Legume-Rhizobia Symbiosis Under Stress

  • Kapudeep Karmakar
  • Anjul Rana
  • Asmita Rajwar
  • Manvika Sahgal
  • Bhavdish N. Johri


Legume-rhizobia symbioses are of practical importance in provision of sustained food supply. Currently, it provides approximately 45 % of N used in agriculture. This quantity will have to be augmented as the world’s population increases and natural resources used in production of fertilizer-N diminish. The major constraints for food security are soil salinity, sodicity, nutrient deficiency, and toxicity which are driven by indiscriminate use of agrochemicals including chemical fertilizers and pesticides, utilization of excess water resource coupled with climate changes, and periodic droughts. In this scenario, legume-rhizobia symbioses are nonpolluting, cost-effective ways to enhance high N2-fixing potential under stress conditions. Several symbiotic systems that are tolerant in extreme conditions of salinity, alkalinity, acidity, drought, toxic doses of fertilizer, and metal toxicity have been identified including rhizobial symbiosis in arid region. Extreme environmental conditions adversely affect rhizobia-legume interactions wherein rhizobial partner utilizes endogenous or exogenous osmolytes and secretes specific proteins to alleviate the problem of aridity, salinity, and toxicity. Thus, change in rhizobial population can be an indicator of soil fertility. Hence, osmoadapted rhizobial strains can be used as biofertilizers for salt-sensitive crops in saline soils. In this context, interaction among rhizobia, plant growth-promoting rhizobacteria (PGPR), and mycorrhiza are also important. Here, we give an account of relevance of biological nitrogen fixation (BNF) in sustained food supply, effects of extreme conditions on legume-rhizobia symbiosis, as well as interaction of rhizobia with belowground microbial diversity including mycorrhiza and adaptive strategies of rhizobia under condition of stress. We also discuss about models wherein osmotolerant rhizobia can be used as biofertilizers and sustain green revolution to evergreen revolution.


Salt Stress Drought Stress Arbuscular Mycorrhizal Fungus Compatible Solute Glycine Betaine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Our work on rhizobia has been supported through the Centre for Research on Bacteria and Archaea, under All India Coordinated Project on Taxonomy (AICOPTAX) of the Ministry of Environment and Forests, Govt. of India.


  1. Abberton MT (2010) Enhancing the role of legumes: potential and obstacles. In: Abberton MT, Conant R, Batello C (eds) Grassland carbon sequestration: management, policy and economics, vol 338. FAO, Rome, pp 177–187Google Scholar
  2. Ahemad M, Khan SM (2013) Pesticides as antagonists of rhizobia and the legume-Rhizobium symbiosis: a paradigmatic and mechanistic outlook. Biochem Mol Biol 1:63–75Google Scholar
  3. Anderson A, Baldock JA, Rogers SL, Bellotti W, Gill G (2004) Influence of chlorsulfuron on rhizobial growth, nodule formation, and nitrogen fixation with chickpea. Aust J Agric Res 55:1059–1070Google Scholar
  4. Aroca R, Ruiz-Lozano JM (2009) Induction of plant tolerance to semi-arid environments by beneficial soil microorganisms – a review. In: Lichtfouse E (ed) Climate change, intercropping, pest control and beneficial microorganisms, sustainable agriculture reviews. Springer, Dordrecht, pp 121–135Google Scholar
  5. Aswathappa N, Marcar NE, Thomson LAJ (1987) Salt tolerance of Australian tropical and subtropical acacias. In: Turnbull JW (ed) Australian acacias in developing countries: proceedings of an international workshop held at Forestry Training Centre, Gympie, Qld., Australia, 4–7 August 1986. Brown Prior Anderson, Burwood, Victoria 3125, pp 70–73Google Scholar
  6. Athar M, Johnson DA (1996) Influence of drought on competition between selected Rhizobium meliloti strains and naturalized soil rhizobia in alfalfa. Plant Soil 184:231–241Google Scholar
  7. Babber S, Sheokand S, Malik S (2000) Nodule structure and functioning in chickpea (Cicer arietinum) as affected by salt stress. Biol Plant 43:269–27Google Scholar
  8. Bahlawane C, McIntosh M, Krol E, Becker A (2008) Sinorhizobium meliloti regulator MucR couples exopolysaccharide synthesis and motility. Mol Plant Microbe Interact 21:1498–1509PubMedGoogle Scholar
  9. Baumgarth B, Bartels FW, Anselmetti D, Becker A, Ros R (2005) Detailed studies of the binding mechanism of the Sinorhizobium meliloti transcriptional activator ExpG to DNA. Microbiology 151:1–10Google Scholar
  10. Becker B, Kosch K, Parniske M, Müller P (1998) Exopolysaccharide synthesis in Bradyrhizobium japonicum: sequence, operon structure and mutational analysis of an exo gene cluster. Mol Gen Genet 259:161–171PubMedGoogle Scholar
  11. Ben Salah I, Albacete A, Martinez Andujar C, Haouala R, Labidi N, Zribi F, Martinez V, Perez-Alfocea F, Abdelly C (2009) Response of nitrogen fixation in relation to nodule carbohydrate metabolism in Medicago ciliaris lines subjected to salt stress. J Plant Physiol 166:477–488PubMedGoogle Scholar
  12. Bernard T, Pocard JA, Perroud B, Le Rudulier D (1986) Variations in the response of salt-stressed Rhizobium strains to betaines. Arch Microbiol 143:359–364Google Scholar
  13. Boivin C, Barran LR, Malpica CA, Rosenberg C (1991) Genetic analysis of a region of the Rhizobium meliloti pSym plasmid specifying catabolism of trigonelline, a secondary metabolite present in legumes. J Bacteriol 173:2809–2817PubMedPubMedCentralGoogle Scholar
  14. Boncompagni E, Osterås M, Poggi MC, Le Rudulier D (1999) Occurrence of choline and glycine betaine uptake and metabolism in the family rhizobiaceae and their roles in osmoprotection. Appl Environ Microbiol 65:2072–2077PubMedPubMedCentralGoogle Scholar
  15. Borch K, Bouma T, Lynch P, Brown KM (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22:425–431Google Scholar
  16. Breedveld MW, Zevenhuizen LPTM, Zehnder AJB (1990) Osmotically induced oligo- and polysaccharide synthesis by Rhizobium meliloti SU-47. J Gen Microbiol 136:2511–2519Google Scholar
  17. Breedveld MW, Zevenhuizen LPTM, Zehnder AJB (1991) Osmotically-regulated trehalose accumulation and cyclic beta-(1,2)-glucan excreted by Rhizobium leguminosarum bv. trifolii TA. Arch Microbiol 156:501–506Google Scholar
  18. Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180Google Scholar
  19. Broughton WJ, Jabbouri S, Perret X (2000) Keys to symbiotic harmony. J Bacteriol 182:5641–5652PubMedPubMedCentralGoogle Scholar
  20. Buchanan BB, Gruissem W, Jones RL (eds) (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, SanterreA, p 849.Google Scholar
  21. Canal MJ, Tames RS, Fernandez B (1987) Glyphosate increased levels of indole–3-acetic acid in yellow nutsedge leaves correlated with gentisic acid levels. Physiol Plant 71:384–388Google Scholar
  22. Chang C, Damiani I, Puppo A, Frendo P (2009) Redox change during the legume rhizobium symbiosis. Mol Plant 2:370–377PubMedGoogle Scholar
  23. Cheng HP, Walker GC (1998) Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. J Bacteriol 180:20–26PubMedPubMedCentralGoogle Scholar
  24. Clement M, Lambert A, Herouart D, Boncompagni E (2008) Identification of new up-regulated genes under drought stress in soybean nodules. Gene 426:15–22PubMedGoogle Scholar
  25. Dakora FD, Keya SO (1997) Contribution of legume nitrogen fixation to sustainable agriculture in Sub-Saharan Africa. Soil Biol Biochem 29:809–817Google Scholar
  26. Davies BW, Walker GC (2007) Identification of novel Sinorhizobium meliloti mutants compromised for oxidative stress protection and symbiosis. J Bacteriol 189:2110–2113PubMedPubMedCentralGoogle Scholar
  27. De la Gardia MD, Benlloch M (1980) Effects of potassium and gibberellic acid on stem growth of whole sunflower plants. Physiol Plant 49:443–448Google Scholar
  28. Deans JD, Diagne O, Lindley DK, Dione M, Parkinson JA (1999) Nutrient and organic-matter accumulation in Acacia senegal fallows over 18 years. For Ecol Manage 124:153–167Google Scholar
  29. Dixon RK, Garg VK, Rao MV (1993) Inoculation of Leucaena and Prosopis seedlings with Glomus and Rhizobium species in saline soil: rhizosphere relations and seedlings growth. Arid Soil Res Rehabil 7:133–144Google Scholar
  30. Djordjevic MA (2004) Sinorhizobium meliloti metabolism in the root nodule: a proteomic perspective. Proteomics 4:1859–1872PubMedGoogle Scholar
  31. Downie JA, Walker SA (1999) Plant responses to nodulation factors. Curr Opin Plant Biol 2:483–489PubMedGoogle Scholar
  32. Drevon JJ, Frangne N, Fleurat-Lessard PH, Ribet J, Vadez V, Serraj R (1998) Is nitrogenase-linked respiration regulated by osmocontractile cells in legume nodules? In: Elmerich C, Kondorosi A, Newton WE (eds) Biological nitrogen fixation for the 21st century. Kluwer Academic, Dordrecht, pp 465–466Google Scholar
  33. Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189Google Scholar
  34. El-Hamdaoui A, Redondo-Nieto M, Rivilla R, Bonilla I, Bolanos L (2003) Effects of boron and calcium nutrition on the establishment of the Rhizobium leguminosarum–pea (Pisum sativum) symbiosis and nodule development under salt stress. Plant Cell Environ 26:1003–1012Google Scholar
  35. Elsheikh EAE (1992) Effect of salinity on growth, nodulation and nitrogen yield of inoculated and nitrogen fertilized chickpea (Cicer arietinum L.). Arch Biotechnol 1:17–28Google Scholar
  36. Elsheikh EAE, Wood M (1990) Effect of salinity on growth, nodulation and nitrogen yield of chickpea (Cicer arietinum L.). J Exp Bot 41:1263–1269Google Scholar
  37. Elsheikh EAE, Wood M (1995) Nodulation and N2 fixation by soybean inoculated with salt-tolerant rhizobia or salt-sensitive Bradyrhizobia in saline soil. Soil Biol Biochem 27:657–661Google Scholar
  38. Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Associates, Sunderland, pp 1–400Google Scholar
  39. Estibaliz L, Stefanie W, Wolfram W, Ruben L, Cesar A, Esther MG (2007) Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress. Plant Physiol 144:1495–1507Google Scholar
  40. Fagg CW, Stewart JL (1994) The value of Acacia and Prosopis in arid and semi-arid environments. J Arid Environ 27:3–25Google Scholar
  41. Fedtke C (1982) Biochemistry and physiology of herbicide action. Springer, Berlin, pp 1–193Google Scholar
  42. Felker P, Clark PR, Laag AE, Pratt PF (1981) Salinity tolerance of the tree legumes: mesquite (Prosopis glandulosa var. Torreyana, P. velutina and P. articulata), algarrobo (P. chilensis), kiawe (P. pallida) and tamarugo (P. tamarugo) grown in sand culture on nitrogen-free media. Plant Soil 61:311–317Google Scholar
  43. Feng ZH, Wang TG, Li DD, Fung P, Wilson BC, Liu B, Ali SF, Langenbach R, Hong JS (2002) Cyclooxygenase-2-deficient mice are resistant to 1-methyl-4-phenyl-1-2,3,6-tetrahydropyridine induced damage of dopaminergic neurons in the substantia nigra. Neurosci Lett 329:354–358PubMedGoogle Scholar
  44. Fox JE, Gulledge J, Engelhaupt E, Burow ME, McLachlan JA (2007) Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proc Natl Acad Sci U S A 104:10282–10287PubMedPubMedCentralGoogle Scholar
  45. Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur J Biochem 270:1365–1380PubMedGoogle Scholar
  46. Galinski EA (1995) Osmoadaptation in bacteria. Adv Microb Physiol 37:273–328Google Scholar
  47. Galvez L, Gonzalez EM, Arrese-Igor C (2005) Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J Exp Bot 56:2551–2561PubMedGoogle Scholar
  48. Giri B, Mukerji KG (2004) Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312PubMedGoogle Scholar
  49. Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175Google Scholar
  50. Glick BR (2004) Changes in plant growth and development by rhizosphere bacteria that modify plant ethylene levels. Acta Hortic 631:265–273Google Scholar
  51. Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339Google Scholar
  52. Gonzalez JE, Semino CE, Wang LX, Castellano-Torres LE, Walker GC (1998) Biosynthetic control of molecular weight in the polymerization of the octasaccharide subunits of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Proc Natl Acad Sci U S A 95:13477–13482PubMedPubMedCentralGoogle Scholar
  53. Gonzalez EM, Galvez L, Arrese-Igor C (2001) Abscisic acid induces a decline in nitrogen fixation that involves leghaemoglobin, but is independent of sucrose synthase activity. J Exp Bot 52:285–293PubMedGoogle Scholar
  54. Gordon AJ, Minchin FR, Skot L, James CL (1997) Stress-induced declines in soybean N2 fixation are related to nodule sucrose synthase activity. Plant Physiol 114:937–946PubMedPubMedCentralGoogle Scholar
  55. Gouffi K, Bernard T, Blanco C (2000) Osmoprotection by pipecolic acid in Sinorhizobium meliloti: specific effects of D and L isomers. Appl Environ Microbiol 66:2358–2364PubMedPubMedCentralGoogle Scholar
  56. Grattan SR, Grieve CM (1999) Salinity mineral nutrient relations in horticultural crops. Sci Hortic (Amst) 78:127–157Google Scholar
  57. Greiger DR, Bestman HD (1990) Self limitation of herbicide mobility by phytotoxic action. Weed Sci 38:324–329Google Scholar
  58. Gyaneshwar P, Naresh KG, Parekh LJ (2002) Effect of buffering on the phosphate solubilizing ability of microorganisms. World J Microbiol Biotechnol 14:669–673Google Scholar
  59. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedGoogle Scholar
  60. Henderson JC, Davies FT (1990) Drought acclimation and the morphology of mycorrhizal Rosa hybrida L. cv. “Frey” is independent of leaf elemental content. New Phytol 115:503–510Google Scholar
  61. Hocking DE (1993) Trees for drylands. International Science Publisher, New York, pp 1–370Google Scholar
  62. Howieson JG, Loi A, Carr SJ (1995) Biserrula pelecinus L.- a legume pasture species with potential for acid, duplex soils which is nodulated by unique root-nodule bacteria. Aust J Agric Res 46:997–1009Google Scholar
  63. Hua S, Tsai VY, Lichens GM, Noma AT (1982) Accumulation of amino acids in Rhizobium sp. strain WRlOOl in response to NaCl salinity. Appl Environ Microbiol 44:135–140PubMedPubMedCentralGoogle Scholar
  64. Ishikura N, Teramoto S, Takeshima Y, Mitsui S (1986) Effects of glyphosate on the shikimate pathway and regulation of phenylalanine ammonia-lyase in Cryptomeria and Perilla cell suspension cultures. Plant Cell Physiol 27:677–684Google Scholar
  65. Jebara S, Drevon JJ, Jebara M (2010) Modulation of symbiotic efficiency and nodular antioxidant enzyme activities in two Phaseolus vulgaris genotypes under salinity. Acta Physiol Plant 32:925–932Google Scholar
  66. Jenkins MB, Virginia RA, Jarrel WM (1987) Rhizobial ecology of the woody legume mesquite Prosopis glandulosa in the Sonoran desert. Appl Environ Microbiol 53:36–40PubMedPubMedCentralGoogle Scholar
  67. Kadiata BD, Mulongoy K, Isirimah NO (1996) Time course of biological nitrogen fixation, nitrogen absorption and biomass accumulation in three woody legumes. Biol Agric Hortic 13:253–266Google Scholar
  68. King CA, Prucell LC (2005) Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol 137:1389–1396PubMedPubMedCentralGoogle Scholar
  69. Kitchen LM, Witt WW, Rieck LE (1981a) Inhibition of aminolevulinic acid synthesis by glyphosate. Weed Sci 29:571–577Google Scholar
  70. Kitchen LM, Witt WW, Rieck LE (1981b) Inhibition of chlorophyll accumulation by glyphosate. Weed Sci 29:513–516Google Scholar
  71. Kozlowski TT, Pallardy SG (1997) Physiology of woody plants. Academic, San Diego, pp 1–411Google Scholar
  72. Laanset L (1987) Incorporation of exogenous tyrosine and phenylalanine into c-glycosylflavones in glyphosate treated barley seedlings. Eesti NSV Tead Akad Toim Biol 36:204–209Google Scholar
  73. Lauter DJ, Munns DN, Clarkin KL (1981) Salt response of chickpeas influenced by N supply. Agric J 73:961–966Google Scholar
  74. Le Rudulier D, Bernard T, Goas G (1984) Osmoregulation in Klebsiella pneumoniae: enhancement of anaerobic growth and nitrogen fixation under stress by proline betaine, γ-butyrobetaine, and other related compounds. Can J Microbiol 30:299–305PubMedGoogle Scholar
  75. Lee T (1984) Release of lateral buds from apical dominance by glyphosate in soybean and pea seedlings. J Plant Growth Regul 3:227–235Google Scholar
  76. Lehman AP, Long SR (2013) Exopolysaccharides from Sinorhizobium meliloti can protect against H2O2-dependent damage. J Bacteriol 195:5362–5369Google Scholar
  77. Lloret J, Wulff BB, Rubio JM, Downie JA, Bonilla I, Rivilla R (1998) Exopolysaccharide II production is regulated by salt in the halotolerant strain Rhizobium meliloti EFB1. Appl Environ Microbiol 64:1024–1028PubMedPubMedCentralGoogle Scholar
  78. Lodwig EM, Hosie AHF, Bordes A, Findley K, Allaway D, Karunakaran R, Downie JA, Poole PS (2003) Amino acid cycling drives nitrogen fixation in legume rhizobia symbiosis. Nature 422:722–726PubMedGoogle Scholar
  79. Lu YL, Chen WF, Wang ET, Guan SH, Yan XR, Chen WX (2009) Genetic diversity and biogeography of rhizobia associated with Caragana species in three ecological regions of China. Syst Appl Microbiol 32:351–361PubMedGoogle Scholar
  80. Lynch J, Brown KM (1997) Ethylene and plant responses to nutritional stress. Physiol Plant 100:613–619Google Scholar
  81. Madhaiyan M, Poonguzhali SST (2007) Characterization of 1-Aminocyclopropane-1-carboxylate (ACC) deaminase containing Methylobacterium oryzae and interactions with auxins and ACC regulation of ethylene in canola (Brassica campestris). Planta 226:867–876PubMedGoogle Scholar
  82. Malik MAB, Tesfai K (1985) Pesticidal effect on soybean rhizobia symbiosis. Plant Soil 85:33–41Google Scholar
  83. Marino D, Frendo P, Ladrera R, Zabalza A, Puppo A, Arrese-Igor C, Gonzalez EM (2007) Nitrogen fixation control under drought stress. Localized or systemic? Plant Physiol 143:1968–1974PubMedPubMedCentralGoogle Scholar
  84. Marino D, Hohnjec N, Kuster H, Moran JF, Gonzalez EM, Arrese-Igor C (2008) Evidence for transcriptional and post translational regulation of sucrose synthase in pea nodule by cellular redox state. Mol Plant Microbe Interact 21:622–630PubMedGoogle Scholar
  85. Mashhady AS, Salem SH, Barakh FN, Heggo AM (1998) Effect of salinity on survival and symbiotic performance between Rhizobium meliloti and Medicago sativa in Saudi Arabian soils. Arid Soil Res Rehabil 12:3–14Google Scholar
  86. Masutha TH, Muofhe ML, Dokora FD (1997) Evaluation of N2 fixation and agroforestry potential in selected tree legumes for sustainable use in South Africa. Soil Biol Biochem 29:993–998Google Scholar
  87. McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiol 120:945–949PubMedPubMedCentralGoogle Scholar
  88. Mendrygal KE, Gonzalez JE (2000) Environmental regulation of exopolysaccharide production in Sinorhizobium meliloti. J Bacteriol 182:599–606PubMedPubMedCentralGoogle Scholar
  89. Michelsen A, Rosendahl S (1990) The effect of VA mycorrhizal fungi, phosphorus and drought stress on the growth of Acacia nilotica and Leucaena leucocephala seedling. Plant Soil 124:7–13Google Scholar
  90. Miller KJ, Wood JM (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50:101–136PubMedGoogle Scholar
  91. Mohammad RM, Akhavan-Kharazian M, Campbell WF, Rumbaugh MD (1991) Identification of salt-and drought-tolerant Rhizobium meliloti L. strains. Plant Soil 134:271–276Google Scholar
  92. Mulligan JT, Long SR (1989) A family of activator genes regulates expression of Rhizobium meliloti nodulation genes. Genetics 122:7–18PubMedPubMedCentralGoogle Scholar
  93. Munns R, Termaat A (1986) Whole-plant responses to salinity. Aust J Plant Physiol 13:143–160Google Scholar
  94. Murphy PJ, Wexler W, Grzemski W, Rao JP, Gordon D (1995) Rhizopines – their role in symbiosis and competition. Soil Biol Biochem 27:525–529Google Scholar
  95. Neo HH, Hunt S, Layzell DB (1996) Can genotypes of soybean (Glycine max) selected for nitrate tolerance provide good ‘models’ for studying the mechanism of nitrate inhibition of nitrogenase activity? Physiol Plant 98:653–660Google Scholar
  96. Niebel A, Gressent F, Bono JJ, Ranjeva R, Cullimore J (1999) Recent advances in the study of Nod factor perception and signal transduction. Biochimie 81:669–674PubMedGoogle Scholar
  97. Nour SM, Fernandez MP, Normand P, Cleyet-Maret JC (1994) Rhizobium ciceri sp. nov. consisting of strains that nodulate chickpea (Cicer arietinum L). Int J Syst Bacteriol 44:511–522PubMedGoogle Scholar
  98. Pandey S, Singh DK (2004) Total bacterial and fungal population after chlorpyrifos and quinalphos treatments in groundnut (Arachis hypogaea L.) soils. Chemosphere 55:197–205PubMedGoogle Scholar
  99. Peoples MB, Gault RR, Scammell GJ, Dear BS, Vigona J, Sandral GA, Paul J, Wolf EC, Angus JF (1998) Effect of pasture management on the contributions of fixed N to the N economy of ley-farming systems. Aust J Agric Res 49:459–474Google Scholar
  100. Pichereau V, Pocard JA, Hamelin J, Blanco C, Bernard T (1998) Differential effects of dimethylsulfoniopropionate, dimethylsulfonioacetate, and other S-methylated compounds on the growth of Sinorhizobium meliloti at low and high osmolarities. Appl Environ Microbiol 64:1420–1429PubMedPubMedCentralGoogle Scholar
  101. Pinedo CA, Gage DJ (2009) HPrK regulates succinate-mediated catabolite repression in the gram-negative symbiont Sinorhizobium meliloti. J Bacteriol 191:298–309PubMedPubMedCentralGoogle Scholar
  102. Pinedo CA, Bringhurst RM, Gage DJ (2008) Sinorhizobium meliloti mutants lacking phosphotransferase system enzyme HPr or EIIA are altered in diverse processes, including carbon metabolism, cobalt requirements and succinoglycan production. J Bacteriol 190:2947–2956PubMedPubMedCentralGoogle Scholar
  103. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805PubMedPubMedCentralGoogle Scholar
  104. Prell J, Poole P (2006) Metabolic changes of rhizobia in legume nodules. Trends Microbiol 14:161–168PubMedGoogle Scholar
  105. Rai R, Prasad V (1983) Salinity tolerance of Rhizobium mutants: growth and relative efficiency of symbiotic nitrogen fixation. Soil Biol Biochem 15:217–219Google Scholar
  106. Rajwar A, Sahgal M, Johri BN (2013) Legume-rhizobia symbiosis and interactions in agroecosystems. In: Arora NK (ed) Plant microbe symbiosis-fundamentals and advances. Springer, India, pp 233–265Google Scholar
  107. Rao DLN, Sharma PC (1995) Effectiveness of rhizobial strains for chickpea (Cicer arietinum L.) under salinity stress and recovery of nodulation on desalinization. Indian J Exp Biol 33:500–504Google Scholar
  108. Rasanen LA, Lindstrom K (2003) Effects of biotic and abiotic constraints on the symbiosis between rhizobia and the tropical leguminous trees Acacia and Prosopis. Indian J Exp Biol 41:1142–1159PubMedGoogle Scholar
  109. Rhoades CC, Coleman DC (1999) Nitrogen mineralization and nitrification following land conversion in montane Ecuador. Soil Biol Biochem 31:1347–1354Google Scholar
  110. Rinaudo M (2004) Role of substituents on the properties of some polysaccharides. Biomacromolecules 5:1155–1165PubMedGoogle Scholar
  111. 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 41:2568–2572Google Scholar
  112. Roshetko JM (2001) Agroforestry species and technologies: a compilation of the highlights and factsheets published by NFTA and FACT Net 1895–1999. A Publication of Winrock International, Morrilton, pp 1–232Google Scholar
  113. Ruberg S, Tian ZX, Krol E, Linke B, Meyer F, Wang YP, Puhler A, Weidner S, Becker A (2003) Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptive gene expression. J Biotechnol 106:255–268PubMedGoogle Scholar
  114. Sagot B, Gaysinski M, Mehiri M, Guigonis JM, Le Rudulier D, Alloing G (2010) Osmotically induced synthesis of the dipeptide N-acetylglutaminylglutamine amide is mediated by a new pathway conserved among bacteria. Proc Natl Acad Sci U S A 107:12652–12657PubMedPubMedCentralGoogle Scholar
  115. Sanchez DH, Pieckenstain FL, Escaray F, Erban A, Kraemer U, Udvardi MK, Kopka J (2011) Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt stress challenge the metabolic pre-adaptation hypothesis. Plant Cell Environ 34:605–617PubMedGoogle Scholar
  116. Schmeisser C, Liesegang H, Krysciak D, Bakkou N, Le Quéré A, Wollherr A, Heinemeyer I, Morgenstern B, Pommerening-Röser A, Flores M (2009) Rhizobium sp. Strain NGR234 possesses a remarkable number of secretion systems. Appl Environ Microbiol 75:4035–4045PubMedPubMedCentralGoogle Scholar
  117. Seghers D, Verthe K, Reheul D, Bulcke R, Siciliano SD, Verstraete W, Top EM (2003) Effect of long-term herbicide applications on the bacterial community structure and function in an agricultural soil. FEMS Microbiol Ecol 46:139–146PubMedGoogle Scholar
  118. Serraj R, Fleurat-Lessard P, Jaillard B, Drevon JJ (1995) Structural changes in the inner-cortex cells of soybean root nodules are induced by short-term exposure to high salt or oxygen concentrations. Plant Cell Environ 18:455–62Google Scholar
  119. Shamseldin A, Nyalwidhe J, Werner D (2006) A proteomic approach towards the analysis of salt tolerance in Rhizobium etli and Sinorhizobium meliloti strains. Curr Microbiol 52:333–339PubMedGoogle Scholar
  120. Shannon MC (1997) Adaptation of plants to salinity. Adv Agron 60:75–120Google Scholar
  121. Sheokand S, Dhandi S, Swaraj K (1995) Studies on nodule functioning and hydrogen peroxide scavenging enzymes under salt stress in chick pea nodule. Plant Physiol Biochem 33:561–566Google Scholar
  122. Singleton PW, Bohlool BB (1984) Effect of salinity on nodule formation by soybean. Plant Physiol 74:72–76PubMedPubMedCentralGoogle Scholar
  123. Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Fact 5:1–19Google Scholar
  124. Skorupska A, Wielbo J, Kidaj D, Marek-Kozaczuk M (2010) Enhancing Rhizobium-legume symbiosis using signaling factors. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer, New York, pp 27–44Google Scholar
  125. Smith LT, Smith GM, D’souza MR, Pocard JA, Le Rudulier D, Madkour MA (1994) Osmoregulation in Rhizobium meliloti: mechanism and control by other environmental signals. J Exp Zool 268:162–165Google Scholar
  126. Sourjik V, Muschler P, Scharf B, Schmitt R (2000) VisN and VisR are global regulators of chemotaxis, flagellar, and motility genes in Sinorhizobium (Rhizobium) meliloti. J Bacteriol 182:782–788PubMedPubMedCentralGoogle Scholar
  127. Straub PF, Shearer G, Reynolds PHS, Sawyer SA, Kohl D (1997) Effect of disabling bacteroid proline catabolism on the response of soybeans to repeated drought stress. J Exp Bot 48:1299–1307Google Scholar
  128. Talibart R, Jebbar M, Gouffi K, Pichereau V, Gouesbet G, Blanco C, Bernard T, Pocard JA (1997) Transient accumulation of glycine betaine and dynamics of endogenous osmolytes in salt-stressed cultures of Sinorhizobium meliloti. Appl Environ Microbiol 63:4657–4663PubMedPubMedCentralGoogle Scholar
  129. Tank ND, Saraf MS (2010) Salinity resistant PGPR ameliorates NaCl stress on tomato plants. J Plant Interact 5:51–58Google Scholar
  130. Tiaz L, Zeiger E (2002) Plant physiology. Sinauer Associates, Sunderland, pp 591–621Google Scholar
  131. Tilman D (1999) Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proc Natl Acad Sci U S A 96:5995–6000PubMedPubMedCentralGoogle Scholar
  132. Turner NC, Wright GC, Siddique KHM (2000) Adaptation of grain legumes (pulses) to water-limited environments. Adv Agron 71:193–231Google Scholar
  133. Vadez V, Sinclair TR (2002) Sensitivity of N2 fixation trait in soybean cultivar Jackson to manganese. Crop Sci 42:791–796Google Scholar
  134. Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397PubMedPubMedCentralGoogle Scholar
  135. Velagaleti RR, Marsh S (1989) Influence of host cultivars and Bradyrhizobium strains on the growth and symbiotic performance of soybean under salt stress. Plant Soil 119:133–138Google Scholar
  136. Velázquez E, Martínez-Romero E, Rodríguez-Navarro DM, Trujillo ME, Daza A, Mateos PE, Martínez-Molina E, van Berkum P (2001) Characterization of rhizobial isolates of Phaseolus vulgaris by staircase electrophoresis of low-molecular weight RNA. Appl Environ Microbiol 67:1008–1010PubMedPubMedCentralGoogle Scholar
  137. Vineusa P, Léon-Barrios M, Silva C, Willems A, Jabaro-Lorenzo A, Pérez-Galdona R, Werner D, Martínez-Romero E (2005) Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575Google Scholar
  138. Vlassak KM, Vanderleyden J (1997) Factors influencing nodule occupancy by inoculant rhizobia. Crit Rev Plant Sci 16:163–229Google Scholar
  139. Vriezen JAC, de Bruijn FJ, Nusslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Appl Environ Microbiol 73:3451–3459PubMedPubMedCentralGoogle Scholar
  140. Vriezen JAC, de Bruijn FJ, Nüsslein KR (2013) Identification and Characterization of a NaCl responsive genetic locus involved in survival during desiccation in Sinorhizobium meliloti. Appl Environ Microbiol 79:5693–5700PubMedPubMedCentralGoogle Scholar
  141. Wadisirisuk P, Danso SKA, Hardarson G, Bowen GD (1989) Influence of Bradyrhizobium japonicum location and movement on nodulation and nitrogen fixation in soybeans. Appl Environ Microbiol 35:1711–1716Google Scholar
  142. Wais RJ, Keating DH, Long SR (2002) Structure function analysis of Nod factor induced calcium spiking in rhizobium-legume symbiosis. Plant Physiol 129:211–224PubMedPubMedCentralGoogle Scholar
  143. Wang ET, Rogel A, Santos AG d, Martínez-Romero J, Cevallos MA, Martínez-Romero E (1999) Rhizobium etli bv mimosae, a novel biovar isolated from Mimosa affinis. Int J Syst Bacteriol 49:1479–1491PubMedGoogle Scholar
  144. Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24:263–290PubMedGoogle Scholar
  145. Yao SY, Luo L, Har KJ, Becker A, Rüberg S, Yu GQ, Zhu JB, Cheng HP (2004) Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. J Bacteriol 186:6042–6049PubMedPubMedCentralGoogle Scholar
  146. Yeh KC, Peck MC, Long SR (2002) Luteolin and GroESL modulation in vitro activity of NodD. J Bacteriol 84:525–530Google Scholar
  147. 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
  148. Zhang XP, Karsisto M, Harper R, Lindstrom K (1991) Diversity of Rhizobium bacteria isolated from the root nodules of leguminous trees. Int J Syst Bacteriol 41:104–113Google Scholar
  149. Zhao Z, Williams SE, Schuman GE (1997) Renodulation and characterization of Rhizobium isolates from cicer milkvetch (Astragalus cicer L.). Biol Fertil Soils 25:169–174Google Scholar
  150. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–274PubMedPubMedCentralGoogle Scholar
  151. Zurayk R, Adlan M, Baalbaki R, Saxena MC (1998) Interactive effects of salinity and biological nitrogen fixation on chickpea (Cicer arietinum L.) growth. J Agron Crop Sci 180:249–258Google Scholar

Copyright information

© Springer India 2015

Authors and Affiliations

  • Kapudeep Karmakar
    • 1
  • Anjul Rana
    • 1
  • Asmita Rajwar
    • 1
  • Manvika Sahgal
    • 1
  • Bhavdish N. Johri
    • 2
  1. 1.Department of MicrobiologyG.B. Pant University of Agriculture & TechnologyPantnagarIndia
  2. 2.Department of BiotechnologyBarkatullah UniversityBhopalIndia

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