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Bradyrhizobia-Mediated Drought Tolerance in Soybean and Mechanisms Involved

  • Abhishek Bharti
  • Richa Agnihotri
  • Hemant S. Maheshwari
  • Anil Prakash
  • Mahaveer P. Sharma
Chapter

Abstract

Among various legume crops grown across the world, soybean (Glycine max L. Merrill) is emerging as one of the fastest-growing oilseed crops in the world containing about 40% protein and 20% oil and is also being used as potential feed for animals. Drought stress being a major abiotic stress factor affects the soybean productivity adversely. Thus, to enhance the productivity of soybean, besides managing the nutrients, stress management is of utmost importance. There is enormous potential for opportunity of application of microbes especially bradyrhizobia either applied alone or co-inoculated with plant growth-promoting rhizobacteria (PGPR), and AM fungi can help in nutrient mobilization and confer tolerance to plants by alleviating adverse effects of stresses. Bradyrhizobia are mainly slow-growing, ubiquitous group of soil bacteria known as root symbiont; this is symbiotically associated with roots of soybean plants. In this chapter, we provided on how drought affects the soybean production worldwide and utilized specific bradyrhizobial strains to confer tolerance to soybean plants under drought stress and to understand the mechanisms imparting in the reduction of abiotic stress, e.g., GOGGAT MAPK, different polysaccharides, and other precursors involved in drought stress recovering mechanism. The enhancement of the soybean bradyrhizobial symbiosis participating in the drought tolerance particularly with climate smart bradyrhizobia having high osmotolerant traits, persisting longer in the field, and availability of such inoculants have also been discussed.

Keywords

Bradyrhizobia PGPR AM fungi Abiotic stress 

Notes

Acknowledgments

The authors would like to thank the Director of ICAR-Indian Institute of Soybean Research, Indore, for providing the necessary facilities. Funding from ICAR-AMAAS network subproject to MPS and fellowship to AB is gratefully acknowledged.

References

  1. Abate T, Alene AD, Bergvinson D, Shiferaw B, Silim S, Orr A, Asfaw S (2012) Tropical grain legumes in Africa and South Asia: knowledge and opportunities. International Crops Research Institute for the SemiArid Tropics, Nairobi. 112 pp. ISBN: 978-92-9066-544-1Google Scholar
  2. Ahuja I, De Vos RCH, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15(12):664–674CrossRefPubMedGoogle Scholar
  3. Aliasgharzad N, Barin M, Samadi A (2005) Effects of NaCl–induced and mixture salinities on leaf proline and growth of tomato in symbiosis with arbuscular mycorrhizal fungi. In: Proceeding of the international conference on environmental management, Hyderabad, India. pp 203–207Google Scholar
  4. Aliasgharzad N, Neyshabouri M, Salimi G (2006) Effects of arbuscular mycorrhizal fungi and Bradyrhizobium japonicum on drought stress of soybean. Biologia (Bratisl) 61:324–328.  https://doi.org/10.2478/s11756-006-0182-x CrossRefGoogle Scholar
  5. Alves BJR, Boddey RM, Urquiaga S (2003) The success of BNF in soybean in Brazil. Plant Soil 252:1–9CrossRefGoogle Scholar
  6. Anonymous (2014–2015) Director’s report and summary tables of experiments 2014–15, all India Coordinated Research Project on Soybean, ICAR–Directorate of Soybean Research, Indore India. p 329Google Scholar
  7. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefPubMedGoogle Scholar
  8. Appunu C, N’Zoue A, Laguerre G (2008) Genetic diversity of native bradyrhizobia isolated from soybeans (Glycine max L.) in different agricultural–ecological–climatic regions of India. Appl Environ Microbiol 74:5991–5996CrossRefPubMedPubMedCentralGoogle Scholar
  9. Augé RM, Kubikova E, Moore JL (2001a) Foliar dehydration tolerance of mycorrhizal cowpea, soybean and bush bean. New Phytol 151:535–541CrossRefGoogle Scholar
  10. Augé RM, Stodola AJW, Tims JE, Saxton AM (2001b) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97CrossRefGoogle Scholar
  11. Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570CrossRefGoogle Scholar
  12. Babalola OA, Atayese MO, Soyoye T (2009) Influence of Bradyrhizobium and two Glomus species on the growth and yield of soybean. J Agric Environ Sci 9:79–95Google Scholar
  13. Bagheri A, Sadeghipour O (2012) Biochemical changes of common bean (Phaseolus vulgaris L.) to pretreatment with salicylic acid (SA) under water stress conditions. Int J Biosci 2:14–22Google Scholar
  14. Bagyaraj DJ, Manjunath A, Patil RB (1979) Interactions between a VAM and Rhizobium and their effects on soybean in the field. New Phytol 82:141–145CrossRefGoogle Scholar
  15. Ballesteros-Almanza L, Altamirano-Hernandez J, Peña-Cabriales JJ, Santoyo G, Sanchez-Yañez JM, Valencia-Cantero E, Macias-Rodriguez L, Lopez-Bucio J, Cardenas-Navarro R, Farias-Rodriguez R (2010) Effect of co–inoculation with mycorrhiza and rhizobia on the nodule trehalose content of different bean genotypes. Open Microbiol J 4:83–92PubMedPubMedCentralGoogle Scholar
  16. Bartels S, Besteiro MAG, Lang D, Ulm R (2010) Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci 15(6):322–329CrossRefPubMedGoogle Scholar
  17. Bethlenfalvay G, Yoder J (1981) The Glycine–Glomus–Rhizobium symbiosis. Physiol Plant 52:141–145CrossRefGoogle Scholar
  18. Bethlenfalvay G, Pacovsky R, Bayne H, Stafford A (1982) Interactions between nitrogen fixation, mycorrhizal colonization, and host–plant growth in the Phaseolus–Rhizobium–Glomus symbiosis. Plant Physiol 70:446–450CrossRefPubMedPubMedCentralGoogle Scholar
  19. Bethlenfalvay GJ, Brown MS, Stafford AE (1985) Glycine–Glomus–Rhizobium symbiosis. 11. Antagonistic effects between mycorrhizal colonization and nodulation. Plant Physiol 79:1054–1058CrossRefPubMedPubMedCentralGoogle Scholar
  20. Betiana C, Grümberg, Urcelay C, María A, Shroeder, Vargas-Gil S, Luna CM (2015) The role of inoculum identity in drought stress mitigation by arbuscular mycorrhizal fungi in soybean. Biol Fertil Soils 51:1–10CrossRefGoogle Scholar
  21. Boudsocq M, Lauriere C (2005) Osmotic signaling in plants. Multiple pathways mediated by emerging kinase families. Plant Physiol 138(3):1185–1194CrossRefPubMedPubMedCentralGoogle Scholar
  22. Brechenmacher L, Lei Z, Libault M, Findley S, Sugawara M, Sadowsky MJ, Sumner LW, Stacey G (2010) Soybean metabolites regulated in root hairs in response to the symbiotic bacterium Bradyrhizobium japonicum. Plant Physiol 153:1808–1822CrossRefPubMedPubMedCentralGoogle Scholar
  23. Bressano M, Curetti M, Giachero L, Vargas GS, Cabello M, March G, Ducasse DA, Luna CM (2010) Mycorrhizal fungi symbiosis as a strategy against oxidative stress in soybean plants. J Plant Physiol 167:1622–1626CrossRefPubMedGoogle Scholar
  24. Catroux G, Hartmann A, Revellin C (2001) Trends in rhizobial inoculant production and use. Plant Soil 230:21–30CrossRefGoogle Scholar
  25. Chi F, Shen S, Cheng H, Jing Y, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278CrossRefPubMedPubMedCentralGoogle Scholar
  26. Clement M, Boncompagni E, Almeida-Engler JD, Herouart D (2006) Isolation of a novel nodulin: a molecular marker of osmotic stress in Glycine max Bradyrhizobium japonicum nodule. Plant Cell Environ 29:1841–1852CrossRefPubMedGoogle Scholar
  27. Daryanto S, Wang L, Jacinthe PA (2015) Global synthesis of drought effects on food legume production. PLoS One 10(6):1–16CrossRefGoogle Scholar
  28. Das A, Eldakak M, Paudel B, Kim DW, Hemmati H, Basu C, Rohila SJ (2016) Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean. Biol Med Res Int 6021047:1–23Google Scholar
  29. Delaux CB, Marburger D, Delaux PM, Conley S, Ané JM (2014) Effect of drought on Bradyrhizobium japonicum populations in Midwest soils. Plant Soil 382:165–173CrossRefGoogle Scholar
  30. Desbrosses GJ, Stougaard J (2011) Root nodulation: a paradigm for how plant–microbe symbiosis influences host development al path–ways. Cell Host Microbe 10:348–358CrossRefPubMedGoogle Scholar
  31. Ding X, Sui X, Wang F, Gao J, He X, Zhang F, Yang J, Feng G (2012) Synergistic interactions between Glomus mosseae and Bradyrhizobium japonicum in enhancing proton release from nodules and hyphae. Mycorrhiza 22:51–58.  https://doi.org/10.1007/s00572-011-0381-3 CrossRefPubMedGoogle Scholar
  32. Driver JD, Holben W, Rillig MC (2005) Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol Biochem 37:101–106CrossRefGoogle Scholar
  33. Elkan GH, Bunn CR (1992) The rhizobia. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes. A handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, 2nd edn. Springer–Verlag, New York, pp 2197–2213Google Scholar
  34. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263CrossRefPubMedPubMedCentralGoogle Scholar
  35. Farooq M, Wahid MA, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212CrossRefGoogle Scholar
  36. Friedman M, Brandon DL (2001) Nutritional and health benefits of soy proteins. J Agric Food Chem 49:1069–1086CrossRefPubMedGoogle Scholar
  37. Gadkar V, Rillig MC (2006) The arbuscular mycorrhizal fungal protein glomalin is a putative homolog of heat shock protein 60. FEMS Microbiol Lett 263:93–101.  https://doi.org/10.1111/j.1574–6968.2006.00412.x CrossRefPubMedGoogle Scholar
  38. Garay AF, Wilhelm W (1983) Root system characteristics of two soybean isolines undergoing water stress condition. Agron J 75:973–977CrossRefGoogle Scholar
  39. Global Soybean Production: The Global Soybean production (2017) http://www.globalsoybeanproduction.com. Accessed 19 Jan 2017
  40. Gonzalez EM, Gordan AJ, James CL, Igor CA (1995) The role of sucrose synthase in the response of soybean nodule to drought. J Exp Bot 46:1515–1524CrossRefGoogle Scholar
  41. Gonzalez EM, Aparicio-Tejo PM, Gordon AJ, Minchin FR, Royuela M, Igor CA (1998) Water–deficit effect on carbon and nitrogen metabolism of pea nodule. J Exp Bot 49:1705–1714CrossRefGoogle Scholar
  42. Harris D, Pacovsky RS, Paul EA (1985) Carbon economy of soybean– Rhizobium–Glomus associations. New Phytol 101:427440CrossRefGoogle Scholar
  43. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta–analysis of context dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407CrossRefPubMedGoogle Scholar
  44. Hungria M, Campo RJ, Mendes IC, Graham PH (2006) Contribution of biological nitrogen fixation to the N nutrition of grain crops in the tropics: the success of soybean (Glycine max L. Merr.) in South America. In: Singh RP, Shankar N, Jaiwa PK (eds) Nitrogen nutrition and sustainable plant productivity. Studium Press, Houston, pp 43–93Google Scholar
  45. Ivanov S, Fedorova EE, Limpens E, De Mita S, Genre A, Bonfante P, Bisseling T (2012) Rhizobium–legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc Natl Acad Sci 109:8316–8321.  https://doi.org/10.1073/pnas.1200407109 CrossRefPubMedGoogle Scholar
  46. Jordan DC (1982) Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow–growing, root nodule bacteria from leguminous plants. Int J Syst Bacteriol 32:136–139CrossRefGoogle Scholar
  47. Keyser HH, Bohlool BB, Hu TS, Weber DF (1982) Fast-growing rhizobia isolated from root nodules of soybean. Science 215:1631–1632CrossRefPubMedGoogle Scholar
  48. King CA, Purcell LC (2001) Soybean nodule size and relationship to nitrogen fixation response to water deficit. Crop Sci 41:1099–1107CrossRefGoogle Scholar
  49. Kloepper JW, Schroth MN (1981) Plant growth promoting rhizobacteria and plant growth under gnotobiotic condition. Phytopathology 71:642–644CrossRefGoogle Scholar
  50. Kloepper JW, Rodriguez-Kabana R, Zehnder GW, Murphy J, Sikora, Fernandez C (1999) Plant root–bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Australas Plant Pathol 28:27–33CrossRefGoogle Scholar
  51. Kramer PJ, Boyer JS (1995) Water relations of plant and soils. Academic, New YorkGoogle Scholar
  52. Kunert KJ, Vorster BJ, Fenta BA, Kibido T, Dionisio G, Foyer CH (2016) Drought stress responses in soybean roots and nodules published. Front Plant Sci 7(1015):1–7Google Scholar
  53. Kuykendall LD, Saxena B, Cevine TE, Udell SE (1992) Genetic diversity in Bradyrhizobium. Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can J Microbiol 38:201–505CrossRefGoogle Scholar
  54. Lauter FR, Ninnemann O, Bucher M, Riesmeier JW, Frommer WB (1996) Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. Proc Natl Acad Sci U S A 93(15):8139–8144CrossRefPubMedPubMedCentralGoogle Scholar
  55. Lee S, Hirt H, Lee Y (2001) Phosphatidic acid activates a wound-activated MAPK in Glycine max. Plant J 26(5):479–486CrossRefPubMedGoogle Scholar
  56. Lovelock CE, Andersen K, Morton JB (2003) Arbuscular mycorrhizal communities in tropical forests are affected by host tree species and environment. Oecologia 135:268–279CrossRefPubMedGoogle Scholar
  57. Lovelock CE, Wright SF, Clark DA, Ruess RW (2004) Soil stocks of glomalin produced by arbuscular mycorrhizal fungi across a tropical rain forest landscape. J Ecol 92:278–287CrossRefGoogle Scholar
  58. Ludlow MM (1989) Strategies in response to water stress. In: Kreeb HK, Richter H, Hinkley TM (eds) Structural and functional response to environmental stresses, water shortage. SPB Academic Press, Netherlands, pp 269–281Google Scholar
  59. Manavalan LP, Guttikonda SK, Tran LSP, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50(7):1260–1276CrossRefPubMedGoogle Scholar
  60. Marulanda A, Barea JM, Azcon R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AMF and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124CrossRefGoogle Scholar
  61. McIntyre HJ, Davies H, Hore HA, Miller SH, Dufour JP, Ronson CW (2007) Trehalose biosynthesis in rhizobium leguminosarum bv. trifolii and its role in desiccation tolerance. Appl Environ Microbiol 73(12):3984–3992CrossRefPubMedPubMedCentralGoogle Scholar
  62. Meghvansi MK, Mahna SK (2009) Evaluating the symbiotic potential of Glomus intraradices and Bradyrhizobium japonicum in vertisol with two soybean cultivars. Am Eurasian J Agron 2:21–25Google Scholar
  63. Meghvansi MK, Prasad K, Harwani D, Mahna SK (2008) Response of soybean cultivars toward inoculation with three arbuscular mycorrhizal fungi and Bradyrhizobium japonicum in the alluvial soil. Eur J Soil Biol 44:316–323CrossRefGoogle Scholar
  64. Morey KJ, Ortega JL, Gopalan SC (2002) Cytosolic glutamine synthetase in soybean is encoded by a multi gene family, and the members are regulated in an organ–specific and developmental manner. Plant Physiol 128:182–193CrossRefPubMedPubMedCentralGoogle Scholar
  65. Ortiz N, Armada E, Duque E, Roldan A, Azcona R (2015) Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. J Plant Physiol 174:87–96CrossRefPubMedGoogle Scholar
  66. Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750.  https://doi.org/10.1093/jxb/erh188 CrossRefPubMedGoogle Scholar
  67. Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143.  https://doi.org/10.1046/j.1469-8137.2003.00658.x CrossRefGoogle Scholar
  68. Purcell L, Serraj R, Sinclair T, De A (2004) Soybean N2 fixation estimates, ureide concentration, and yield responses to drought. Crop Sci 44:484–492CrossRefGoogle Scholar
  69. Rahmani H, Saleh-Rastin N, Khavazi K, Asgharzadeh A, Fewer D, Kiani S, Lindstrom K (2009) Selection of thermo tolerant Bradyrhizobial strains for nodulation of soybean (Glycine max L.) in semi–arid regions of Iran. World J Microbiol Biotechnol 25:591–600CrossRefGoogle Scholar
  70. Ramos MLG, Parsons R, Sprent JI (2005) Differences in ureide and amino acid content of water stressed soybean inoculated with Bradyrhizobium japonicum and B. elkanii. Pesq Agrop Brasileira 40:453–458CrossRefGoogle Scholar
  71. Reibach P, Streeter J (1983) Metabolism of 14C–labeled photosynthate and distribution of enzyme of glucose metabolism in soybean nodules. Plant Physiol 72:634–640CrossRefPubMedPubMedCentralGoogle Scholar
  72. Rillig MC, Steinberg PD (2002) Glomalin production by an arbuscular mycorrhizal fungus: a mechanism of habitat modification. Soil Biol Biochem 34:371–1374.  https://doi.org/10.1016/S0038-0717(02)00060-3 CrossRefGoogle Scholar
  73. Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151CrossRefPubMedPubMedCentralGoogle Scholar
  74. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317CrossRefPubMedPubMedCentralGoogle Scholar
  75. Ruiz-Lozano JM, Azcón R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plant 95:472–478CrossRefGoogle Scholar
  76. Ruiz-Lozano JM, Azcón R, Palma JM (1996) Superoxide dismutase activity in arbuscular mycorrhizal Lactuca sativa plants subjected to drought stress. New Phytol 134:327–333CrossRefGoogle Scholar
  77. Ruiz-Lozano JM, Collados C, Barea JM, Azcn R (2001) Arbuscular mycorrhizal symbiosis can alleviate drought induced nodule senescence in soybean plants. New Phytol 151:493–502CrossRefGoogle Scholar
  78. Saeki Y, Aimi N, Tsukamoto S, Yamakawa T, Nagatomo Y, Akao S (2006) Diversity and geographical distribution of indigenous soybean–nodulating bradyrhizobia in Japan. Soil Sci Plant Nutr 52:418–426CrossRefGoogle Scholar
  79. Safir GR, Boyer JS, Gerdemann JW (1972) Nutrient status and mycorrhizal enhancement of water transport in soybean. Plant Physiol 49:700–703CrossRefPubMedPubMedCentralGoogle Scholar
  80. Sahgal M, Johri BN (2003) The changing face of rhizobial systematics. Curr Sci 84:43–48Google Scholar
  81. Sanchez FJ, Manzanares M, de Andres EF, Tenorio JL, Ayerbe L (1998) Turgor maintenance, osmotic adjustment and soluble sugar and proline accumulation in 49 pea cultivars in response to water stress. Field Crop Res 59:225–235CrossRefGoogle Scholar
  82. Sandhya V, Ali SZ, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress effects in sunflower seedlings by exopolysaccharides producing Pseudomonas putida strain P45. Biol Fertil Soils 46:17–26CrossRefGoogle Scholar
  83. Serraj R, Sinclair TR, Purcell L (1999) Symbiotic N2 fixation response to drought. J Exp Bot 50:143–155Google Scholar
  84. Sharma MP, Srivastava K, Sharma SK (2010) Biochemical characterization and metabolic diversity of soybean rhizobia isolated from Malwa region of central India. Plant Soil Environ 56:375–383CrossRefGoogle Scholar
  85. Sharp RE, Silk WK, Hsiao TC (1988) Growth of the maize primary root at low water potentials. I. Spatial distribution of expansive growth. Plant Physiol 87:50–57CrossRefPubMedPubMedCentralGoogle Scholar
  86. Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351CrossRefPubMedGoogle Scholar
  87. Smith SE, Read DJ (2008) Mineral nutrition, toxic element accumulation and water relations of arbuscular mycorrhizal plants. In: Smith SE, Read DJ (eds) Mycorrhizal symbiosis, 3rd edn. Academic, London, pp 145–118CrossRefGoogle Scholar
  88. Spaink HR (1994) The molecular basis of the host specificity of the Rhizobium bacteria. Antonie Van Leeuwenhoek 65:81–98CrossRefPubMedGoogle Scholar
  89. Sprent JI (1971) The effect of water stress on nitrogen–fixing root nodules. I. Effects on the physiology of detached soybean nodules. New Phytol 70:9–16CrossRefGoogle Scholar
  90. Streeter JG (2003) Effects of drought on nitrogen fixation in soybean root nodules. Plant Cell Environ 26:1199–1204CrossRefGoogle Scholar
  91. Streeter JG, Gomez ML (2006) Three enzymes for trehalose synthesis in Bradyrhizobium cultured bacteria and in bacteroids from soybean nodules. Appl Environ Microbiol 72(6):4250–4255CrossRefPubMedPubMedCentralGoogle Scholar
  92. Streeter JG, Salminen SO, Whitmoyer RE, Carlson RW (1992) Formation of novel polysaccharides by Bradyrhizobium japonicum bacteroids in soybean nodules. Appl Environ Microbiol 58:607–613PubMedPubMedCentralGoogle Scholar
  93. Tilak KVBR, Saxena AK, Sadasivam KV (1995) Synergistic effects of phosphate–solubilizing bacterium (Pseudomonas striata) and arbuscular mycorrhizae on soybean. In: Adholeya A, Singh S (eds) Mycorrhizae: biofertilizer for the future. Tata Energy Research Institute, New Delhi, pp 224–226Google Scholar
  94. Tisdall JM, Oades JM (1982) Organic matter and water–stable aggregates in soils. J Soil Sci 33:141–163.  https://doi.org/10.1111/j.1365-2389.1982.tb01755.x CrossRefGoogle Scholar
  95. Uma C, Sivagurunathan P, Sangeetha D (2013) Performance of Bradyrhizobial isolates under drought conditions. Int J Curr Microbiol App Sci 2(5):228–232Google Scholar
  96. Vaishnav A, Varma A, Tuteja N, Choudhary DK (2017) PGPR–mediated amelioration of crops under salt stress. In: Choudhary DK et al (eds) Plant–microbe interaction: an approach to sustainable agriculture. Springer Nature, Singapore, pp 205–226Google Scholar
  97. Valentine AJ, Benedito VA, Kang Y (2011) Legume nitrogen fixation and soil abiotic stress: from physiology to genomics and beyond. Ann Plant Rev 42:207–248Google Scholar
  98. Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3:547–560CrossRefPubMedPubMedCentralGoogle Scholar
  99. Vurukonda SSKP, Vardharajula S, Shrivastava M, Ali SKZ (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24CrossRefPubMedGoogle Scholar
  100. Wang X, Pan Q, Chen F, Yan X, Liao H (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181.  https://doi.org/10.1007/s00572-010-0319-1 CrossRefPubMedGoogle Scholar
  101. Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33(4):510–525CrossRefPubMedGoogle Scholar
  102. Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14CrossRefGoogle Scholar
  103. Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, Heide TV, Smith LT (2001) Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol Part A 130:437–460CrossRefGoogle Scholar
  104. Wright SF (2000) A fluorescent antibody assay for hyphae and glomalin from arbuscular mycorrhizal fungi. Plant Soil 226:171–177.  https://doi.org/10.1023/A:1026428300172 CrossRefGoogle Scholar
  105. Xie ZP, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton WJ, Vogeli-Lange R, Boller T (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol 108:1519–1525CrossRefPubMedPubMedCentralGoogle Scholar
  106. Xu ML, Ge C, Cui Z, Li J, Fan H (1995) Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 45:706–711CrossRefPubMedGoogle Scholar
  107. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4CrossRefGoogle Scholar
  108. Young JPW (1996) Phylogeny and taxonomy of rhizobia. Plant Soil 186:45–52CrossRefGoogle Scholar
  109. Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97(1):111–119CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Abhishek Bharti
    • 2
  • Richa Agnihotri
    • 2
  • Hemant S. Maheshwari
    • 2
  • Anil Prakash
    • 1
  • Mahaveer P. Sharma
    • 2
  1. 1.Department of Microbiology, Faculty of Life SciencesBarkatullah UniversityBhopalIndia
  2. 2.ICAR-Indian Institute of Soybean ResearchIndoreIndia

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