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Salt-Tolerant Microbes: Isolation and Adaptation

  • Mohammad Javad ZareaEmail author
Chapter
Part of the Soil Biology book series (SOILBIOL, volume 56)

Abstract

One of the major obstacles limiting agriculture in arid and semiarid areas of the world is salinity. Arid and semiarid areas are affected by salinity of soil and water. Global changes aggress this issue and trigger the agricultural area into unproductive. Increasing salinity of soil and water decreases yield of importance of economic crops. Several strategies have been assumed to be used in order to deal with soil salinity. Moreover, using beneficial microorganisms is of great interest. This article review doesn’t aim to repeat the beneficial role of plant growth-promoting bacteria in agriculture since, in this regard, many valuable article reviews have been published previously. The major aim and point of this review are to discuss the strategies used for the isolation of the beneficial saline-adapted bacteria for crop production under salinity condition. Isolation procedures of the different groups of beneficial bacteria including rhizobacteria, rhizobia, and phosphorus solubilizing bacteria have been reviewed in this chapter.

Keywords

Salinity Salt stress Crop production Plant growth-promoting rhizobacteria Salt adaptation 

References

  1. Abdelmoumen H, Filali-Maltouf A, Neyra M, Belabed A, El Idrissi MM (1999) Effect of high salts concentrations on the growth of rhizobia and responses to added osmotica. J Appl Microbiol 86:889–898CrossRefGoogle Scholar
  2. Baldani JI, Baldani VLD, Sampaio MJAM, Döbereiner J (1984) A fourth Azospirillum species from cereal roots. An Acad Bras Ci 56:265Google Scholar
  3. Baldani VLD, Baldani JI, Olivares FL, Döbereiner J (1992) Identification and ecology of Herbaspirillum seropedicae and the closely related Pseudomonas rubrisubalbicans. Symbiosis 19:65–73Google Scholar
  4. Baldani JI, Pot TB, Kirchhof G, Falsen E, Baldani VLD, Olivares FL, Hoste B, Kersters K, Hartmann A, Gillis M, Döbereiner J (1996) Emended description of Herbaspirillum, a mild plant pathogen, as Herbaspirillum rubrisubalbicans comb. nov.; and classification of a group of clinical isolates (EF group 1) as Herbaspirillum species 3. Int J Syst Bacteriol 46:802–810PubMedCrossRefGoogle Scholar
  5. Baldani VLD, Baldani JI, Döbereiner J (2000) Inoculation of rice plants with the endophytic diazotrophs Herbapirillum seropedicae and Burkholderia spp. Biol Fertil Soils 30:485–491CrossRefGoogle Scholar
  6. Baldani JI, Reis VM, Videira SS, Boddey LH, Baldani VLD (2014) The art of isolating nitrogen-fixing bacteria from non-leguminous plants using N-free semi-solid media: a practical guide for microbiologists. Plant Soil 384:413–431CrossRefGoogle Scholar
  7. Bertrand A, Dhont C, Bipfubusa M, Chalifour FP, Drouin P, Beauchamp CJ (2015) Improving salt stress responses of the symbiosis in alfalfa using salt-tolerant cultivar and rhizobial strain. Appl Soil Ecol 87:108–117CrossRefGoogle Scholar
  8. Bharti N, Yadav D, Barnawal D, Maji D, Kalra A (2013) Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J Microbiol Biotechnol 29:379–387PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bibi F, Chung EJ, Yoon HS, Song GC, Jeon CO, Chung YR (2011) Haloferula luteola sp nov., an endophytic bacterium isolated from the root of a halophyte, Rosa rugosa, and emended description of the genus Haloferula. Int J Syst Evol Microbiol 61:1837–1841PubMedCrossRefGoogle Scholar
  10. Brignoli E, Lauteri M (1991) Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt-tolerant (Gossypium hirsutum L.) and salt-sensitive (Phaseolus vulgaris L.) C, non-halophytes. Plant Physiol 95:638–635Google Scholar
  11. Cavalcante VA, Döbereiner J (1988) A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. Plant Soil 108:23–31CrossRefGoogle Scholar
  12. Çelen E, Mehmet AK (2004) Isolation and characterization of aerobic denitrifiers from agriculture soil. Turk J Biol 28:9–14Google Scholar
  13. Chen WM, Lee TM, Lan CC, Cheng CP (2000) Characterization of halotolerant rhizobia isolated from root nodules of Canavalia rosea from seaside areas. FEMS Microbiol Ecol 34:9–16PubMedCrossRefGoogle Scholar
  14. Chen M-H, Sheu S-Y, James EK, Young C-C, Chen W-M (2013) Azoarcus olearius sp. nov., a nitrogen-fixing bacterium isolated from oil-contaminated soil. Int J Syst Evol Microbiol 63:3755–3761PubMedCrossRefGoogle Scholar
  15. Chung EJ, Park JA, Jeon CO, Chung YR (2015) Gynuella sunshinyii gen. nov., sp nov., an antifungal rhizobacterium isolated from a halophyte, Carex scabrifolia Steud. Int J Syst Evol Microbiol 65:1038–1043PubMedPubMedCentralCrossRefGoogle Scholar
  16. Craig GF, Atkins CA, Bell DT (1991) Effect of salinity on growth of Rhizobium and their infectivity and effectiveness on two species of Acacia. Plant Soil 133:253–262CrossRefGoogle Scholar
  17. Dalton H, Postgate JR (1968) Effect of oxygen on growth of Azotobacter chroococcum in batch and continuous cultures. J Gen Microbiol 54:463–473PubMedCrossRefGoogle Scholar
  18. Delvasto P, Valverde A, Igual JM, Munoz JA, Gonzalez F, Blazquez ML, Garcia-Balboa C (2006) Diversity and activity of phosphate bioleaching bacteria from a high phosphorous iron-ore. Soil Biol Biochem 38:2645–2654CrossRefGoogle Scholar
  19. Diby P, Sarma YR, Srinivasan V, Anandaraj M (2005) Pseudomonas fluorescens mediated vigour in black pepper (piper nigrum L.) under greenhouse cultivation. Ann Microbiol 55:171–174Google Scholar
  20. Döbereiner J, Day JM (1976) Associative symbiosis in tropical grasses: characterization of microorganisms and dinitrogen fixing sites. In: Newton WE, Nyman CJN (eds) Proceedings of 1st international symposium on nitrogen fixation. Washington State University Press, Washington, pp 518–538Google Scholar
  21. Döbereiner J, Pedrosa FO (1987) Nitrogen-fixing bacteria in nonleguminous crop plants, Brock/Springer series in contemporary bioscience. Springer, New YorkGoogle Scholar
  22. Domínguez-Ferreras A, Pérez-Arnedo R, Becker A, Olivares J, Soto MJ, Sanjuán J (2006) Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti. J Bacteriol 188:7617–7625PubMedPubMedCentralCrossRefGoogle Scholar
  23. Dong R, Zhang J, Huan H, Bai C, Chen Z, Liu G (2017) High salt tolerance of a Bradyrhizobium strain and its promotion of the growth of Stylosanthes guianensis. Int J Mol Sci 18:1625PubMedCentralCrossRefPubMedGoogle Scholar
  24. Eckert B, Weber OB, Kirchhof G, Halbritter A, Stoffels M, Hartmann A (2001) Azospirillum doebereinerae sp. nov., a nitrogen fixing bacterium associated with the C4-grass Miscanthus. Int J Syst Evol Microbiol 51:17–26PubMedCrossRefGoogle Scholar
  25. Egamberdieva D, Lindström LL, Räsänen La K (2015) A synergistic interaction between salt-tolerant Pseudomonas and Mesorhizobium strains improves growth and symbiotic performance of liquorice (Glycyrrhiza uralensis Fish.) under salt stress. Appl Microbiol Biotechnol 100:2829–2841PubMedCrossRefGoogle Scholar
  26. El-Sheikh EAE, Wood M (1995) Nodulation and N2 fixation by soybean inoculated with salt-tolerant rhizobia or salt-sensitive Bradyrhizobium in saline soil. Soil Biol Biochem 27:657–661CrossRefGoogle Scholar
  27. Estrada-de-los-Santos P, Bustillos-Cristales R, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67:2790–2798PubMedPubMedCentralCrossRefGoogle Scholar
  28. Fred EB, Waksman SA (1928) Laboratory manual of general microbiology. McGraw-Hill Book, LondonGoogle Scholar
  29. Fujihara S, Yoneyama T (1993) Effects of pH and osmotic stress on cellular polyamine contents in the soybean rhizobia Rhizobium fredii P220 and Bradyrhizobium japonicum A1017. Appl Environ Microbiol 59:1104–1109PubMedPubMedCentralGoogle Scholar
  30. Georg J, Voss B, Scholz I, Mitschke J, Wilde A, Hess W (2009) Evidence for a major role of antisense RNAs in cyanobacterial gene regulation. Mol Syst Biol 5:305PubMedPubMedCentralCrossRefGoogle Scholar
  31. Goswami D, Dhandhukia P, Patel P, Thakker JN (2014) Screening of PGPR from saline desert of Kutch: growth promotion in Arachis hypogaea by Bacillus licheniformis A2. Microbiol Res 169:66–75PubMedPubMedCentralCrossRefGoogle Scholar
  32. Graham PH (1992) Stress tolerance in Rhizobium and Bradyrhizobium and nodulation under adverse soil conditions. Can J Microbiol 38:475–484CrossRefGoogle Scholar
  33. Graham PH, Parker CA (1964) Diagnostic features in the characterization of the root nodule bacteria of legumes. Plant Soil 20:383–396CrossRefGoogle Scholar
  34. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395–412CrossRefGoogle Scholar
  35. Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35:87–123PubMedCrossRefGoogle Scholar
  36. Han Y, Wang Ch, Li X, Cao X, Cao A, Zhao N (2014) Isolation and identification of saline tolerance phosphate-solubilizing bacteria derived from salt-affected soils and their mechanisms of P-solubilizing. In: Zhang TC et al (eds) Proceedings of the 2012 international conference on applied biotechnology (ICAB 2012). Lecture notes in electrical engineering, vol 250. Springer, Berlin.  https://doi.org/10.1007/978-3-642-37922-2_135 Google Scholar
  37. Hartmann A, Baldani JI (2006) The Genus Azospirillum. In: Rosemberg E, Schleifer K-H, Stackerbrandt E (eds) The prokaryotes. Springer, New YorkGoogle Scholar
  38. Helemish FA, El-Gammal SMA (1987) Salt and pH tolerance of Rhizobium leguminosarum TAL-271. Zbl Microbiol 142:211Google Scholar
  39. Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation to agricultural systems. Plant Soil 311:1–18CrossRefGoogle Scholar
  40. Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 8:1768PubMedPubMedCentralCrossRefGoogle Scholar
  41. Jha B, Gontia I, Hartmann A (2012) The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil 356:265–277CrossRefGoogle Scholar
  42. Kirchhof G, Eckert B, Stoffels M, Baldani JI, Reis VM, Hartmann A (2001) Herbaspirillum frisingense sp. nov., a new nitrogen-fixing bacterial species that occurs in C4-fiber plants. Int J Syst Evol Microbiol 51:157–168PubMedCrossRefPubMedCentralGoogle Scholar
  43. Klein W, Weber MH, Marahiel MA (1999) Cold shock response of Bacillus subtilis: isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures. J Bacteriol 181:5341–5349PubMedPubMedCentralGoogle Scholar
  44. Lal B, Khanna S (1995) Selection of salt tolerant Rhizobium isolates of Acacia nilotica. World J Microbiol Biotechnol 10:637–639CrossRefGoogle Scholar
  45. Laranjo M, Oliveira S (2011) Tolerance of Mesorhizobium type strains to different environmental stresses. Anton Leeuw 99:651–662CrossRefGoogle Scholar
  46. Lavrinenko K, Chernousova E, Gridneva E et al (2010) Azospirillum thiophilum sp. nov., a novel diazotrophic bacterium isolated from a sulfide spring. Int J Syst Evol Microbiol 60:2832–2837PubMedCrossRefGoogle Scholar
  47. Lin S-H, Liu Y-C, Hameed A, Hsu YH, Lai WA, Shen FT, Young CC (2013) Azospirillum fermentarium sp. nov., a novel nitrogen fixing species isolated from a fermenter. Int J Syst Evol Microbiol 63:3762–3768. (in Taiwan)PubMedCrossRefGoogle Scholar
  48. Liu Y, Gao W, Wang Y, Wu L, Liu X, Yan T et al (2005) Transcriptome analysis of Shewanella oneidensis MR-1 in response to elevated salt conditions. J Bacteriol 187:2501–2507PubMedPubMedCentralCrossRefGoogle Scholar
  49. Loganathan P, Nair S (2004) Swaminathania salitolerans gen. nov., sp. nov., a salt-tolerant, nitrogen-fixing and phosphate solubilizing bacterium from wild rice (Porteresia coarctata Tateoka). Int J Syst Evol Microbiol 54:1185–1190PubMedCrossRefGoogle Scholar
  50. Magalhães FMM, Döbereiner J (1984) Occurrence of Azospirillum amazonense in some Amazonian ecosystems. Rev Microbiol 4:246–252Google Scholar
  51. Mehnaz S, Weselowski B, Lazarovits G (2007a) Azospirillum canadense sp. nov., a nitrogen-fixing bacterium isolated from corn rhizosphere. Int J Syst Evol Microbiol 57:620–624PubMedCrossRefGoogle Scholar
  52. Mehnaz S, Weselowski B, Lazarovits G (2007b) Azospirillum zeae sp. nov., a diazotrophic bacterium isolated from rhizosphere soil of Zea mays. Int J Syst Evol Microbiol 57:2805–2809PubMedCrossRefGoogle Scholar
  53. Moussaid S, Domínguez-Ferreras A, Muñoz S, Aurag J, Sanjuán J (2015) Increased trehalose biosynthesis improves Mesorhizobium ciceri growth and symbiosis establishment in saline conditions. Symbiosis 67:103–111CrossRefGoogle Scholar
  54. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedPubMedCentralCrossRefGoogle Scholar
  55. Nabti E, Sahnoune M, Adjrad S, Van Dommelen A, Ghoul M, Schmid M, Hartmann A (2007) A halophilic and osmotolerant Azospirillum brasilense strain from Algerian soil restores wheat growth under saline conditions. Eng Life Sci 7:354–360CrossRefGoogle Scholar
  56. Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270PubMedCrossRefGoogle Scholar
  57. Oren A (2006) The order Halobacteriales. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes, vol 3, 3rd edn, pp 113–164CrossRefGoogle Scholar
  58. Parker CA, Trinick MR, Chatel DL (1977) Rhizobia as soil and rhizosphere inhabitants. In: Hardy RWF, Gibson AH (eds) A treatise on dinitrogen fixation, vol 4. Wiley, New York, pp 311–352Google Scholar
  59. Paul D, Lade H (2014) Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev 34:737–752CrossRefGoogle Scholar
  60. Paul D, Dineshkumar N, Nair S (2006) Proteomics of a plant growth promoting rhizobacterium, Pseudomonas fluorescens MSP-393, subjected to salt shock. World J Microbiol Biotechnol 22:369–374CrossRefGoogle Scholar
  61. Peng G, Wang H, Zhang G et al (2006) Azospirillum melinis sp. nov., a group of diazotrophs isolated from tropical molasses grass. Int J Syst Evol Microbiol 56:1263–1271PubMedCrossRefGoogle Scholar
  62. Pérez-Montaño F, del Cerro P, Jiménez-Guerrero I, López-Baena FJ, Cubo MT, Hungria M, Megías M, Ollero FJ (2016) RNA-seq analysis of the Rhizobium tropici CIAT 899 transcriptome shows similarities in the activation patterns of symbiotic genes in the presence of apigenin and salt. BMC Genomics 17:198PubMedPubMedCentralCrossRefGoogle Scholar
  63. Pikovskaya RI (1948) Mobilization of phosphorous in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17:362–370Google Scholar
  64. Qu LQ, Huang YY, Zhu CM, Zeng HQ, Shen CJ, Liu C, Zhao Y, Pi EX (2016) Rhizobia-inoculation enhances the soybean’s tolerance to salt stress. Plant Soil 400:209–222CrossRefGoogle Scholar
  65. Ramadoss D, Lakkineni VK, Bose P, Ali S, Annapurna K (2013) Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats. Springerplus 2:1–7CrossRefGoogle Scholar
  66. Reinhold B, Hurek T, Niemann EG, Pendrik I (1986) Close association of Azospirillum and diazotrophic rods with different root zones of Kallar grass. Appl Environ Microbiol 52:520–526PubMedPubMedCentralGoogle Scholar
  67. Reinhold B, Hurek T, Fendrik I, Pot B, Gillis M, Kersters K, Thielemans S, De Ley J (1987) Azospirillum halopraeferens sp. nov., a nitrogen-fixing organism associated with roots of Kallar Grass (Leptochloa fusca (L.) Kunth). Int J Syst Bacteriol 37:43–51CrossRefGoogle Scholar
  68. Reinhold B, Hurek T, Baldani J, Dobereiner J (1988) Temperature and salt tolerance of Azospirillum spp. from salt affected soils in Brazil. In: Klingmueller W (ed) Azospirillum IV genetics, physiology, ecology. Springer, Berlin, pp 234–241Google Scholar
  69. Reis VM, Olivares FL, Döbereiner J (1994) Improved methodology for isolation of Acetobacter diazotrophicus and confirmation of its endophytic habitat. World J Microbiol Biotechnol 10:401–405PubMedCrossRefGoogle Scholar
  70. Richardson AE (2007) Making microorganisms mobilize soil phosphorus. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilizationGoogle Scholar
  71. Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114PubMedCrossRefGoogle Scholar
  72. Rosenberg A (1983) Pseudomonas halodurans sp. nov., a halotolerant bacterium. Arch Microbiol 136:117–123CrossRefGoogle Scholar
  73. Sandhya V, ASK Z, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAPP45. Biol Fertil Soils 46:17–26CrossRefGoogle Scholar
  74. Santos H, da Costa MS (2002) Compatible solutes of organisms that live in hot saline environments. Environ Microbiol 4:501–509PubMedCrossRefGoogle Scholar
  75. Sauvage D, Hamelin J, Larher F (1983) Glycine betaine and other structurally related compounds improve the salt tolerance of Rhizobium meliloti. Plant Sci Lett 31:291–302CrossRefGoogle Scholar
  76. Seeman JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomata1 behaviour and photosynthetic capacity of a salt-sensitive species Phaseolus vulgaris L. Plania 144:151–162Google Scholar
  77. Shamseldin A, Werner D (2005) High salt and high pH tolerance of new isolated Rhizobium etli strains from Egyptian soils. Curr Microbiol 50:11–16PubMedCrossRefGoogle Scholar
  78. Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front Microbiol Front Microbiol 7:1600PubMedGoogle Scholar
  79. Shukla PS, Agarwal PK, Jha B (2012) Improved salinity tolerance of Arachis hypogaea (L.) by the interaction of halotolerant plant-growth-promoting rhizobacteria. J Plant Growth Regul 31:195–206CrossRefGoogle Scholar
  80. Singleton PW, Bohlool BB (1984) Effect of salinity on nodule formation by soybean. Plant Physiol 74:72–76PubMedPubMedCentralCrossRefGoogle Scholar
  81. Singleton PW, EL-Swaify SA, Bohlool BB (1982) Effect of salinity on Rhizobium growth and survival. Appl Environ Microbiol 44:884–890PubMedPubMedCentralGoogle Scholar
  82. Son HJ, Park GT, Cha MS, Heo MS (2006) Solubilization of insoluble inorganic phosphates by a novel salt and pH tolerant Pantoea agglomerans R-42 isolated from Soybean rhizophere. Bioresour Technol 97:204–210PubMedCrossRefGoogle Scholar
  83. Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen JG (2001) Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalimicrobium sibiricum. sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp. nov. and Thioalkalivibrio denitrificans sp. nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int J Syst Evol Microbiol 51:565–580PubMedCrossRefGoogle Scholar
  84. Steil L, Hoffmann T, Budde I, Volker U, Bremer E (2003) Genome-wide transcriptional profiling analysis of adaptation of Bacillus subtilis to high salinity. J Bacteriol 185:6358–6370PubMedPubMedCentralCrossRefGoogle Scholar
  85. Ventorino V, Caputo R, De Pascale S, Fagnano M, Pepe O, Moschetti G (2012) Response to salinity stress of Rhizobium leguminosarum bv. viciae strains in the presence of different legume host plants. Ann Microbiol 62:811–823CrossRefGoogle Scholar
  86. Videira SS, Araújo JLS, Rodrigues LS, Baldani VLD, Baldani JI (2009) Occurrence and diversity of nitrogen-fixing Sphingomonas bacteria associated with rice plants grown in Brazil. FEMS Microbiol Lett 293:11–19PubMedCrossRefPubMedCentralGoogle Scholar
  87. Weber A, Jung K (2002) Profiling early osmostress-dependant gene expression in Escherichia coli using DNA macroarrays. J Bacteriol 184:5502–5507PubMedPubMedCentralCrossRefGoogle Scholar
  88. Wei GH, Yang XY, Zhang ZX, Yang YZ, Lindstrom K (2008) Strain Mesorhizobium sp. CCNWGX035; A stress tolerant isolate from Glycyrrhiza glabra displaying a wide host range of nodulation. Pedosphere 18:102–112CrossRefGoogle Scholar
  89. Whatmore AM, Chudek JA, Reed RH (1990) The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis. J Gen Microbiol 136:2527–2535PubMedCrossRefGoogle Scholar
  90. Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate solubilizing fungi. Adv Agron 69:99–151CrossRefGoogle Scholar
  91. Winogradsky S (1949) Microbiologie du sol. Masson et Cie, Paris, 861 pGoogle Scholar
  92. Xiang W, Liang H, Liu S, Luo F, Tang J, Li M-Y, Che Z-M (2011) Isolation and performance evaluation of halotolerant phosphate solubilizing bacteria from the rhizospheric soils of historic Dagong Brine Well in China. World J Microbiol Biotechnol 27:2629–2637CrossRefGoogle Scholar
  93. Yelton MM, Yang SS, Edie SA, Lim ST (1983) Characterization of an effective salt tolerant fast growing strain of Rhizobium japonicum. J Gen Microbiol 129:1537–1547Google Scholar
  94. Zarea MJ, Hajinia S, Karimi N, Mohammadi Goltapeh E, Rejali F, Varma A (2012) Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol Biochem 45:139–146CrossRefGoogle Scholar
  95. Zarea MJ, Chordia P, Varma A (2013a) Piriformospora indica versus salt stress. In: Varma A, Kost G, Oelmüller R (eds) Piriformospora indica. Springer, Berlin, pp 263–281CrossRefGoogle Scholar
  96. Zarea MJ, Mohammadi Goltapeh E, Karimi N, Varma A (2013b) Sustainable agriculture in saline-arid and semiarid by use potential of AM fungi on mitigates NaCl effects. In: Mohammadi Goltapeh EM, Rezaidanesh Y, Varama A (eds) Fungi as bioremediators, Soil biology, vol 32. Springer, Berlin, pp 340–370CrossRefGoogle Scholar
  97. Zarea MJ, Miransari M, Karimi N (2014) Plant physiological mechanisms of salt tolerance induced by mycorrhizal fungi and Piriformospora indica. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses. Springer, New YorkGoogle Scholar
  98. Zhao XR, Lin QM (2001) A review of phosphate—dissolving microorganisms. Soil Fertil 3:7–11Google Scholar
  99. Zhou S, Han L, Wang Y, Yang G, Zhuang L, Hu P (2012) Azospirillum humicireducens sp. nov., a nitrogen-fixing bacterium isolated from a microbial fuel cell. Int J Syst Evol Microbiol 63:2618–2624PubMedCrossRefGoogle Scholar
  100. Zhu F, Qu L, Hong X, Sun X (2011) Isolation and characterization of a phosphate-solubilizing halophilic bacterium Kushneria sp. YCWA18 from Daqiao Saltern on the coast of yellow sea of China. J Evid Based Complement Altern 2011:1–6Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Faculty of Agriculture, Department of Agronomy and Plant BreedingIlam UniversityIlamIran

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