effects on the functional biology of legumes. Acta Physiol Plant 30:595–618CrossRefGoogle Scholar
  109. Mandal SM, Gouri SS, De D, Das BK, Mondal KC, Pati BR (2011) Effect of arsenic on nodulation and nitrogen fixation of blackgram (Vigna mungo). Indian J Microbiol 51:44–47CrossRefPubMedPubMedCentralGoogle Scholar
  110. Meena KK et al (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8Google Scholar
  111. Mhadhbi H, Aouani ME (2008) Growth and nitrogen-fixing performances of Medicago truncatula-Sinorhizobium meliloti symbioses under salt (NaCl) stress: micro-and macro-symbiont contribution into symbiosis tolerance. In: Biosaline Agriculture and High Salinity Tolerance. pp 91–98Google Scholar
  112. Michiels J, Verreth C, Vanderleyden J (1994) Effects of temperature stress on bean-nodulating Rhizobium strains. Appl Environ Microbiol 60:1206–1212PubMedPubMedCentralGoogle Scholar
  113. Miller-Williams M, Loewen PC, Oresnik IJ (2006) Isolation of salt-sensitive mutants of Sinorhizobium meliloti strain Rm1021. Microbiol 152:2049–2059CrossRefGoogle Scholar
  114. Mnasri B, Aouani ME, Mhamdi R (2007) Nodulation and growth of common bean (Phaseolus vulgaris) under water deficiency. Soil Biol Biochem 39:1744–1750CrossRefGoogle Scholar
  115. Moulin L, James EK, Klonowska A, Miana de Faria S, Simon MF (2015) Phylogeny, diversity, geographical distribution, and host range of legume-nodulating betaproteobacteria: what is the role of plant taxonomy? de Bruijn FJ Biol nitrogen Fixat Chichester: Wiley:177–190Google Scholar
  116. Mouradi M, Bouizgaren A, Farissi M, Latrach L, Qaddoury A, Ghoulam C (2016) Seed osmopriming improves plant growth, nodulation, chlorophyll fluorescence and nutrient uptake in alfalfa (Medicago sativa L.) – rhizobia symbiosis under drought stress. Sci Hortic 213:232–242CrossRefGoogle Scholar
  117. Münchbach M, Dainese P, Staudenmann W, Narberhaus F, James P (1999) Proteome analysis of heat shock protein expression in Bradyrhizobium japonicum. FEBS J 264:39–48Google Scholar
  118. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  119. Nandal K, Sehrawat AR, Yadav AS, Vashishat R, Boora K (2005) High temperature-induced changes in exopolysaccharides, lipopolysaccharides and protein profile of heat-resistant mutants of Rhizobium sp.(Cajanus). Microbiol Res 160:367–373CrossRefPubMedGoogle Scholar
  120. Nandasena KG, O'Hara GW, Tiwari RP, Sezmiş E, Howieson JG (2007) In situ lateral transfer of symbiosis islands results in rapid evolution of diverse competitive strains of Mesorhizobia suboptimal in symbiotic nitrogen fixation on the pasture legume Biserrula pelecinus L. Environ Microbiol 9:2496–2511CrossRefPubMedGoogle Scholar
  121. Neudorf KD, Vanderlinde EM, Tambalo DD, Yost CK (2015) A previously uncharacterized tetratricopeptide-repeat-containing protein is involved in cell envelope function in Rhizobium leguminosarum. Microbiol 161:148–157CrossRefGoogle Scholar
  122. Nomura M et al (2010) Differential protein profiles of Bradyrhizobium japonicum USDA110 bacteroid during soybean nodule development. J Soil Sci Plant Nutr 56:579–590CrossRefGoogle Scholar
  123. O'Connell KP, Thomashow MF (2000) Transcriptional organization and regulation of a polycistronic cold shock operon in Sinorhizobium meliloti RM1021 encoding homologs of the Escherichia coli major cold shock gene cspA and ribosomal protein gene rpsU. Appl Environ Microbiol 66:392–400CrossRefPubMedPubMedCentralGoogle Scholar
  124. Paço A, Brígido C, Alexandre A, Mateos PF, Oliveira S (2016) The symbiotic performance of chickpea rhizobia can be improved by additional copies of the clpB chaperone gene. PLoS One 11:e0148221CrossRefPubMedPubMedCentralGoogle Scholar
  125. Pajuelo E, Rodríguez-Llorente ID, Dary M, Palomares AJ (2008) Toxic effects of arsenic on SinorhizobiumMedicago sativa symbiotic interaction. Environ Pollut 154:203–211CrossRefPubMedGoogle Scholar
  126. Pal A, Paul AK (2008) Microbial extracellular polymeric substances: central elements in heavy metal bioremediation. Indian J Microbiol 48:49CrossRefPubMedPubMedCentralGoogle Scholar
  127. Parker MA (2015) The spread of Bradyrhizobium lineages across host legume clades: from Abarema to Zygia. Microb Ecol 69:630–640CrossRefPubMedGoogle Scholar
  128. Paudyal S, Aryal RR, Chauhan S, Maheshwari D (2007) Effect of heavy metals on growth of Rhizobium strains and symbiotic efficiency of two species of tropical legumes. Sci World 5:27–32CrossRefGoogle Scholar
  129. Pauly N et al (2006) Reactive oxygen and nitrogen species and glutathione: key players in the legume–Rhizobium symbiosis. J Exp Bot 57:1769–1776CrossRefPubMedGoogle Scholar
  130. Payakapong W, Tittabutr P, Teaumroong N, Boonkerd N, Singleton PW, Borthakur D (2006) Identification of two clusters of genes involved in salt tolerance in Sinorhizobium sp. strain BL3. Symbiosis 41:47–53Google Scholar
  131. Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial associations with legumes. CRC Crit Rev Plant Sci 34:17–42CrossRefGoogle Scholar
  132. Platero R et al (2016) Novel Cupriavidus strains isolated from root nodules of native Uruguayan Mimosa species. Appl Environ Microbiol:AEM. 04142–04115Google Scholar
  133. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755PubMedPubMedCentralGoogle Scholar
  134. Queitsch C, Hong S-W, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492CrossRefPubMedPubMedCentralGoogle Scholar
  135. Raju RM et al (2014) Post-translational regulation via Clp protease is critical for survival of Mycobacterium tuberculosis. PLoS Pathog 10:e1003994CrossRefPubMedPubMedCentralGoogle Scholar
  136. Ramos JL, Gallegos M-T, Marqués S, Ramos-González M-I, Espinosa-Urgel M, Segura A (2001) Responses of gram-negative bacteria to certain environmental stressors. Curr Opin Microbiol 4:166–171CrossRefPubMedGoogle Scholar
  137. Reeve WG et al (2004) Probing for pH-regulated proteins in Sinorhizobium medicae using proteomic analysis. J Mol Microbiol Biotechnol 7:140–147CrossRefPubMedGoogle Scholar
  138. Reichman S (2007) The potential use of the legume–rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol Biochem 39:2587–2593CrossRefGoogle Scholar
  139. Remigi P, Zhu J, Young JPW, Masson-Boivin C (2016) Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. TIM 24:63–75Google Scholar
  140. Riccillo PM, Muglia CI, de Bruijn FJ, Roe AJ, Booth IR, Aguilar OM (2000) Glutathione is involved in environmental stress responses in <em>Rhizobium tropici</em>, Including acid tolerance. J Bacteriol 182:1748–1753. CrossRefPubMedPubMedCentralGoogle Scholar
  141. Robinson B, Russell C, Hedley M, Clothier B (2001) Cadmium adsorption by rhizobacteria: implications for New Zealand pastureland. Agric Ecosyst Environ 87:315–321CrossRefGoogle Scholar
  142. Rodrigues CS, Laranjo M, Oliveira S (2006) Effect of heat and pH stress in the growth of chickpea mesorhizobia. Curr Microbiol 53:1–7CrossRefPubMedGoogle Scholar
  143. Romdhane SB, Trabelsi M, Aouani ME, De Lajudie P, Mhamdi R (2009) The diversity of rhizobia nodulating chickpea (Cicer arietinum) under water deficiency as a source of more efficient inoculants. Soil Biol Biochem 41:2568–2572CrossRefGoogle Scholar
  144. Roughley RJ, Gemell LG, Thompson JA, Brockwell J (1993) The number of Bradyrhizobium SP. (Lupinus) applied to seed and its effect on rhizosphere colonization, nodulation and yield of lupin. Soil Biol Biochem 25:1453–1458CrossRefGoogle Scholar
  145. Sadowsky MJ (2005) Soil stress factors influencing symbiotic nitrogen fixation. In: Nitrogen fixation in agriculture, forestry, ecology, and the environment. Springer, pp 89–112Google Scholar
  146. Saikia SP, Bora D, Goswami A, Mudoi KD, Gogoi A (2012) A review on the role of Azospirillum in the yield improvement of non leguminous crops. Afr J Microbiol Res 6:1085–1102CrossRefGoogle Scholar
  147. Salehizadeh H, Shojaosadati S (2003) Removal of metal ions from aqueous solution by polysaccharide produced from Bacillus firmus. Water Res 37:4231–4235CrossRefPubMedGoogle Scholar
  148. Sankhla IS et al (2017) Molecular characterization of nitrogen fixing microsymbionts from root nodules of Vachellia (acacia) jacquemontii, a native legume from the Thar Desert of India. Plant Soil 410:21–40CrossRefGoogle Scholar
  149. Sarma AD, Emerich DW (2005) Global protein expression pattern of Bradyrhizobium japonicum bacteroids: a prelude to functional proteomics. Proteomics 5:4170–4184CrossRefPubMedGoogle Scholar
  150. Sassi-Aydi S, Aydi S, Abdelly C (2014) Inorganic nitrogen nutrition enhances osmotic stress tolerance in Phaseolus vulgaris: lessons from a drought-sensitive cultivar. HortScience 49:550–555CrossRefGoogle Scholar
  151. Schneider KA et al (1997) Improving common bean performance under drought stress. Crop Sci 37:43–50CrossRefGoogle Scholar
  152. Serraj R (2003) Effects of drought stress on legume symbiotic nitrogen fixation: physiological mechanisms. Indian J Exp Biol 41:1136–1141PubMedGoogle Scholar
  153. Shirkey B et al (2000) Active Fe-containing superoxide dismutase and abundant sodF mRNA in Nostoc commune (cyanobacteria) after years of desiccation. J Bacteriol 182:189–197CrossRefPubMedPubMedCentralGoogle Scholar
  154. Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2Google Scholar
  155. Silvente S, Sobolev AP, Lara M (2012) Metabolite adjustments in drought tolerant and sensitive soybean genotypes in response to water stress. PLoS One 7:e38554CrossRefPubMedPubMedCentralGoogle Scholar
  156. Smith E, Smith J, Smith L, Biswas T, Correll R, Naidu R (2003) Arsenic in Australian environment: an overview. J Environ Sci Health A 38:223–239CrossRefGoogle Scholar
  157. Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhiza. Plant Soil 326:3–20CrossRefGoogle Scholar
  158. Soussi M, Santamaria M, Ocana A, Lluch C (2001) Effects of salinity on protein and lipopolysaccharide pattern in a salt-tolerant strain of Mesorhizobium ciceri. J Appl Microbiol 90:476–481CrossRefPubMedGoogle Scholar
  159. Sprent JI, Ardley J, James EK (2017) Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol 215:40–56CrossRefPubMedGoogle Scholar
  160. Stępkowski T, Watkin E, McInnes A, Gurda D, Gracz J, Steenkamp ET (2012) Distinct Bradyrhizbium communities nodulate legumes native to temperate and tropical monsoon Australia. Mol Phylogenet Evol 63:265–277CrossRefPubMedGoogle Scholar
  161. Streeter JG (1985) Accumulation of alpha, alpha-trehalose by Rhizobium bacteria and bacteroids. J Bacteriol 164:78–84PubMedPubMedCentralGoogle Scholar
  162. Streeter JG (2003) Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation. J Appl Microbiol 95:484–491CrossRefPubMedGoogle Scholar
  163. Sugawara M, Cytryn EJ, Sadowsky MJ (2010) Functional role of Bradyrhizobium japonicum Trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Appl Environ Microbiol 76:1071–1081CrossRefPubMedGoogle Scholar
  164. Turner NC, Wright GC, Siddique K (2001) Adaptation of grain legumes (pulses) to water-limited environments. Adv Agron 71:193–231CrossRefGoogle Scholar
  165. Vanderlinde EM, Harrison JJ, Muszyński A, Carlson RW, Turner RJ, Yost CK (2010) Identification of a novel ABC transporter required for desiccation tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Lett 71:327–340CrossRefGoogle Scholar
  166. Vriezen JAC, de Bruijn FJ, Nüsslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Appl Environ Microbiol 73:3451–3459CrossRefPubMedPubMedCentralGoogle Scholar
  167. Wdowiak-Wróbel S, Małek W, Leszcz A, Typek R, Dawidowicz AL (2016) Effect of osmotic stress on Astragalus cicer microsymbiont growth and survival. Eur J Soil Biol 76:46–52CrossRefGoogle Scholar
  168. Wei W, Jiang J, Li X, Wang L, Yang S (2004) Isolation of salt-sensitive mutants from Sinorhizobium meliloti and characterization of genes involved in salt tolerance. Lett Appl Microbiol 39:278–283CrossRefPubMedGoogle Scholar
  169. 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 174:1–8CrossRefPubMedGoogle Scholar
  170. Yates RJ, Howieson JG, Nandasena KG, O'Hara GW (2004) Root-nodule bacteria from indigenous legumes in the north-west of Western Australia and their interaction with exotic legumes. Soil Biol Biochem 36:1319–1329CrossRefGoogle Scholar
  171. Yelton M, Yang S, Edie S, Lim S (1983) Characterization of an effective salt-tolerant, fast-growing strain of Rhizobium japonicum. Microbiol 129:1537–1547CrossRefGoogle Scholar
  172. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989PubMedPubMedCentralGoogle Scholar
  173. Zhang X, Harper R, Karsisto M, Lindström K (1991) Diversity of Rhizobium bacteria isolated from the root nodules of leguminous trees. Int J Syst Evol Microbiol 41:104–113Google Scholar
  174. Zhang F, Lynch DH, Smith DL (1995) Impact of low root temperatures in soybean [Glycine max.(L.) Merr.] on nodulation and nitrogen fixation. Environ Exp Bot 35:279–285CrossRefGoogle Scholar
  175. Zhang JJ et al (2012) Distinctive Mesorhizobium populations associated with Cicer arietinum L. in alkaline soils of Xinjiang, China. Plant Soil 353:123–134CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.CIAT-AsiaHanoiVietnam
  2. 2.Eco&SolsUniversity Montpellier, CIRADMontpellierFrance
  3. 3.CIRAD, UMR Eco&Sols, CIAT-AsiaHanoiVietnam
  4. 4.Deakin UniversityMelbourneAustralia

Personalised recommendations