Plant growth promoting rhizobia: challenges and opportunities

3 Biotech

Volumn 5, Issue 4, 2015, Pages 355-377

  Gopalakrishnan, Subramaniam ^a   Sathya, Arumugam ^a   Vijayabharathi, Rajendran ^a   Varshney, Rajeev Kumar ^a   Gowda, C L Laxmipathi ^a   Krishnamurthy, Lakshmanan ^a  

^a INTERNATIONAL CROPS RESEARCH INSTITUTE FOR THE SEMI ARID TROPICS ICRISAT   (India)

Author keywords

Biocontrol; Co inoculation; Heavymetal; PGPR; Rhizobium; Stress

Indexed keywords

1 AMINOCYCLOPROPANECARBOXYLIC ACID; ABSCISIC ACID; CHITINASE; CYTOKININ; GIBBERELLIN; GROWTH PROMOTOR; HEAVY METAL; HYDROGEN CYANIDE; INDOLEACETIC ACID; NITROGEN FERTILIZER; NITROGENASE; PESTICIDE; PHOSPHORUS; PHYTOHORMONE; PLANT GROWTH PROMOTOR; PYOCYANINE; PYRROLNITRIN; SIDEROPHORE; UNCLASSIFIED DRUG;

ABIOTIC STRESS; BIOLOGICAL PEST CONTROL; LEGUME; NITRIFICATION; NITROGEN FIXATION; NONHUMAN; PHYTOREMEDIATION; PLANT GROWTH; PRIORITY JOURNAL; REVIEW; RHIZOBIACEAE; SALINITY; SEED PRODUCTION; SOIL ACIDITY; SYMBIOSIS; TEMPERATURE;

BRADYRHIZOBIACEAE; PHYLLOBACTERIACEAE; RHIZOBIACEAE; RHIZOBIUM;

EID: 85017324740     PISSN: 2190572X     EISSN: 21905738     Source Type: Journal    
DOI: 10.1007/s13205-014-0241-x     Document Type: Review

References (281)

1. Abd-Alla MH (1994a) Solubilization of rock phosphates by Rhizobium and Bradyrhizobium. Folia Microbiol 39:53–56
2. Abd-Alla MH (1994b) Use of organic phosphorus by Rhizobium leguminosarum biovar. viceae phosphatases. Biol Fertil Soils 18:216–218
3. Afzal A, Bano A (2008) Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum L.). Int J Agric Biol 10:85–88
4. Ahemad M, Khan MS (2009a) Toxicity assessment of herbicides quizalafop-p-ethyl and clodinafop towards Rhizobium pea symbiosis. Bull Environ Contam Toxicol 82:761–766
5. Ahemad M, Khan MS (2009b) Effect of insecticide-tolerant and plant growth promoting Mesorhizobium on the performance of chickpea grown in insecticide stressed alluvial soils. J Crop Sci Biotech 12:217–226
6. Ahemad M, Khan MS (2010a) Comparative toxicity of selected insecticides to pea plants and growth promotion in response to insecticide-tolerant and plant growth promoting Rhizobium leguminosarum. Crop Prot 29:325–329
7. Ahemad M, Khan MS (2010b) Ameliorative effects of Mesorhizobium sp. MRC4 on chickpea yield and yield components under different doses of herbicide stress. Pestic Biochem Physiol 98:183–190
8. Ahemad M, Khan MS (2010c) Insecticide-tolerant and plant growth promoting Rhizobium improves the growth of lentil (Lens esculentus) in insecticide-stressed soils. Pest Manag Sci 67:423–429
9. Ahemad M, Khan MS (2010d) Growth promotion and protection of lentil (Lens esculenta) against herbicide stress by Rhizobium species. Ann Microbiol 60:735–745
10. Ahemad M, Khan MS (2010e) Improvement in the growth and symbiotic attributes of fungicide-stressed chickpea plants following plant growth promoting fungicide-tolerant Mesorhizobium inoculation. Afr J Basic Appl Sci 2:111–116
11. Ahemad M, Khan MS (2011a) Effect of pesticides on plant growth promoting traits of green gram-symbiont, Bradyrhizobium sp. strain MRM6. Bull Environ Contam Toxicol 86:384–388
12. Ahemad M, Khan MS (2011b) Ecotoxicological assessment of pesticides towards the plant growth promoting activities of Lentil (Lens esculentus)-specific Rhizobium sp. strain MRL3. Ecotoxicology 20:661–669
13. Ahemad M, Khan MS (2011c) Insecticide-tolerant and plant growth promoting Bradyrhizobium sp. (vigna) improves the growth and yield of green gram [Vigna radiata (L.) Wilczek] in insecticide stressed soils. Symbiosis 54:17–27
14. Ahemad M, Khan MS (2011d) Effect of tebuconazole-tolerant and plant growth promoting Rhizobium isolate MRP1 on pea-Rhizobium symbiosis. Sci Hortic 129:266–272
15. Ahemad M, Khan MS (2011e) Plant growth promoting fungicide tolerant Rhizobium improves growth and symbiotic characteristics of lentil (Lens esculentus) in fungicide-applied soil. J Plant Growth Regul 30:334–342
16. Ahemad M, Khan MS (2011f) Insecticide-tolerant and plant growth promoting Rhizobium improves the growth of lentil (Lens esculentus) in insecticide-stressed soils. Pest Manag Sci 67:423–429
17. Ahemad M, Khan MS (2012a) Ecological assessment of biotoxicity of pesticides towards plant growth promoting activities of pea (Pisum sativum)-specific Rhizobium sp. strain MRP1. Emir J Food Agric 24:334–343
18. Ahemad M, Khan MS (2012b) Productivity of green gram in tebuconazole-stressed soil, by using a tolerant and plant growth promoting Bradyrhizobium sp. MRM6 strain. Acta Physiol Plant 34:245–254
19. Ahemad M, Khan MS (2012c) Effects of pesticides on plant growth promoting traits of Mesorhizobium strain MRC4. J Saudi Soc Agric Sci 11:63–71
20. Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181
21. Akhtar N, Qureshi MA, Iqbal A, Ahmad MJ, Khan KH (2012) Influence of Azotobacter and IAA on symbiotic performance of Rhizobium and yield parameters of lentil. J Agric Res 50:361–372
22. Alexandre A, Oliveira S (2011) Most heat-tolerant rhizobia show high induction of major chaperone genes upon stress. FEMS Microbiol Ecol 75:28–36
23. 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 188:6308–6317
24. Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effects on radish (Raphanus sativus L.). Plant Soil 204:57–67
25. Aouani ME, Mhamdi R, Mars M, Ghrir R (1998) Nodulation and growth of common bean under NaCl stress. Soil Biol Biochem 30:1473–1475
26. Arora NK, Kang SC, Maheshwari DK (2001) Isolation of siderophore producing strains of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr Sci 81:673–677
27. Bardin SD, Huang HC, Pinto J, Amundsen EJ, Erickson RS (2004) Biological control of Pythium damping-off of pea and sugar beet by Rhizobium leguminosarum bv. viceae. Can J Bot 82:291–296
28. 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 229:183–188
29. Bashan Y, de Bashan LE (2005) Bacterial plant growth promotion. In: Hillel D (ed) Encyclopedia of soils in the environment. Elsevier, Oxford, pp 103–115
30. Beltra R, Del-Solar G, Sanchez-Serrano JJ, Alonso E (1988) Mutants of Rhizobium phaseoli HM Mel (2) obtained by means of elevated temperatures. Zentbl Mikrobiol 143:529–532
31. Berraho EL, Lesueur D, Diem HG, Sasson A (1997) Iron requirement and siderophore production in Rhizobium ciceri during growth on an iron-deficient medium. World J Microbiol Biotechnol 13:501–510
32. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350
33. Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobial inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650
34. Bodek I, Lyman WJ, Reehl WF, Rosenblatt DH (1988) Environmental inorganic chemistry: properties, processes, and estimation methods. In: Walton BT, Conway RA (eds) SETAC special publication series. Pergamon Press, New York
35. Bohlool BB, Ladha JK, Garrity DP, George T (1992) Biological nitrogen fixation for sustainable agriculture: a perspective. Plant Soil 141:1–11
36. Boiero L, Perrig D, Masciarelli O, Penna C, Cassan F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880
37. Boscari A, Mandon K, Dupont L, Poggi MC, Le-Rudulier D (2002) BetS is a major glycine betaine/praline betaine transporter required for early osmotic adjustment in Sinorhizobium meliloti. J Bacteriol 184:2654–2663
38. Boscari A, Mandon K, Poggi MC, Le Rudulier D (2004) Functional expression of Sinorhizobium meliloti BetS, a high-affinity betaine transporter, in Bradyrhizobium japonicum USDA110. Appl Environ Microbiol 70:5916–5922
39. Buol S, Eswaran H (2000) Oxisols. Adv Agron 68:151–195
40. Caba JM, Centeno ML, Fernandez B, Gresshoff PM, Ligero F (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a super nodulating mutant and the wild type. Planta 211:98–104
41. Camerini S, Senatore B, Lonardo E, Imperlini E, Bianco C, Moschetti G, Rotino GL, Campion B, Defez R (2008) Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development. Arch Microbiol 190:67–77
42. Carrasco JA, Armario P, Pajuelo E, Burgos A, Caviedes MA, López R, Chamber MA, Palomares AJ (2005) Isolation and characterization of symbiotically effective Rhizobium resistant to arsenic and heavy metals after the toxic spill at the Aznalcóllar pyrite mine. Soil Biol Biochem 37:1131–1140
43. Carson KC, Meyer JM, Dilworth MJ (2000) Hydroxamate siderophore of root nodule bacteria. Soil Biol Biochem 32:11–21
44. Cassan F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35
45. Castro IV, Ferreira EM, McGrath SP (1997) Effectiveness and genetic diversity of Rhizobium leguminosarum bv. trifolii isolates in Portuguese soils polluted by industrial effluents. Soil Biol Biochem 29:1209–1213
46. Chabot R, Antoun H, Cescas MC (1996) Growth promotion of maize and lettuce by phosphate solubilizing Rhizobium leguminosarum bv. phaseoli. Plant Soil 184:311–321
47. Chandra R, Pareek RP (2002) Effect of rhizobacteria in urd bean and lentil. Ind J Pulse Res 15:152–155
48. Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere competent Mesorhizobium loti MP6 induces root hair curling, inhibits Sclerotinia sclerotiorum and enhances growth of Indian mustard (Brassica campestris). Braz J Microbiol 38:128–130
49. Chaudhary P, Dudeja SS, Kapoor KK (2004) Effectiveness of host-Rhizobium leguminosarum symbiosis in soils receiving sewage water containing heavy metals. Microbiol Res 159:121–127
50. Chaudri AM, Allain CMG, 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 221:167–179
51. Chein CT, Maundu J, Cavaness J, Daudurand LM, Orser CS (1992) Characterization of salt-tolerant and salt-sensitive mutants of Rhizobium leguminosarum biovar viciae strain C1204b. FEMS Microbiol Lett 90:135–140
52. Chen P (2011) Symbiotic effectiveness, competitiveness and salt tolerance of lucerne rhizobia. RMIT University, Australia
53. Chen RJ, Bhagwat AA, Yaklich R, Keister DL (2002) Characterization of ndvD, the third gene involved in the synthesis of cyclic beta-(1– > 3) (1– > 6)-D-glucans in Bradyrhizobium japonicum. Can J Microbiol 48:1008–1016
54. Chi F, Yang P, Han F, Jing Y, Shen S (2010) Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021. Proteomics 10:1861–1874
55. Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832
56. Dardanelli MS, de Cordoba FJF, Espuny MR, Carvajal MAR, Diaz MES, Serrano AMG, OkonY MM (2008) Effect of Azospirillum brasilense co-inoculated with Rhizobium on Phaseolus vulgaris flavonoids and nod factor production under salt stress. Soil Biol Biochem 40:2713–2721
57. Dashadi M, Khosravi H, Moezzi A, Nadian H, Heidari M, Radjabi R (2011) Co-inoculation of Rhizobium and Azotobacter on growth indices of faba bean under water stress in the green house condition. Adv Stud Biol 3:373–385
58. Davies PJ (1995) The plant hormones: their nature, occurrence and functions. In: Davies PJ (ed) Plant hormones: physiology, biochemistry and molecular biology. Kluwer Academic Publishers, Dordrecht, pp 1–12
59. Dazzo FB, Yanni YG, Rizk R, Zidan M, Gomaa M, Abu-Baker, Squartini A, Jing Y, Chi F, Shen SH (2005) Recent studies on the Rhizobium cereal association. In: Wang YP, Lin M, Tian ZX, Elmericj C, Newton WE (eds) Biological nitrogen fixation: sustainable agriculture and the environment. Proceedings of the 14th international nitrogen fixation congress. Springer, Dordrecht, pp 379–380
60. Deanand BJ, Patil AB, Kulkaarni JH, Algawadi AR (2002) Effect of plant growth promoting rhizobacteria on growth and yield of pigeonpea (Cajanus cajan L.) by application of plant growth promoting rhizobacteria. Microbiol Res 159:371–394
61. Deshwal VK, Dubey RC, Maheshwari DK (2003a) Isolation of plant growth promoting strains of Bradyrhizobium (Arachis) sp. with biocontrol potential against Macrophomina phaseolina causing charcoal rot of peanut. Curr Sci 84:443–444
62. Deshwal VK, Pandey P, Kang SC, Maheshwari DK (2003b) Rhizobia as a biological control agent against soil borne plant pathogenic fungi. Ind J Exp Biol 41:1160–1164
63. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149
64. Downie A (1997) Fixing a symbiotic circle. Nature 387:352–353
65. Duan J, Muller KM, Charles TC, Vesely S, Glick BR (2009) 1-Aminocyclopropane-1carboxylate (ACC) deaminase gene in Rhizobium from Southern Saskatchewan. Microbial Ecol 57:423–436
66. Duhan JS, Dudeja SS, Khurana AL (1998) Siderophore production in relation to N2 fixation and iron uptake in pigeonpea-Rhizobium symbiosis. Folia Microbiol 43:421–426
67. Eaglesham ARJ, Ayanaba A (1984) Tropical stress ecology of rhizobia, root-nodulation and legume fixation. In: Subba Rao NS (ed) Current developments in biological nitrogen fixation. Edward Arnold Publishers, London, pp 1–35
68. Egamberdiyeva D, Juraeva D, Poberejskaya S, Myachina O, Teryuhova P, Seydalieva L, Aliev A (2004) Improvement of wheat and cotton growth and nutrient uptake by phosphate solubilizing bacteria. In: Proceeding of 26th annual conservation tillage conference for sustainable agriculture, Auburn, pp 58–65
69. Ehteshamul-Haque S, Ghaffar A (1993) Use of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mung bean. J Phytopathol 138:157–163
70. El Abyad MS, Abou-Taleb AM (1985) Effects of the herbicides simazine and bromophenoxim on the microflora of two soil types in Egypt. Zentralblatt für Mikrobiologie 40:607–619
71. El Sheikh EE, Wood M (1990) Salt effects on survival and multiplication of chickpea and soybean rhizobia. Soil Biol Biochem 22:343–347
72. Elkoca E, Kantar F, Sahin F (2008) Influence of nitrogen fixing and phosphorus solubilizing bacteria on the nodulation, plant growth and yield of chickpea. J Plant Nutr 31:157–171
73. Estevez J, Dardanelli MS, Megías M, Rodríguez-Navarro DN (2009) Symbiotic performance of common bean and soybean co-inoculated with rhizobia and Chryseobacterium balustinum Aur9 under moderate saline conditions. Symbiosis 49:29–36
74. Fan LM, Maa ZQ, Liang JQ, Li HF, Wangc ET, Wei GH (2011) Characterization of a copper-resistant symbiotic bacterium isolated from Medicago lupulina growing in mine tailings. Bioresour Technol 102:703–709
75. FAO (2011) The state of the world’s land and water resources for food and agriculture (SOLAW)—Managing systems at risk. Food and Agriculture Organization of the United Nations, Rome and Earthscan, London
76. Figueira EMAP, Lima AIG, Pereira SIA (2005) Monitoring glutathione levels as a marker for cadmium stress in Rhizobium leguminosarum biovar viciae. Can J Microbiol 51:7–14
77. Figueiredo MVB, Burity HA, Martinez CR, Chanway CP (2008) Alleviation of drought stress in common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182–188
78. Foster LJR, Moy YP, Rogers PL (2000) Metal binding capabilities of Rhizobium etli and its extracellular polymeric substances. Biotechnol Lett 22:1757–1760
79. Fox SL, O’Hara GW, Bräu L (2011) Enhanced nodulation and symbiotic effectiveness of Medicago truncatula when co-inoculated with Pseudomonas fluorescens WSM3457 and Ensifer (Sinorhizobium) medicae WSM419. Plant Soil 348:245–254
80. Frankenberger WTJ, Arshad M (1995) Photohormones in soil: microbial production and function. Dekker, New York
81. Gal SW, Choi YJ (2003) Isolation and characterization of salt tolerance rhizobia from Acacia root nodules. Agric Chem Biotechnol 46:58–62
82. Gianfreda L, Rao MA (2004) Potential of extra cellular enzymes in remediation of polluted soils: a review. Enzyme Microb Technol 35:339–354
83. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117
84. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica, Article ID 963401. doi:http://dx.doi.org/10.6064/2012/963401
85. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39
86. Gopalakrishnan S, Watanabe T, Pearse SJ, Ito O, Hossian AKMZ, Subbarao GV (2009) Biological nitrification inhibition by Brachiaria humidicola roots varies with soil type and inhibits nitrifying bacteria, but not other major soil microorganisms. Soil Sci Plant Nutr 55:725–733
87. Graham PH (1992) Stress tolerance in Rhizobium and Bradyrhizobium and nodulation under adverse soil conditions. Can J Microbiol 38:475–484
88. Graham PH, Draeger KJ, Ferrey ML, Conroy MJ, Hammer BE, Martínez E, Aarons SR, Quinto C (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 40:198–207
89. Gray J, Murphy B (2002) Parent material and world soil distribution, 17th world congress of soil science. Bangkok, Thailand
90. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412
91. Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2010) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240
92. Gügi B, Orange N, Hellio F, Burini JF, Guillou C, Leriche F, Guespin-Michel JF (1991) Effect of growth temperature on several exported enzyme activities in the psychrotropic bacterium Pseudomonas fluorescens. J Bacteriol 173:3814–3820
93. Guo J, Chi J (2014) Effect of Cd-tolerant plant growth promoting Rhizobium on plant growth and Cd uptake by Lolium multiflorum Lam. and Glycine max (L.) Merr. in Cd-contaminated soil. Plant Soil 375:205–214
94. Gupta A, Saxena AK, Gopal M, Tilak KVBR (1998) Effect of plant growth promoting rhizobacteria on competitive ability of introduced Bradyrhizobium sp. (Vigna) for nodulation. Microbiol Res 153:113–117
95. Hadi F, Bano A (2010) Effect of diazotrophs (Rhizobium and Azatobactor) on growth of maize (Zea mays L.) and accumulation of lead (PB) in different plant parts. P J Bot 42:4363–4370
96. Hafeez FY, Hassan Z, Naeem F, Basher A, Kiran A, Khan SA, Malik KA (2008) Rhizobium leguminosarum bv. viciae strain LC–31: analysis of novel bacteriocin and ACC-deaminase gene(s). In: Dakora FD, Chimphango SBM, Valentine AJ, Elmerich C, Newton WE (eds) Biological nitrogen fixation: towards poverty alleviation through sustainable agriculture. Springer, Dordrecht, pp 247–248
97. Halder AK, Chakrabarty PK (1993) Solubilization of inorganic phosphate by Rhizobium. Folia Microbiol 38:325–330
98. Halder AK, Mishra AK, Bhattacharya P, Chakrabarthy PK (1990) Solubilization of rock phosphate by Rhizobium and Bradyrhizobium. J Gen Appl Microbiol 36:1–92
99. Hall AE (2004) Breeding for adaptation to drought and heat in cowpea. Eur J Agron 21:447–454
100. Han MJ, Yun H, Lee SY (2008) Microbial small heat shock proteins and their use in biotechnology. Biotechnol Adv 26:591–609
101. Hartel PG, Alexander M (1984) Temperature and desiccation tolerance of cowpea rhizobia. Can J Microbiol 30:820–823
102. Hartl FU, Hayer-Hartl M (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 16:574–581
103. Hellweg C, Puhler A, Weidner S (2009) The time course of the transcriptomic response of Sinorhizobium meliloti 1021 following a shift to acidic pH. BMC Microbiol 9:37
104. Hirsch PR, Jones MJ, McGrath SP, Giller KE (1993) Heavy metals from past applications of sewage sludge decrease the genetic diversity of Rhizobium leguminosarum biovar trifolii populations. Soil Biol Biochem 25:1485–1490
105. Huang XD, El Alawi Y, Gurska J, Glick BR, Greenberg BM (2005) A multi-process phytoremediation system for decontamination of persistent total petroleum hydrocarbons (TPHs) from soils. Microchem J 81:139–147
106. Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolusvulgaris L. Plant Soil 149:95–102
107. IFPRI (2012) Global food policy report. International Food Policy Research Institute, Washington
108. Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2008) Promotion of metal accumulation in nodule of Astragalus sinicus by the expression of the iron-regulated transporter gene in Mesorhizobium huakuii subsp. rengei B3. J Biosci Bioeng 105:642–648
109. Islam MZ, Sattar MA, Ashrafuzzaman M, Berahim Z, Shamsuddoha ATM (2013) Evaluating some salinity tolerant rhizobacterial strains to lentil production under salinity stress. Int J Agric Biol 15:499–504
110. Jarvis SC (1996) Future trends in nitrogen research. Plant Soil 181:47–56
111. Jebara M, Mhamdi R, Aouani ME, Ghrir R, Mars M (2001) Genetic diversity of Sinorhizobium populations recovered from different Medicago varieties cultivated in Tunisian soils. Can J Microbiol 47:139–147
112. Jenson JB, Peters NK, Bhuvaneswari TV (2002) Redundancy in periplasmic binding protein-dependent transport systems for trehalose, sucrose, and maltose in Sinorhizobium meliloti. J Bacteriol 184:2978–2986
113. 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 239:139–146
114. Johri BN, Sharma A, Virdi JS (2003) Rhizobacterial diversity in India and its influence on soil and plant health. Adv Biochem Eng Biotechnol 84:49–89
115. Joseph B, Patra RR, Lawrence R (2007) Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.). Int J Plant Prod 2:141–152
116. Kagi JHR (1991) Overview of metallothionein. Methods Enzymol 205:613–626
117. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2000) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331–338
118. 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 112:15–22
119. Khan MS, Zaidi A, Aamil M (2002) Biocontrol of fungal pathogens by the use of plant growth promoting rhizobacteria and nitrogen fixing microorganisms. Ind J Bot Soc 81:255–263
120. Kinkle BK, Sadowsky MJ, Johnstone K, Kokinen WC (1994) Tellurium and selenium resistance in rhizobia and its potential use for direct isolation of Rhizobium meliloti from Soil. Appl Environ Microbiol 60:1674–1677
121. Krasova-Wade T, Diouf O, Ndoye I, Sall CE, Braconnier S, Neyra M (2006) Water condition effects on rhizobia competition for cowpea nodule occupancy. African J Biotech 5:1457–1463
122. Kulkarni S, Nautiyal CS (2000) Effects of salt and pH stress on temperature tolerant Rhizobium sp. NBRI330 nodulating Prosopis juliflora. Curr Microbiol 40:221–226
123. Kumar P (2012) Ph.D. thesis. Gurukul Kangri University, Haridwar, India
124. Kumar S, Mukerji KG, Lai R (1996) Molecular aspects of pesticide degradation by microorganisms. Crit Rev Microbiol 22:1–26
125. Lakzian A, Murphy P, Turner A, Beynon JL, Giller KE (2002) Rhizobium leguminosarum bv. viciae populations in soils with increasing heavy metal contamination: abundance, plasmid profiles, diversity and metal tolerance. Soil Biol Biochem 34:519–529
126. Laranjo M, Alexandre A, Oliveira S (2014) Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. Microbiol Res 169:2–17
127. Lindström K, Lipsanen P, Kaijalainen S (1990) Stability of markers used for identification of two Rhizobium galegae inoculant strains after five years in the field. Appl Environ Microbiol 56:444–450
128. Liu Y, Lam MC, Fang HHP (2001) Adsorption of heavy metals by EPS of activated sludge. Water Sci Technol 43:59–66
129. Lloret J, Bolanos L, Lucas MM, Peart JM, Brewin NJ, Bonilla I, Rivilla R (1995) Ionic stress and osmotic pressure induce different alterations in the lipopolysaccharide of a Rhizobium meliloti strain. Appl Environ Microbiol 61:3701–3704
130. Lloret J, Wulff BBH, Rubio JM, Downie JA, Bonilla I, Rivilla R (1998) Exo-polysaccharide II production is regulated by salt in the halotolerant strain Rhizobium meliloti EFB1. J Bacteriol 179:5366–5371
131. Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25
132. Lugtenberg B, Kamilova F (2009) Plant growth promoting rhizobacteria. Ann Rev Microbiol 63:541–556
133. Ma W, Guinel FC, Glick BR (2003a) The Rhizobium leguminosarum bv. viciae ACC deaminase protein promotes the nodulation of pea plants. Appl Environ Microbiol 69:4396–4402
134. Ma W, Sebestianova S, Sebestian J, Burd GI, Guinel F, Glick BR (2003b) Prevalence of 1-aminocyclopropaqne-1-carboxylate in deaminase in Rhizobiaum sp. Antonie Van Leeuwenhoek 83:285–291
135. Ma W, Charles TC, Glick BR (2004) Expression of an exogenous 1 aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Appl Environ Microbiol 70:5891–5897
136. Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258
137. Madhaiyan M, Poonguzhali S, Ryu JH, Sa TM (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224:268–278
138. Martinez-Toledo MV, Salmeron V, Rodelas B, Pozo C, Gonzalez-Lopez J (1996) Studies on the effects of the herbicide simazine on microflora of four agricultural soils. Environ Toxicol Chem 15:1115–1118
139. Mathur SC (1999) Future of Indian pesticides industry in next millennium. Pestic Inf 24:9–23
140. Mauseth JD (1991) Botany: an introduction to plant biology. Saunders, Philadelphia, pp 348–415
141. McGrath JW, Hammerschmidt F, Quinn JP (1998) Biodegradation of phosphonomycin by Rhizobium huakuii PMY1. Appl Environ Microbiol 64:356–358
142. Mehboob I, Naveed M, Zahir ZA, Ashraf M (2012) Potential of rhizobia for sustainable production of non-legumes. In: Ashraf M, Öztürk M, Ahmad M, Aksoy A (eds) Crop production for agricultural improvement. Springer, Netherlands, pp 659–704
143. Mehboob I, Naveed M, Zahir ZA, Sessitch A (2013) Potential or rhizosphere bacteria for improving Rhizobium-Legume symbiosis. In: Arora NK (ed) Plant microbe symbiosis: fundamentals and advances. Springer, India, pp 305–349
144. Mehra RK, Mulchandani P (1995) Glutathione-mediated transfer of Cu (I) into phytochelatins. Biochem J 307:697–705
145. Mhadhbi H, Jebara M, Limam F, Aouani ME (2004) Rhizobial strain involvement in plant growth, nodule protein composition and antioxidant enzyme activities of chickpea–rhizobia symbioses: modulation by salt stress. Plant Physiol Biochem 42:717–722
146. Mhadhbi H, Jebara M, Zitoun A, Limam F, Aouani ME (2008) Symbiotic effectiveness and response to mannitol-mediated osmotic stress of various chickpea–rhizobia associations. World J Microbiol Biotech 24:1027–1035
147. Michiels J, Verreth C, Vanderleyden J (1994) Effects of temperature stress on bean nodulating Rhizobium strains. Appl Environ Microbiol 60:1206–1212
148. Miller-Williams M, Loewen PC, Oresnik IJ (2006) Isolation of salt sensitive mutants of Sinorhizobium meliloti strain Rm1021. Microbiol 152:2049–2059
149. Mishra RPN, Singh RK, Jaiswal HK, Kumar V, Maurya S (2006) Rhizobium-mediated induction of phenolics and plant growth promotion in rice (Oryza sativa L.). Curr Microbiol 52:383–389
150. Mishra PK, Mishra S, Selvakumar G, Bisht JK, Kundu S, Gupta HS (2009) Co-inoculation of Bacillus thuringeinsis -KR1 with Rhizobium leguminosarum enhances plant growth and nodulation of pea (Pisum sativum L.) and lentil (Lens culinaris L.). World J Microbiol Biotechnol 25:753–761
151. Moorma TB (1988) A review of pesticide effects on microorganisms and microbial processes related to soil fertility. J Prod Agric 2:14–23
152. Mpepereki SF, Makoneses Wollum AG (1997) Physiological characterization of indigenous rhizobia nodulating Vigna unguiculata in Zimbabwean soils. Symbiosis 22:275–292
153. Mrabet M, Mhamdi R, Tajini F, Tiwari R, Trabelsi M, Aouani ME (2005) Competitiveness and symbiotic effectiveness of a R. gallicum strain isolated from root nodules of Phaseolus vulgaris. Europ J Agron 22:209–216
154. Muglia CI, Grasso DH, Aguilar OM (2007) Rhizobium tropici response to acidity involves activation of glutathione synthesis. Microbiol 153:1286–1296
155. Münchbach M, Nocker A, Narberhaus F (1999) Multiple small heat shock proteins in Rhizobia. J Bacteriol 181:83–90
156. Munns DN, Keyser HH, Fogle VW, Hohenberg JS, Righetti TL, Lauter DL, Zaruog MG, Clarkin KL, Whitacre KW (1979) Tolerance of soil acidity in symbiosis of mung bean with rhizobia. Agron J 71:256–260
157. Naidu VSGR, Panwar JDS, Annapurna K (2004) Effect of synthetic auxins and Azorhizobium caulinodans on growth and yield of rice. Ind J Microbiol 44:211–213
158. Nandal K, Sehrawat AR, Yadav AS, Vashishat RK, Boora KS (2005) High temperature-induced changes in exo-polysaccharides, lipo-polysaccharides and protein profile of heat-resistant mutants of Rhizobium sp. (Cajanus). Microbiol Res 160:367–373
159. Nascimento F, Brígido C, Alho L, Glick BR, Oliveira S (2012) Enhanced chickpea growth promotion ability of a mesorhizobia expressing an exogenous ACC deaminase gene. Plant Soil 353:221–230
160. Neubauer U, Furrer G, Kayser A, Schulin R (2000) Siderophores, NTA, and citrate: potential soil amendments to enhance heavy metal mobility in phytoremediation. Int J Phytoremed 2:353–368
161. Nieto KF, Frankenberger WT Jr (1990) Influence of adenine, isopentyl alcohol and Azotobacter chroococcum on the growth of Raphanus sativus. Plant Soil 127:147–156
162. Nieto KF, Frankenberger WT Jr (1991) Influence of adenine, isopentyl alcohol and Azotobacter chroococcum on the vegetative growth of Zea mays. Plant Soil 135:213–221
163. Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF (1996) Rhizobium leguminosarum as a plant growth promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J Microbiol 42:279–283
164. Nogales J, Campos R, Ben-Abdelkhalek H, Olivares J, Lluch C, Sanjuan J (2002) Rhizobium tropici genes involved in free-living salt tolerance are required for the establishing of efficient nitrogen-fixing symbiosis with Phaseolus vulgaris. Mol Plant Microbe Interact 15:225–232
165. Nonnoi F, Chinnaswamy A, de la Torre VSG, de la Pẽna TC, Lucas MM, Pueyo JJ (2012) Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes (Medicago spp. and Trifolium spp.) growing in mercury-contaminated soils. Appl Soil Ecol 61:49–59
166. Ohtake H, Wu H, Imazu K, Ambe Y, Kato J, Kuroda A (1996) Bacterial phosphonate degradation, phosphite oxidation and polyphosphate accumulation. Res Conserv Recycl 18:125–134
167. Okazaki S, Sugawara M, Minamisawa K (2004) Bradyrhizobium elkanii rtxC gene is required for expression of symbiotic phenotypes in the final step of rhizobitoxine biosynthesis. Appl Environ Microbiol 70:535–541
168. Ozkoc I, Deliveli MH (2001) In vitro inhibition of the mycelial growth of some root rot fungi by Rhizobium leguminosarum biovar phaseoli isolates. Turk J Biol 25:435–445
169. Parker JH (1972) How fertilizer moves and reacts in soil. Crops Soils 72:7–11
170. Pathak DV, Sharma MK, Sushil K, Naresh K, Sharma PK (2007) Crop improvement and root rot suppression by seed bacterization in chickpea. Arch Agron Soil Sci 53:287–292
171. Paton GI, Palmer G, Burton M, Rattray EAS, McGrath SP, Glover LA, Killham K (1997) Development of an acute and chronic ecotoxicity assay using lux-marked Rhizobium leguminosarum biovar trifolii. Lett Appl Microbiol 24:296–300
172. Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220
173. Paudyal SP, Aryal RR, Chauhan SVS, Maheshwari DK (2007) Effect of heavy metals on growth of rhizobium strains and symbiotic efficiency of two species of tropical legumes. Sci World 5:27–32
174. 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 41:47–53
175. Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martínez-Molina E, Velazquez E (2001) Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorhizobium mediterraneum under growth. Soil Biol Biochem 33:103–110
176. Peng S, Biswas JC, Ladha JK, Gyaneshwar P, Chen Y (2002) Influence of rhizobial inoculation on photosynthesis and grain yield of rice. Argon J 94:925–929
177. Penning de Vries FWT, Van Laar HH, Chardon MCM (1983) Bioenergetics of growth of seeds, fruits and storage organs. Proceedings on Potential productivity of field crops under different environments on 22–26th September 1980. International Rice Research Institute, Los Banos, pp 37–59
178. Peoples MB, Brockwell J, Herridge DF, Rochester IJ, Alves BJR, Urquiaga S, Boddey RM, Dakora FD, Bhattarai S, Maskey SL, Sampet C, Rerkasem B, Khan DF, Hauggaard-Nielsen H, Jensen ES (2009) The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48:1–17
179. Peoples MB, Crasswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant Soil 141:13–39
180. Pereira SIA, Lima AIG, Figueira EMAP (2006a) Heavy metal toxicity in Rhizobium leguminosarum biovar viciae isolated from soils subjected to different sources of heavy-metal contamination: effects on protein expression. Appl Soil Ecol 33:286–293
181. Pereira SIA, Lima AIG, Figueira EMAP (2006b) Screening possible mechanisms mediating cadmium resistance in Rhizobium leguminosarum bv. viciae isolated from contaminated Portuguese soils. Microbial Ecol 52:176–186
182. Prabha C, Maheshwari DK, Bajpai VK (2013) Diverse role of fast growing rhizobia in growth promotion and enhancement of psoralen content in Psoralea corylifolia L. Pharmacogn Mag 9:S57–S65
183. Pulsawat W, Leksawasdi N, Rogers PL, Foster LJR (2003) Anions effects on biosorption of Mn(II) by extracellular polymeric substance (EPS) from Rhizobium etli. Biotechnol Lett 25:1267–1270
184. Purchase D, Miles RJ (2001) Survival and nodulating ability of indigenous and inoculated Rhizobium leguminosarum biovar trifolii in sterilized and unsterilized soil treated with sewage sludge. Curr Microbiol 42:59–64
185. Purchase D, Miles RJ, Young TWK (1997) Cadmium uptake and nitrogen fixing ability in heavy-metal-resistant laboratory and field strains of Rhizobium leguminosarum biovar trifolii. FEMS Microbiol Ecol 22:85–93
186. Qureshi MA, Ahmad MJ, Naveed M, Iqbal A, Akhtar N, Niazi KH (2009) Co-inoculation with Mesorhizobium ciceri and Azotobacter chroococcum for improving growth, nodulation and yield of chickpea (Cicer arietinum L.). Soil Environ 28:124–129
187. Rajendran G, Sing F, Desai AJ, Archana G (2008) Enhanced growth and nodulation of pigeonpea by co-inoculation of Bacillus strains with Rhizobium sp. Bioresour Technol 99:544–550
188. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149
189. Reddy PP (2013) Plant growth promoting rhizobacteria (PGPR). Recent advances in crop protection. Springer, India, pp 131–145
190. Reichman SM (2007) The potential use of the legume-rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol Biochem 39:2587–2593
191. Reitz M, Rudolph K, Schroder I, Hoffmann-Hergarten S, Hallmann J, Sikora RA (2000) Lipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida. Appl Environ Microbiol 66:3515–3518
192. Remans R, Croonenborghs A, Gutierrez RT, Michiels J, Vanderleyden J (2007) Effects of plant growth-promoting rhizobacteria on nodulation of Phaseolus vulgaris L. are dependent on plant P nutrition. Eur J Plant Pathol 119:341–351
193. Remans R, Ramaekers L, Schelkens S, Hernandez G, Garcia A, Reyes JL, Mendez N, Toscano V, Mulling M, Galvez L, Vanderleyden J (2008) Effect of Rhizobium-Azospirillum coinoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in Cuba. Plant Soil 312:25–37
194. Richardson AE, Hadobas PA (1997) Soil isolates of Pseudomonas sp. that utilize inositol phosphates. Can J Microbiol 43:509–516
195. Richardson AE, Henderson AP, James GS, Simpson RJ (1988) Consequences of soil acidity and the effect of lime on the nodulation of Trifolium subterraneum L. growing in an acid soil. Soil Biol Biochem 20:439–445
196. Robinson B, Russell C, Hedley M, Clothier B (2001) Cadmium adsorption by rhizobacteria: implications for New Zealand pastureland. Agric Ecosyst Environ 87:315–321
197. Rodrigues C, Laranjo M, Oliveira S (2006) Effect of heat and pH stress in the growth of chickpea mesorhizobia. Curr Microbiol 53:1–7
198. Rodríguez-Echevarría S, Pérez-Fernández MA (2005) Potential use of Iberian shrubby legumes and rhizobia inoculation in re-vegetation projects under acidic soil conditions. Appl Soil Ecol 29:203–208
199. 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 41:2568–2572
200. Roseline R, Lara R, Sarah S, German H, Aurelio G, Jorge R, Nancy M, Vidalina T, Miguel M, Lazaro G, Jos V (2008) Effect of Rhizobium-Azospirillum co-inoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in Cuba. Plant Soil 312:25–37
201. Sanginga N, Danso SKA, Mulongoy K, Ojeifo AA (1994) Persistence and recovery of introduced Rhizobium 10 years after inoculation on Leucaena leucocephala grown on an Alfisol in Southwestern Nigeria. Plant Soil 159:199–204
202. Sardesai N, Babu CR (2001) Cold stress induced high molecular weight membrane polypeptides are responsible for cold tolerance in Rhizobium DDSS69. Microbiol Res 156:279–284
203. Saxena D, Amin M, Khanna S (1996) Modulation of protein profiles in Rhizobium sp. under salt stress. Can J Microbiol 42:617–620
204. Senthilkumar M, Madhaiyan M, Sundaram SP, Kannaiyan S (2009) Intercellular colonization and growth promoting effects of Methylobacterium sp. with plant-growth regulators on rice (Oryza sativa L. CvCO-43). Microbiol Res 164:92–104
205. Serraj R, Roy G, Drevon JJ (1994) Salt stress induces a decrease in the oxygen uptake of soybean nodules and in their permeability to oxygen diffusion. Physiol Plant 191:161–168
206. Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean. Lett Appl Microbiol 42:155–159
207. Sharma P, Padh H, Shrivastava N (2013) Hairy root cultures: a suitable biological system for studying secondary metabolic pathways in plants. Eng Life Sci 13:62–75
208. Shaukat SS, Siddqui IA (2003) The influence of mineral and carbon sources on biological control of charcoal rot fungus, Macrophomina phaseolina by fluorescent pseudomonads in tomato. Lett Appl Microbiol 36:392–398
209. Siddiqui ZA, Mahmood I (2001) Effects of rhizobacteria and root symbionts on the reproduction of Meloidogyne javanica and growth of chickpea. Bioresour Technol 79:41–45
210. Siddiqui IA, Ehteshamul-Haque S, Ghaffar A (1998) Effect of rhizobia and fungal antagonists in the control of root infecting fungi on sun flower and chickpea. Pak J Bot 30:279–286
211. Siddiqui IA, Ehteshamul-Haque S, Zaki MJ, Ghaffar A (2000) Effect of urea on the efficacy of Bradyrhizobium sp. and Trichoderma harzianum in the control of root infecting fungi in mungbean and sunflower. Sarhad J Agric 16:403–406
212. Sinclair TR, de Wit CT (1975) Photosythate and nitrogen requirement for seed production of various crops. Science 189:565–567
213. Sindhu SS, Dadarwal KR (2001) Chitinolytic and cellulolytic Pseudomonas sp. antagonistic to fungal pathogen enhances nodulation by Mesorhizobium sp. Cicer in chickpea. Microbiol Res 156:353–358
214. Singh G, Wright D (2002) In vitro studies on the effects of herbicides on the growth of rhizobia. Lett Appl Microbiol 35:12–16
215. Singh RK, Mishra RPN, Jaiswal HK, Kumar V, Pandev SP, Rao SB, Annapurna K (2006) Isolation and identification of natural endophytic rhizobia from rice (Oryza sativa L.) through rDNA PCR-RFLP and sequence analysis. Curr Microbiol 52:345–349
216. Singh G, Sekhon HS, Sharma P (2011) Effect of irrigation and biofertilizer on water use, nodulation, growth and yield of chickpea (Cicer arietinum L.). Arch Agron Soil Sci 57:715–726
217. Skrary FA, Cameron DC (1998) Purification and characterization of a Bacillus licheniformis phosphatase specific for D-alphaglycerphosphate. Arch Biochem Biophys 349:27–35
218. Smith SR (1997) Rhizobium in soils contaminated with copper and zinc following the long-term application of sewage sludge and other organic wastes. Soil Biol Biochem 29:1475–1489
219. 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 268:162–165
220. Soussi M, Santamaría M, Ocaña A, Lluch C (2001) Effects of salinity on protein and lipopolysaccharide pattern in a salt-tolerant strain of Mesorhizobium ciceri. J Appl Microbiol 90:476–481
221. Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3:a001438
222. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448
223. Sriprang R, Hayashi M, Yamashita M, Ono H, Saeki K, Murooka Y (2002) A novel bioremediation system for heavy metals using the symbiosis between leguminous plant and genetically engineered rhizobia. J Biotech 99:279–293
224. Sriprang R, Hayashi M, Ono H, Takagi M, Hirata K, Murooka Y (2003) Enhanced accumulation of Cd2+ by a Mesorhizobium sp. transformed with a gene from Arabidopsis thaliana coding for phytochelatin synthase. Appl Environ Microbiol 69:1791
225. Stajkovic O, Delic D, Josic D, Kuzmanovic D, Rasulic N, Knezevic-Vukcevic J (2011) Improvement of common bean growth by co-inoculation with Rhizobium and plant growth promoting bacteria. Rom Biotechnol Lett 16:5919–5926
226. Stan V, Gament E, Cornea CP, Voaides C, Dusa M, Plopeanu G (2011) Effects of heavy metal from polluted soils on the Rhizobium diversity. Not Bot Hort Agrobot Cluj 39:88–95
227. Streeter JG (2003) Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation. J Appl Microbiol 95:484–491
228. Suárez R, Wong A, Ramírez M, Barraza A, Orozco MC, Cevallos MA, Lara M, Hernández G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant Microbe Interact 21:958–966
229. Subbarao GV, Johansen C, Jana MK, Kumar Rao JVDK (1990) Effects of the sodium/calcium ratio in modifying salinity responses in pigeonpea (Cajanus cajan). Plant Physiol 136:439–443
230. Subbarao GV, Ito O, Sahrawat KL, Berry WL, Nakahara K, Ishikawa T, Watanabe T, Suenaga K, Rondon M, Rao IM (2006) Scope and strategies for regulation of nitrification in agricultural systems challenges and opportunities. Crit Rev Plant Sci 25:303–335
231. Subbarao GV, Sahrawat KL, Nakahara K, Ishikawa T, Kishii M, Rao IM, Hash CT, George TS, Srinivasa Rao P, Nardi P, Bonnett D, Berry W, Suenaga K, Lata JC (2012) Bio-logical nitrification inhibition—a novel strategy to regulate nitrification in agricultural systems. Adv Agron 114:249–302
232. 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 76:1071–1081
233. Sullivan JT, Trzebiatowski JR, Cruickshank RW, Gouzy J, Brown SD, Elliot RM, Fleetwood DJ, McCallum NG, Rossbach U, Stuart GS, Weaver JE, Webby RJ, De Bruijin FJ, Ronson CW (2002) Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 184:3086–3095
234. Sutherland IW (2001) Exo-polysaccharides in biofilms, flocs and related structure. Water Sci Technol 43:77–86
235. Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5:51–58
236. Tao G, Tian S, Cai M, Xie G (2008) Phosphate solubilizing and mineralizing abilities of bacteria isolated from soils. Pedosphere 18:515–523
237. Tchebotar VK, Kang UG, Asis CA Jr, Akao S (1998) The use of GUS-reporter gene to study the effect of Azospirillum-Rhizobium co-inoculation on nodulation of white clover. Biol Fertil Soils 27:349–352
238. Tejera NA, Soussi M, Lluch C (2006) Physiological and nutritional indicators of tolerance to salinity in chickpea plants growing under symbiotic conditions. Environ Exp Bot 58:17–24
239. Thami-Alami I, Elboutahiri N, Udupa SM (2010) Variability in natural populations of Sinorhizobium meliloti in Morocco. In: Porqueddu C, Ríos S (eds) The contributions of grasslands to the conservation of Mediterranean biodiversity. Zaragoza, CIHEAM/CIBIO/FAO/SEEP, pp 265–269
240. Tittabutr P, Payakapoig W, Teaumroong N, Boonkerd N, Singleton PW, Borthakur D (2006) The alternative sigma factor rpoH2 is required for salt tolerance in Sinorhizobium sp. strain BL3. Res Microbiol 157:811–818
241. Tokala RK, Strap JL, Jung CM, Crawford DF, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus Wyec 108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171
242. Turner NC, Wright GC, Siddique KHM (2000) Adaptation of grain legumes (pulses) to water-limited environments. Adv Agron 71:193–231
243. Uchiumi T, Oowada T, Itakura M, Mitsui H, Nukui N, Dawadi P, Kaneko T, Tabata S, Yokoyama T, Tejima T, Saeki K, Oomori H, Hayashi M, Maekawa T, Sriprang R, Murooka Y, Tajima S, Simomura K, Nomura M, Suzuki A, Shimoda S, Sioya K, Abe M, Minamisawa K (2004) Expression islands clustered on symbiosis island of Mesorhizobium loti genome. J Bacteriol 186:2439–2448
244. Uma C, Sivagurunathan P, Sangeetha D (2013) Performance of bradyrhizobial isolates under drought conditions. Int J Curr Microbiol App Sci 2:228–232
245. Uren NC (2007) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil–plant interface. CRC Press, Boca Ratón, pp 1–22
246. USDA (2012) Climate change and agriculture in the United States: effects and adaptation. USDA Technical Bulletin 1935. Washington, DC
247. Vanderlinde EM, Harrison JJ, Muszynski A, Carlson RW, Turner RJ, Yost CK (2010) Identification of a novel ABC transporter required for desicattion tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Ecol 71:327–340
248. Velázquez E, Peix A, Zurdo-Piñeiro JL, Palomo JL, Mateos PF, Rivas R, Muñoz-Adelantado E, Toro N, García-Benavides P, Martínez-Molina E (2005) The coexistence of symbiosis and pathogenicity determining genes in Rhizobium strains enables them to induce nodules and tumors or hairy roots in plants. Mol Plant Microbe Interact 18:1325–1332
249. Verma JP, Yadav J, Tiwari KN, Kumar A (2013) Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286
250. Verma JP, Yadav J, Tiwari KN, Jaiswal DK (2014) Evaluation of plant growth promoting activities of microbial strains and their effect on growth and yield of chickpea (Cicer arietinum L.) in India. Soil Biol Biochem 70:33–37
251. Vessey KJ (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
252. Vidal C, Chantreuil C, Berge O, Maure L, Escarreé J, Béna G, Brunel B, Cleyet-Marel JC (2009) Mesorhizobium metallidurans sp. nov., a metalresistant symbiont of Anthyllis vulneraria growing on metallicolous soil in Languedoc France. Int J Syst Evol Microbiol 59:850–855
253. Villacieros M, Power B, Sanchez-Contreras M, Lloret J, Oruezabal RI, Martin M, Fernandez-Pinas F, Bonilla I, Whelan C, Dowling DN, Rivilla R (2003) Colonization behaviour of Pseudomonas fluorescens and Sinorhizobium meliloti in the alfalfa (Medicago sativa) rhizosphere. Plant Soil 251:47–54
254. Walton DC, Li Y (1995) Abscisic acid biosynthesis and metabolism. Plant hormones: physiology, biochemistry and molecular biology. Kluwer, Dordrecht, pp 140–157
255. Wani PA, Khan MS (2012) Bioremediaiton of lead by a plant growth promoting Rhizobium species RL9. Bacteriology J 2:66–78
256. Wani PA, Khan MS (2013) Nickel detoxification and plant growth promotion by multi metal resistant plant growth promoting Rhizobium species RL9. Bull Environ Contam Toxicol 91:117–124
257. Wani PA, Khan MS, Zaidi A (2007a) Co-inoculation of nitrogen fixing and phosphate solubilizing bacteria to promote growth, yield and nutrient uptake in chickpea. Acta Agron Hung 55:315–323
258. Wani PA, Khan MS, Zaidi A (2007b) Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by green gram plants. Chemosphere 70:36–45
259. Wani PA, Khan MS, Zaidi A (2007c) Synergistic effects of the inoculation with nitrogen fixing and phosphate solubilizing rhizobacteria on the performance of field grown chickpea. J Plant Nutr Soil Sci 170:283–287
260. Wani PA, Khan MS, Zaidi A (2008a) Chromium-reducing and plant growth promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163
261. Wani PA, Khan MS, Zaidi A (2008b) Effect of metal-tolerant plant growth promoting Rhizobium on the performance of pea grown in metal-amended soil. Arch Environ Contam Toxicol 55:33–42
262. Watkin ELJ, O’Hara GW, Glenn AR (1997) Calcium and acid stress interact to affect the growth of Rhizobium leguminosarum bv. trifolii. Soil Biol Biochem 29:1427–1432
263. Watkin ELJ, O’Hara GW, Glenn AR (2003) Physiological responses to acid stress of an acid-soil tolerant and an acid-soil sensitive strain of Rhizobium leguminosarum biovar trifolii. Soil Biol Biochem 35:621–624
264. Wei W, Jiang J, Li X, Wang L, Yang SS (2004) Isolation of salt-sensitive mutants from Sinorhizobium meliloti and characterization of genes involved in salt tolerance. Lett Appl Microbiol 39:278–283
265. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254
266. Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14
267. Wilson PW, Burris RH (1947) The mechanism of biological nitrogen fixation. Bacteriol Rev 11(1):41–73
268. Wittenberg JB, Wittenberg BA, Day DA, Udvardi MK, Appleby CA (1996) Siderophore bound iron in the peribacteroid space of soybean root nodules. Plant Soil 178:161–169
269. Xu J, Xiao-Lin L, Luo L (2012) Effects of engineered Sinorhizobium meliloti on cytokinin synthesis and tolerance of alfalfa to extreme drought stress. Appl Environ Microbiol 78:8056
270. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4
271. Yanni YG, Rizk RY, Abd El-Fattah FK, Squartini A, Corich V, Giacomini A, De Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M, Hollingsworth RI, Martinez-Molina E, Mateos P, Velazquez E, Wopereis J, Triplett E, Umali-Gracia M, Anarna JA, Rolfe BG, Ladha JK, Hill J, Mujoo R, Ng PK, Dazzo FB (2001) The beneficial plant growth promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust J Plant Physiol 28:845–870
272. Yelton MM, Yang SS, Edie SA, Lim ST (1983) Characterization of an effective salt-tolerant fast-growing strain of Rhizobium japonicum. J Gen Microbiol 129:1537–1547
273. Younis M (2007) Responses of Lablab purpureus-Rhizobium symbiosis to heavy metals in pot and field experiments. World J Agric Sci 3:111–122
274. Zafar-ul-Hye M, Ahmad M, Shahzad SM (2013) Synergistic effect of rhizobia and plant growth promoting rhizobacteria on the growth and nodulation of lentil seedlings under axenic conditions. Soil Environ 32:79–86
275. Zahir ZA, Shah MK, Naveed M, Akhter MJ (2010) Substrate dependent auxin production by Rhizobium phaseoli improves the growth and yield of Vigna radiata L. under salt stress conditions. J Microbiol Biotechnol 20:1288–1294
276. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an aird climate. Microbiol Mol Biol Rev 63(4):968–989
277. Zahran HH, Rasanen LA, Karsisto M, Lindstrom K (1994) Alteration of lipopolysaccharide and protein profiles in SDS-PAGE of rhizobia by osmotic and heat stress. World J Microbiol Biotechnol 10:100–105
278. Zhan HJ, Lee CC, Leigh JA (1991) Induction of the second exo-polysaccharide (EPS) in Rhizobium meliloti SU47 by low phosphate concentrations. J Bacteriol 173:7391–7394
279. Zhang XP, Karsisto M, Harper R, LindstroÈm K (1991) Diversity of Rhizobium bacteria isolated from the root nodules of leguminous trees. Int J Syst Evol Bacteriol 41:104–113
280. Zhou K, Binkley D, Doxtader KG (1992) A new method for estimating gross phosphorus mineralization and immobilization rates in soils. Plant Soil 147:243–250
281. Zhu JK (2001) Plant salt tolerance. Plant Sci 6:66–71