Rhizobial Inoculants for Sustainable Agriculture: Prospects and Applications

  • Iqra Naseer
  • Maqshoof Ahmad
  • Sajid Mahmood Nadeem
  • Iqra Ahmad
  • Najm-ul-Seher
  • Zahir Ahmad Zahir
Part of the Soil Biology book series (SOILBIOL, volume 55)


Due to continuous growth of world population, there is dire need of serious efforts and innovative approaches to meet food demands through sustainable production practices, improvement in supply chain, and control of food wastage. All these efforts should ensure the access to nutritious food to all suffering from hunger and malnutrition. Due to intensive crop cultivation and use of synthetic fertilizers, soil health is seriously deteriorating. However, soil fertility can be improved by incorporating legumes in the cropping system and/or use of rhizobial inoculants, which not only increase nitrogen fixation but also improve soil fertility and crop production through several other attributes such as phosphate solubilization, siderophores production, phytohormones production, enzymes synthesis, and exopolysaccharides production. Moreover, these bacteria can be helpful for improvement in crop production on marginal lands due to their tolerance against various biotic and abiotic stresses. All these characteristics make rhizobia equally important for non-legumes as for legumes. The use of rhizobial inoculants can ensure improvement in crop productivity and environment sustainability by enhancing soil fertility and reduction in use of synthetic chemical fertilizers. Present review focuses on important plant growth-promoting mechanisms of rhizobia and the use of these rhizobia for sustainable crop production through improvement in crop nutrition, physiology, productivity, and stress tolerance of crop plants. The potential of the synergistic use of rhizobia with other soil microorganisms for sustainable agriculture has also been elucidated with examples, followed by their future prospects.


Rhizobium Plant growth promotion Sustainable agriculture Soil health and fertility 


  1. Aamir M, Aslam A, Khan MY, Jamshaid MU, Ahmad M, Asghar HN, Zahir ZA (2013) Co-inoculation with Rhizobium and plant growth promoting rhizobacteria (PGPR) for inducing salinity tolerance in mung bean under field condition of semi-arid climate. Asian J Agric Biol 1:17–22Google Scholar
  2. Abdalla AS, Abdelgani ME, Osman AG (2013) Effects of biological and mineral fertilization on yield, chemical composition and physical characteristics of chickpea (Cicer arietinum L.) seeds. Pakistan J Nutrition 12:1–7CrossRefGoogle Scholar
  3. Abrar T (2017) Isolation and characterization of rhizobia from rhizosphere and root nodule of cowpea. IJNRIS 4:1–7Google Scholar
  4. Afzal A, Bano A (2008) Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum). Inter J Agric Biol 10:85–88Google Scholar
  5. Afzal A, Bano A, Fatima M (2010) Higher soybean yield by inoculation with N-fixing and P-solubilizing bacteria. Agron Sustain Dev 30:487–495CrossRefGoogle Scholar
  6. Agegnehu G, Bass AM, Nelson PN, Muirhead B, Wright G, Bird MI (2015) Biochar and biochar-compost as soil amendments: effects on peanut yield soil properties and greenhouse gas emissions in tropical North Queensland, Australia. Agric Ecosyst Environ 213:72–85CrossRefGoogle Scholar
  7. Aguado-Santacruz GAA, Moreno-Gomez BA, Jimenez-Francisco BB, Garcia-Moya EB, Preciado-Ortiz RE (2012) Impact of the microbial siderophores and phytosiderophores on the iron assimilation by plants: a synthesis. Rev Fitotec Mex 35:9–21Google Scholar
  8. Ahemad M, Khan MS (2010) Growth promotion and protection of lentil (Lens esculenta) against herbicide stress by Rhizobium species. Ann Microbiol 60:735–745CrossRefGoogle Scholar
  9. Ahemad M, Khan MS (2011a) Ecotoxicological assessment of pesticides towards the plant growth promoting activities of Lentil (Lens esculentus) specific Rhizobium sp. strain MRL3. Ecotoxicology 20:661–669PubMedCrossRefGoogle Scholar
  10. Ahemad M, Khan MS (2011b) Effect of pesticides on plant growth promoting traits of green gram-symbiont, Bradyrhizobium sp. strain MRM6. Bull Environ Contam Toxicol 86:384–388PubMedCrossRefGoogle Scholar
  11. Ahemad M, Khan MS (2011c) Effect of tebuconazole-tolerant and plant growth promoting Rhizobium isolate MRP1 on pea-Rhizobium symbiosis. Sci Hort 129:266–272CrossRefGoogle Scholar
  12. Ahemad M, Khan MS (2012) Effects of pesticides on plant growth promoting traits of Mesorhizobium strain MRC4. J Saudi Soc Agric Sci 11:63–71Google Scholar
  13. Ahmad M (2011) Microbial ACC-deaminase may improve the efficiency of Rhizobium inoculation in mung bean under salt affected conditions. PhD thesis, Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad, PakistanGoogle Scholar
  14. Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181PubMedCrossRefGoogle Scholar
  15. Ahmad M, Zahir ZA, Asghar HN, Asghar M (2011) Inducing salt tolerance in mung bean through co-inoculation with Rhizobium and PGPR containing ACC-deaminase. Can J Microbiol 57:578–589PubMedCrossRefGoogle Scholar
  16. Ahmad E, Zaidi A, Khan MS, Oves M (2012) Heavy metal toxicity to symbiotic nitrogen-fixing microorganism and host legumes. In: Zaidi A (ed) Toxicity of heavy metals to legumes and bioremediation. Springer, Vienna, pp 29–44CrossRefGoogle Scholar
  17. Ahmad M, Zahir ZA, Nadeem SM, Nazli F, Jamil M, Khalid M (2013a) Field evaluation of Rhizobium and Pseudomonas strains to improve growth, nodulation and yield of mung bean under salt-affected conditions. Soil Environ 32:158–166Google Scholar
  18. Ahmad M, Zahir ZA, Khalid M, Nazli F, Arshad M (2013b) Efficacy of Rhizobium and Pseudomonas strains to improve physiology, ionic balance and quality of mungbean under salt-affected conditions on farmer’s fields. Plant Physiol Biochem 63:170–176PubMedCrossRefGoogle Scholar
  19. Ahmad M, Zahir ZA, Nadeem SM, Nazli F, Jamil M, Jamshaid MU (2014) Physiological response of mung bean to Rhizobium and Pseudomonas based biofertilizers under salinity stress. Pak J Agr Sci 51:557–564Google Scholar
  20. Ahmed E, Holmstrom SJM (2014) Siderophores in environmental research: roles and applications. Microb Biotechnol 7:196–208PubMedPubMedCentralCrossRefGoogle Scholar
  21. Akhal ELMR, Rincon A, Pena C, Lucas T, Mourabit MM, Barrijal S, Pueyo JJ (2013) Effects of salt stress and rhizobial inoculation on growth and nitrogen fixation of three peanut cultivars. Plant Biol 15:415–421PubMedCrossRefGoogle Scholar
  22. Akhtar MS, Siddiqui ZA, Wiemken A (2011) Arbuscular mycorrhizal fungi and rhizobium to control plant fungal diseases. In: Lichtfouse E (ed) Alternative farming systems, biotechnology, drought stress and ecological fertilization, vol 6. Sustainable agriculture reviews. Springer, Dordrecht, pp 263–292CrossRefGoogle Scholar
  23. Alam F, Bhuiyan MAH, Alam SS, Waghmode TR, Kim JP, Lee YB (2015) Effect of Rhizobium sp. BARIRGm901 inoculation on nodulation, nitrogen fixation and yield of soybean (Glycine max) genotype in gray terrace soil. Biosci Biotechnol Biochem 79:1660–1668PubMedCrossRefGoogle Scholar
  24. Alami Y, Achouak WA, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflower by an exopolysaccharide producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66:3393–3398PubMedPubMedCentralCrossRefGoogle Scholar
  25. Al-Falih AMK (2002) Factors affecting the efficiency of symbiotic nitrogen fixation by Rhizobium. Pak J Biol Sci 5:1277–1293CrossRefGoogle Scholar
  26. Allito BB (2015) Soil population and phenotypic characterization of soybean (Glycin max) and haricot bean (Phaseolus vulgaris) nodulating rhizobia at Hawassa and Ziway. Scholarly J Agric Sci 5:30–38Google Scholar
  27. Allito BB, Ewusi-Mensah N, Alemneh AA (2014) Rhizobia strain and host-legume interaction effects on nitrogen fixation and yield of grain legume: a review. Mol Soil Biol 6:1–12Google Scholar
  28. Al-Mughrabi KI (2010) Biological control of fusarium dry rot and other potato tuber diseases using Pseudomonas fluorescens and Enterobacter cloacae. Biol Control 53:280–284CrossRefGoogle Scholar
  29. Andrews M, Lea PJ, Raven JA, Azevedo RA (2009) Nitrogen use efficiency. 3. Nitrogen fixation: genes and costs. Ann Appl Biol 155:1–13CrossRefGoogle Scholar
  30. Angus JJ, Gupta VVSR, Good AJ, Pitson GD (1999) Wheat yield and protein response to anhydrous ammonia (Coldflo) and urea and their effects on soil. Final report on project CSP 169 for the grains research and development corporation. CSIRO, Canberra, p 17Google Scholar
  31. Anjum MA (2011) Substrate dependent microbial biosynthesis of auxins and their effect on growth and yield of mung bean (Vigna radiata L.). PhD thesis, Institute of Soil and Environmental Sciences, University of Faisalabad, Faisalabad, PakistanGoogle Scholar
  32. Argaw A (2016) Effectiveness of Rhizobium inoculation on common bean productivity as determines by inherent soil fertility status. J Crop Sci Biotech 19:311–322CrossRefGoogle Scholar
  33. Argaw A (2018) Integrating inorganic NP application and Bradyrhizobium inoculation to minimize production cost of peanut (Arachis hypogea L.) in eastern Ethiopia. Agric & Food Secur 7:20CrossRefGoogle Scholar
  34. Argaw A, Mnalku A (2017) Vermicompost application as affected by Rhizobium inoculation on nodulation and yield of faba bean (Vicia faba L.). Ethiop J Agric Sci 27:17–29Google Scholar
  35. Argaw A, Muleta D (2017) Effect of genotype-Rhizobium-environment interaction on nodulation and productivity of common bean (Phaseolus vulgaris L.) in eastern Ethiopia. Environ Syst Res 6:1–16CrossRefGoogle Scholar
  36. Arkhipova TN, Prinsen EA, Veselov SU, Martinenko EV, Melentiev LV, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315CrossRefGoogle Scholar
  37. Arora NK, Kang SC, Maheshwari DK (2001) Isolation of siderophores producing strains of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr Sci 81:673–677Google Scholar
  38. Arshad M, Frankenberger WT Jr (2002) Ethylene: agricultural sources and applications. Ann Bot 90(3):424CrossRefGoogle Scholar
  39. Aseri GK, Jain N, Tarafdar JC (2009) Hydrolysis of organic phosphate forms by phosphatases and phytase producing fungi of arid and semi-arid soils of India. JAES 5:564–570Google Scholar
  40. Ashraf M, Berge SH, Mahmood OT (2004) Inoculating wheat seedling with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol Fert Soils 40:157–162Google Scholar
  41. Babu S et al (2015) Synergistic action of PGP agents and Rhizobium spp. for improved plant growth, nutrient mobilization and yields in different leguminous crops. Biocatal Agric Biotechnol 4(4):456–464. CrossRefGoogle Scholar
  42. Badawi FSF, Biomy AMM, Desoky AH (2011) Peanut plant growth and yield as influenced by co-inoculation with Bradyrhizobium and some rhizo-microorganisms under sandy loam soil conditions. AOAS 56(1):17–20Google Scholar
  43. Bai B, Suri VK, Kumar A, Choudhary AK (2016) Influence of dual inoculation of AM fungi and Rhizobium on growth indices, production economics, and nutrient use efficiencies in garden pea (Pisum sativum L.). Commun Soil Sci Plant Anal 47:941–954CrossRefGoogle Scholar
  44. Bambara S, Ndakidemi PA (2009) Effects of Rhizobium inoculation, lime and molybdenum on photosynthesis and chlorophyll content of Phaseolus vulgaris. Afr J Microbiol Res 3(11):791–798Google Scholar
  45. Bano SA, Iqbal SM (2016) Biological nitrogen fixation to improve plant growth and productivity. IJAIR 4(4):15Google Scholar
  46. Barroso CV, Pereira GT, Nahas E (2006) Solubilization of CaHPO4 and AlPO4 by Aspergillus niger in culture media with different carbon and nitrogen sources. Braz J Microbiol 37(4):434–438CrossRefGoogle Scholar
  47. Bellenger JP, Wichard T, Kustka AB, Kraepiel AML (2008) Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores. Nat Geosci 1:243–246CrossRefGoogle Scholar
  48. Beneduzi A, Moreira F, Costa PB, Vargas LK, Lisboa BB, Favreto R, Baldani JI, Passaglia LMP (2013) Diversity and plant growth promoting evaluation abilities of bacteria isolated from sugarcane cultivated in the South of Brazil. Appl Soil Ecol 63:94–104CrossRefGoogle Scholar
  49. Bhatt P, Chandra R (2014) Inoculation effect of Mesorhizobium ciceri and rhizospheric bacteria on nodulation and productivity of chickpea (Cicer arietinum L.) and soil health. Indian J Plant Soil 1:5–10Google Scholar
  50. Bhattacharjya S, Chandra R (2013) Effect of inoculation methods of Mesorhizobium ciceri and PGPR in chickpea (Cicer arietinum L.) on symbiotic traits, yield, nutrient uptake and soil properties. Legume Res 36:331–337Google Scholar
  51. Bhattacharya C, Deshpande B, Pandey B (2013) Isolation and characterization of Rhizobium sp. form root of Legume plant (Pisum sativum) and its antibacterial activity against different bacterial strains. Int gric Food Sci 3(4):138–141Google Scholar
  52. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350PubMedCrossRefGoogle Scholar
  53. Bianco C, Defez R (2010) Improvement of phosphate solubilization and Medicago plant yield by an indole-3-acetic acid-overproducing strain of Sinorhizobium meliloti. Appl Environ Microbiol 76:4626–4632PubMedPubMedCentralCrossRefGoogle Scholar
  54. Biate DL, Kumar LV, Ramadoss D, Kumari A, Naik S, Reddy KK, Annapurna K (2014) Genetic diversity of soybean root nodulating bacteria. In: Maheshwari DK (ed) Bacterial diversity in sustainable agriculture. Springer, Heidelberg, pp 131–145CrossRefGoogle Scholar
  55. 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 74:874–880PubMedCrossRefGoogle Scholar
  56. Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503PubMedCrossRefGoogle Scholar
  57. Braud A, Hoegy F, Jezequel K, Lebeau T, Schalk IJ (2009) New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine–iron uptake pathway. Environ Microbiol 11:1079–1091PubMedCrossRefGoogle Scholar
  58. Broos K, Beyens H, Smolders E (2005) Survival of rhizobia in soil is sensitive to elevated zinc in the absence of the host plant. Soil Biol Biochem 37:573–579CrossRefGoogle Scholar
  59. Bumunang EW, Babalola OO (2014) Characterization of Rhizobacteria from field grown genetically modified (GM) and non-GM Maizes. Braz Arch Biol Technol 57:1–8CrossRefGoogle Scholar
  60. Burgess CM, Smid EJ, Sinderen D (2009) Bacterial vitamin B2, B11 and B12 overproduction: an overview. Int J Food Microbiol 133:1–7PubMedCrossRefGoogle Scholar
  61. Carson KC, Meyer JM, Dillworth MJ (2000) Hydroxamate siderophores of root nodule bacteria. Soil Biol Biochem 32:11–21CrossRefGoogle Scholar
  62. Cassan F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna C (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(1):28–35CrossRefGoogle Scholar
  63. Castellane TCL, Otoboni AMMB, Lemos EGM (2015) Characterization of exopolysaccharides produced by rhizobia species. R Bras Ci Solo 39:1566–1575CrossRefGoogle Scholar
  64. Castro S, Furlan A, Llanes AA, Luna V (2012) International scholarly research network. ISRN Agronomy. CrossRefGoogle Scholar
  65. Cerezini P, Kuwanoa BH, Santosb MBD, Terassic F, Hungriad M (2016) Strategies to early nodulation in soybean under drought. Marco Antonio Nogueirad Field Crop Res 196:160–167CrossRefGoogle Scholar
  66. Chalk PM, Souza RDF, Urquiaga S, Alves BJR, Boddy RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol Biochem 38:2944–2951CrossRefGoogle Scholar
  67. Chandra R, Pareek N (2015) Comparative performance of plant growth promoting rhizobacteria with rhizobia on symbiosis and yields in urdbean and chickpea. J Food Legumes 28:86–89Google Scholar
  68. 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 38:128–130CrossRefGoogle Scholar
  69. 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 221:167–179CrossRefGoogle Scholar
  70. Cheung KH, Gu JD (2007) Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior Biodegradation 59:8–15CrossRefGoogle Scholar
  71. Chi F, Yang P, Han F, Jing Y, Shen S (2010) Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021. Proteomics 10:1861–1874PubMedCrossRefGoogle Scholar
  72. Clayton GW, Rice WA, Lupwayi NZ, Johnston AM, Lafond GP, Grant CA, Walley F (2004) Inoculant formulation and fertilizer nitrogen effects on field pea: nodulation, N fixation, and nitrogen partitioning. Can J Plant Sci 84:79–88CrossRefGoogle Scholar
  73. Crossley RA, Gaskin DGH, Holmes K, Mulholland F, Wells JM, Kelly DJ, van Vliet AHM, Walton NJ (2007) Riboflavin biosynthesis is associated with assimilatory ferric reduction and iron acquisition by Campylobacter jejuni. J Appl Environ Microbiol 73(24):7819–7825CrossRefGoogle Scholar
  74. D’Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R–105RPubMedCrossRefGoogle Scholar
  75. Dakora FD (2003) Defining new roles for plant and rhizobial molecules in sole and mixed plant cultures involving symbiotic legumes. New Phytol 58:39–49CrossRefGoogle Scholar
  76. Das S, Pareek N, Raverkar KP, Chandra R, Kaustav A (2012) Effectiveness of micronutrient application and Rhizobium inoculation on growth and yield of chickpea. Int J Agric Environ Biotech 5:445–452Google Scholar
  77. Dazzo FB, Yanni YG (2006) The natural rhizobium-cereal crop association as an example of plant-bacterial interaction. In: Uphoff N, Ball AS, Fernandes E, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P, Sanginga N, Thies J (eds) Biological approaches to sustainable soil systems. CRC, Boca Raton, FL, pp 109–127CrossRefGoogle Scholar
  78. 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 379–380CrossRefGoogle Scholar
  79. De Smet I, Zhang H, Inze D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439PubMedCrossRefGoogle Scholar
  80. Denison RF, Kiers ET (2011) Life histories of symbiotic rhizobia and mycorrhizal fungi. Curr Biol 21:R775–R785PubMedCrossRefGoogle Scholar
  81. Deshwal VK, Chaubey A (2014) Isolation and characterization of Rhizobium leguminosarum from root nodule of Pisum sativum L. J Academia Industrial Res 2:464–467Google Scholar
  82. Dhami N, Prasad B (2009) Increase in root nodulation and crop yield of soybean by native Bradyrhizobium japonicum strains. J Plant Sci 6:1–3Google Scholar
  83. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149CrossRefGoogle Scholar
  84. Donot F, Fontana A, Baccou JC, Schorr-Galindo S (2012) Microbial exopolysaccharides: main examples of synthesis, excretion, genetics and extraction. Carbohydr Polym 87:951–962CrossRefGoogle Scholar
  85. Duan J, Muller KM, Charles TC, Vesely S, Glick BR (2009) 1-Aminocyclopropane-1carboxylate (ACC) deaminase gene in Rhizobium from Southern Saskatchewan. Microbial Ecol 57:423–436CrossRefGoogle Scholar
  86. 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: The “26th Southern Conservation Tillage Conference for Sustainable Agriculture”. J.S. Mckimmon Centre, North Carolina State University, Raleigh, North Carolina, 8–9 June 2004, pp 58–66Google Scholar
  87. El-Batanony NH, Massoud ON, Mazen MM, Abd El-Monium MM (2007) The inhibitory effects of cultural filtrates of some wild rhizobium spp. on some faba bean root rot pathogens and their antimicrobial synergetic effect when combined with Arbuscular Mycorrhiza (AM). World J Agric Sci W J Agric 3:721–730Google Scholar
  88. Elkoca E, Turan M, Donmez MF (2010) Effects of single, dual and triple inoculations with Bacillus subtilis, Bacillus megaterium and Rhizobium leguminosarum bv. phaseoli on nodulation, nutrient uptake, yield and yield parameters of common bean (Phaseolus vulgaris L. cv. ‘elkoca-05’). J Plant Nutr 33:2104–2119CrossRefGoogle Scholar
  89. 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 102:703–709PubMedCrossRefGoogle Scholar
  90. Fatima Z, Bano A, Sial R, Aslam M (2008) Response of chickpea to plant growth regulators on nitrogen fixation and yield. Pak J Bot 40:2005–2013Google Scholar
  91. Fernandez LA, Zalpa P, Gomez MA, Sagardoy MA (2007) Phosphate solubilization activity of bacterial strains in soil and their effect on soybean growth under greenhouse conditions. Biol Fert Soils 43:805–809CrossRefGoogle Scholar
  92. Ferri GC, Braccini AL, Anghinoni FBG, Pereira LC (2017) Effects of associated co-inoculation of Bradyrhizobium japonicum with Azospirillum brasilense on soybean yield and growth. AJAR 12(1):6–11Google Scholar
  93. Figueiredo MVB, Burity HA, Martınez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182–188CrossRefGoogle Scholar
  94. Fituma T, Tamado T, Anteneh A (2018) Effect of inoculating Bradyrhizobium on phosphorus use efficiency and nutrient uptake of soybean intercropped with sugarcane in calcareous soil of metehara, central rift valley, Ethiopia. Adv Crop Sci Tech 28(1):17–32Google Scholar
  95. Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the house of biofilm cells. J Bacteriol 189:7945–7947PubMedPubMedCentralCrossRefGoogle Scholar
  96. Flores-Felix JD, Menendez E, Rivera LP (2012) Use of Rhizobium leguminosarum as a potential biofertilizer for Lactuca sativa and Daucus carota crops. J Plant Nutr Soil Sci 176:876–882CrossRefGoogle Scholar
  97. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300PubMedPubMedCentralCrossRefGoogle Scholar
  98. Galindo FS, Filho TMC, Salatier B, Ludkiewicz MGZ, Rosa PAL, Tritapepe CA (2018) Technical and economic viability of co-inoculation with Azospirillum brasilense in soybean cultivars in the Cerrado. Rev Bras Eng Agríc Ambient 22(1):51–56CrossRefGoogle Scholar
  99. Gao X, Lu X, Wu M, Zhang H, Pan R, Tian J, Li S, Liao H (2012) Co-inoculation with rhizobia and AMF inhibited soybean red crown rot: from field study to plant defense-related gene expression analysis. PLoS One 7(3):e33977PubMedPubMedCentralCrossRefGoogle Scholar
  100. Garcia-Fraile P, Carro L, Robledo M (2012) Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans. PLoS One 7(5):e38122. CrossRefPubMedPubMedCentralGoogle Scholar
  101. Gaur R, Tiwari S, Chauhan RK, Singh R, Shukla R (2017) Integrated effect of Rhizobium and Azotobacter cultures on the leguminous crop black gram (Vigna mungo). Adv Crop Sci Tech doi 5(3):289. CrossRefGoogle Scholar
  102. Gauri SAK, Bhatt RB, Pant S, Bedi MK, Naglot A (2011) Characterization of Rhizobium isolated from root nodules of Trifolium alexandrinum. J Agric Technol 7:1705–1723Google Scholar
  103. Geetha SJ, Joshi SJ (2013) Engineering Rhizobial bioinoculants: a strategy to improve iron nutrition. Sci World J 2013:1–15Google Scholar
  104. Geneva M, Zehirov G, Djonova E, Kaloyanova N, Georgiev G, Stancheva I (2006) The effect of inoculation of pea plants with Mycorrhizal fungi and Rhizobium on nitrogen and phosphorus assimilation. Plant Soil Environ 52(10):435–440CrossRefGoogle Scholar
  105. Giller KE (2001) Nitrogen fixation in tropical cropping systems. CAB International, WallingfordCrossRefGoogle Scholar
  106. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:15. CrossRefGoogle Scholar
  107. Goggin DE, Steadman KJ, Emery RJN, Farrow SC, Benech-Arnold RL, Powles SB (2009) ABA inhibits germination but not dormancy release in mature imbibed seeds of Lolium rigidum gaud. J Exp Bot 60:3387–3396. CrossRefPubMedPubMedCentralGoogle Scholar
  108. Gontijo JB, Andrade GVS, Baldotto MA, Baldotto LEB (2018) Bioprospecting and selection of growth-promoting bacteria for Cymbidium sp. Orchids Sci Agric 75(5):368–374CrossRefGoogle Scholar
  109. Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CCL, Krishnamurthy L (2014) Plant growth promoting rhizobia: challenges and opportunities. Biotechnology 3:1–23Google Scholar
  110. Goswami D, Pithwa S, Dhandhukia P, Thakker JN (2014) Delineating Kocuria turfanensis 2M4 as a credible PGPR: a novel IAA-producing bacteria isolated from saline desert. J Plant Interact 9:566–576CrossRefGoogle Scholar
  111. Grichko VP, Glick BR (2001) Amelioration of flooding stress by ACC deaminase containing plant growth promoting bacteria. Plant Physiol Biochem 39:11–17CrossRefGoogle Scholar
  112. 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 27:1231–1240CrossRefGoogle Scholar
  113. Guo Y, Ni Y, Huang J (2010) Effects of rhizobium, arbuscular mycorrhiza and lime on nodulation, growth and nutrient uptake of lucerne in acid purplish soil in China. Trop Grasslands 44:109–114Google Scholar
  114. 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 247–248CrossRefGoogle Scholar
  115. Hahn L, Sa ELS, Filho BDO, Machado RG, Damasceno RG, Giongo A (2016) Rhizobial inoculation, alone or coinoculated with Azospirillum brasilense, promotes growth of wetland rice. Rev Bras Cienc Solo 40:e0160006CrossRefGoogle Scholar
  116. Haque MA, Bala P, Azad AK (2014) Performance of lentil varieties as influenced by different Rhizobium inoculations. Bangladesh Agron J 17:41–46CrossRefGoogle Scholar
  117. Hatice O, Omer F, Erdal E, Faik K (2008) The determination of symbiotic effectiveness of Rhizobium strains isolated from wild chickpeas collected from high altitudes in Erzurum. Turk J Agric For 32:241–248Google Scholar
  118. Havugimana E, Bhople BS, Byiringiro E, Mugabo BP (2016) Role of dual inoculation of Rhizobium and Arbuscular Mycorrhizal (AM) fungi on pulse crops production. J Sci Tech 13(1):1–7Google Scholar
  119. Htwe ZA, Seinn MM, Moe M, Yamakawa K (2018) Effects of co-inoculation of Bradyrhizobium elkanii BLY3-8 and Streptomyces griseoflavus P4 on Rj 4 soybean varieties. Soil Sci Plant Nutr 64(4):449–454. CrossRefGoogle Scholar
  120. Huang HC, Erickson RS (2007) Effect of seed treatment with Rhizobium leguminosarum on pythium damping-off, seedling height, root nodulation, root biomass, shoot biomass, and seed yield of pea and lentil. J Phytopathol 155:31–37CrossRefGoogle Scholar
  121. Hungria M, Kaschuk G (2014) Regulation of N2 fixation and NO3−/NH4 + assimilation in nodulated and N-fertilized Phaseolus vulgaris L. exposed to high temperature stress. Environ Exp Bot 98:32–39CrossRefGoogle Scholar
  122. Hussain MI, Akhtar MJ, Asghar HN, Ahmad M (2011) Growth, nodulation and yield of mash bean (Vigna mungo L.) as affected by Rhizobium inoculation and soil applied L-tryptophan. Soil Environ 30:13–17Google Scholar
  123. Hussain MB, Zahir ZA, Asghar HN, Asghar M (2014) Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat? Int J Agric Biol 16:3–13Google Scholar
  124. Hussain MB, Mahmood S, Ahmed N, Nawaz H (2018) Rhizobial inoculation for improving growth physiology, nutrition and yield of maize under drought stress conditions. Pak J Bot 50(5):1681–1689Google Scholar
  125. Islam MR, Madhaiyan M, Deka HPB, Yim W, Lee G, Saravanan VS, Fu Q, Hu H, Sa T (2009) Characterization of plant growth-promoting traits of free-living diazotrophic bacteria and their inoculation effects on growth and nitrogen uptake of crop plants. J Microbiol Biotechnol 19(10):1213–1222PubMedGoogle Scholar
  126. Janczarek M, Rachwał K, Cieśla J, Ginalska G, Bieganowski A (2015) Production of exopolysaccharide by Rhizobium leguminosarum bv. trifolii and its role in bacterial attachment and surface properties. Plant Soil 388:211–227CrossRefGoogle Scholar
  127. Jha CK, Patel B, Sarf M (2012) Stimulation of the growth of Jatropha curcas by the plant growth bacterium Enterobacter cancerogenus MSA2. World J Microbiol Biotechnol 28:891–899PubMedCrossRefGoogle Scholar
  128. Jimenez-Gomez A, Flores-Felix JD, Garcia-Fraile P, Mateos PF, Menendez E, Velazquez E, Rivas R (2018) Probiotic activities of Rhizobium laguerreae on growth and quality of spinach. Sci Rep 8(1):295. CrossRefPubMedPubMedCentralGoogle Scholar
  129. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633PubMedPubMedCentralCrossRefGoogle Scholar
  130. Kamran S, Shahid I, Baig DN, Rizwan M, Malik KA, Mehnaz S (2017) Contribution of zinc solubilizing bacteria in growth promotion and zinc content of wheat. Front Microbiol 8:2593. CrossRefPubMedPubMedCentralGoogle Scholar
  131. Kang BR, Yang KY, Cho BH, Han TH, Kim IS, Lee MC, Anderson AJ, Kim YC (2006) Production of indole-3-acetic acid in the plant-beneficial strain Pseudomonas chlororaphis O6 is negatively regulated by the global sensor kinase GacS. J Current Microbiol 52:473–476CrossRefGoogle Scholar
  132. Kang X, Yu X, Zhang Y, Cui Y, Tu W, Wang Q, Li Y, Hu L, Gu Y, Zhao K, Xiang Q, Chen Q, Ma M, Zou L, Zhang X, Kang J (2018) Inoculation of Sinorhizobium saheli YH1 heads to reduced metal uptake for Leucaena leucocephala grown in mine tailings and metal-polluted soils. Front Microbiol 9:1–13CrossRefGoogle Scholar
  133. Karpagam T, Nagalakshmi PK (2014) Isolation and characterization of phosphate solubilizing microbes from agricultural soil. J Curr Microbiol App Sci 3(3):601–614Google Scholar
  134. Kaur N, Sharma P, Sharma S (2015) Co-inoculation of Mesorhizobium sp. and plant growth promoting rhizobacteria Pseudomonas sp. as bio-enhancer and bio-fertilizer in chickpea (Cicer arietinum L.). ARCC Res 38:367–374Google Scholar
  135. Khaitov B, Kurbonov A, Abdiev A, Adilov M (2016) Effect of chickpea in association with Rhizobium to crop productivity and soil fertility. Eurasian J Soil Sci 5:105–112CrossRefGoogle Scholar
  136. Khalid M, Arshad M, Zahir ZA (2006) Phytohormones: microbial production and application. In: Uphoff N, Ball AS, Palm C, Fernandes E, Pretty J, Herren H, Sanchez P, Husson O, Sanginga N, Laing M, Thies J (eds) Biological approaches to sustainable soil systems. Taylor & Francis, Boca Raton, pp 207–220CrossRefGoogle Scholar
  137. Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi—current perspective. Arch Agron Soil Sci 56:73–98CrossRefGoogle Scholar
  138. Khan MY, Asghar HN, Jamshaid MU, Akhtar MJ, Zahir ZA (2013) Effect of microbial inoculation on wheat growth and phyto-stabilization of chromium contaminated soil. Pak J Bot 45:27–34Google Scholar
  139. Khan MS, Zaidi A, Ahmad E (2014) Mechanism of phosphate solubilization and physiological functions of phosphate-solubilizing microorganisms. In: Khan M, Zaidi A, Musarrat J (eds) Phosphate solubilizing microorganisms. Springer Cham, pp 31-62Google Scholar
  140. Khanna V, Sharma P, Sharma S (2011) Studies on synergism between Rhizobium and plant growth promoting rhizobacteria in lentil (Lens culinaris Medikus). J Food Legume 24(2):158–159Google Scholar
  141. Kisiala A, Laffont C, Emery RJN, Frugier F (2013) Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonnodulating strains. Mol Plant-Microbe Interact 26:1225–1231PubMedCrossRefGoogle Scholar
  142. Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152PubMedCrossRefGoogle Scholar
  143. Korir H, Mungai NW, Thuita M, Hamba Y, Masso Y (2017) Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil front. Plant Sci 8:141. CrossRefGoogle Scholar
  144. Koskey G, Mburu SW, Njeru EM, Kimiti JM, Ombori O, Maingi JM (2017) Potential of native rhizobia in enhancing nitrogen fixation and yields of climbing beans (Phaseolus vulgaris L.) in contrasting environments of Eastern Kenya. Front Plant Sci 8:1–12CrossRefGoogle Scholar
  145. Krishnan HB, Kang BR, Krishnan AH, Kil Kim KY, Kim YC (2007) Rhizobium etli USDA9032 engineered to produce a phenazine antibiotic inhibits the growth of fungal pathogens but is impaired in symbiotic performance. Appl Environ Microbiol 73:327–330PubMedCrossRefGoogle Scholar
  146. Krujatz F, Haarstrick A, Neortemann B, Greis T (2011) Assessing the toxic effects of nickel, cadmium and EDTA on growth of the plant growth-promoting rhizobacterium Pseudomonas brassicacearum. Water Air Soil Pollut 223(3):1281–1293. CrossRefGoogle Scholar
  147. Kulasooriya SA, Ekanayake EMHGS, Kumara RKGK, Bandar AMS (2017) Rhizobial inoculation of Trifolium repens L. in Sri Lanka. J Natn Sci Foundation Sri Lanka 45:361–366CrossRefGoogle Scholar
  148. Kumar H, Bajpai VK, Dubey RC (2010) Wilt disease management and enhancement of growth and yield of Cajanus cajan (L) var. Manak by bacterial combinations amended with chemical fertilizer. Crop Protect 29:591–598CrossRefGoogle Scholar
  149. Kumar D, Arvadiya LK, Kumawat AK, Desai KL, Patel TU (2014) Yield, protein content, nutrient content and uptake of chickpea (Cicer arietinum L.) as influenced by graded levels of fertilizers and bio-fertilizers. Res J Chem Environ Sci 2:60–64Google Scholar
  150. Kyei-Boahen S, Slinkard AE, Walley FL (2002) Evaluation of Rhizobial inoculation methods for chickpea. J Agron 94:851–859CrossRefGoogle Scholar
  151. Laabas S, Boukhatem ZS, Bouchiba Z, Benkritly S, Abed NE, Yahiaoui H, Bekki A, Tsaki H (2017) Impact of single and co-inoculations with Rhizobial and PGPR isolates on chickpea (Cicer arietinum) in cereal-growing zone soil. J Plant Nutr 40(11):1616–1626CrossRefGoogle Scholar
  152. Leytem AB, Mikkelson RL (2005) The nature of phosphorus in calcareous soils. Better Crops 89:11–13Google Scholar
  153. Liu Y, Wu L, Baddeley JA, Watson CA (2011) Models of biological nitrogen fixation of legumes. A review. Agron Sustain Dev 31:155–172CrossRefGoogle Scholar
  154. Liu H, Wang X, Qi H, Wang Q, Chen Y, Li Q (2017) The infection and impact of Azorhizobium caulinodans ORS571 on wheat (Triticum aestivum L.). PLoS One 12(11):e0187947PubMedPubMedCentralCrossRefGoogle Scholar
  155. Lodwig EM, Poole PS (2003) Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci 22:37–38CrossRefGoogle Scholar
  156. Lodwig EM, Hosie AHF, Bourdes A, Findlay K, Allaway D, Karunakaran R, Downie JA, Poole PS (2003) Amino-acid cycling drives nitrogen fixation in the legume- Rhizobium symbiosis. Nature 422:722–726PubMedCrossRefPubMedCentralGoogle Scholar
  157. Ma W, Carles TC, Glick BR (2004) Expression of an exogenous 1-aminocyclopropane carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Appl Environ Microbiol 70(10):5891–5897PubMedPubMedCentralCrossRefGoogle Scholar
  158. Maheshwari DK, Chandra S, Choure K, Dubey RC (2007) Rhizosphere competent Mesorhizobium loti mp6 induces root hair curling, inhibits Sclerotinia sclerotiorum and enhances growth of Indian mustard (Brassica campestris). BJM 38:124–130Google Scholar
  159. Makoi JH, Bambara S, Ndakidemi PA (2013) Rhizobium inoculation and the supply of molybdenum and lime affect the uptake of macroelements in common bean (P. vulgaris L.) plants. Aust J Crop Sci 7:784–793Google Scholar
  160. Malisorn K, Prasarn C (2014) Isolation and characterization of Rhizobium spp. from root of legume plants species. Agron J 4:157–160Google Scholar
  161. Manasa K, Reddy SR, Triveni S (2017) Characterization of potential PGPR and antagonistic activities of Rhizobium isolates from different rhizosphere soils. J Pharmacogn Phytochem 6(3):51–54Google Scholar
  162. Mandri B, Drevon J, Bargaz A, Oufdou K, Faghire M, Plassard C, Payer H, Goulam C (2012) Interactions between common bean genotypes and rhizobia strains isolated from Moroccan soils for growth, phosphatase and phytase activities under phosphorus deficiency conditions. J Plant Nutr 35:1477–1490CrossRefGoogle Scholar
  163. Maougal RT, Brauman A, Plassard C, Abadie J, Djekoun J, Drevon JJ (2014) Bacterial capacities to mineralize phytate increase in the rhizosphere of nodulated common bean (Phaseolus vulgaris) under P deficiency. Eur J Soil Biol 62:8–14CrossRefGoogle Scholar
  164. Marchiol L, Assolari S, Sacco P, Zerbi G (2004) Phytoextraction of heavy metals by canola (Brassica napus) and radish (Raphanus sativus) grown on multi contaminated soil. Environ Pollut 132:21–27PubMedCrossRefGoogle Scholar
  165. Marczak M, Mazur A, Koper P, Żebracki K, Genes AS (2017) Synthesis of rhizobial exopolysaccharides and their importance for symbiosis with legume plants. Genes 8(12):360. CrossRefPubMedCentralPubMedGoogle Scholar
  166. Mark BB, Megias M, Ollero FJ, Araujo RS (2015) Maize growth promotion by inoculation with Azospirillum brasilense and metabolites of Rhizobium tropici enriched on lipo-chitooligosaccharides (LCOs). AMB Express 5:71CrossRefGoogle Scholar
  167. Martyniuk S, Kozieł M, Gałązk A (2018) Response of pulses to seed or soil application of rhizobial inoculants. Ecol Chem Eng S 25:323–329Google Scholar
  168. Masalha J, Kosegarten H, Elmaci O, Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fertil Soils 30:433–439CrossRefGoogle Scholar
  169. Masciarelli O, Llanes A, Luna V (2014) A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol Res 169(7–8):609–661PubMedCrossRefPubMedCentralGoogle Scholar
  170. Matiru VN, Dakora FD (2005) The rhizosphere signal molecule lumichrome alters seedling development in both legumes and cereals. New Phytol 166:439–444PubMedCrossRefPubMedCentralGoogle Scholar
  171. McAdam EL, Reid JB, Foo E (2018) Gibberellins promote nodule organogenesis but inhibit the infection stages of nodulation. J Exp Bot 69:2117–2130PubMedPubMedCentralCrossRefGoogle Scholar
  172. McLaughlin MJ, McBeath TM, Smernik R, Stacey SP, Ajiboye B, Guppy C (2011) The chemical nature of P accumulation in agricultural soils-implications for fertilizer management and design: an Australian perspective. Plant Soil 349:69–87CrossRefGoogle Scholar
  173. Mehboob I, Naveed M, Zahir ZA (2009) Rhizobial association with non-legumes: mechanisms and applications. Crit Rev Plant Sci 28:432–456CrossRefGoogle Scholar
  174. Mehboob I, Zahir ZA, Arshad M, Tanveer A, Farroq-E-Azam (2011) Growth promoting activities of different Rhizobium sp. in wheat. Pak J Bot 43:1643–1650Google Scholar
  175. Messele B, Pant LM (2012) Effects of inoculation of Sinorhizobium ciceri and phosphate solubilizing bacteria on nodulation, yield and nitrogen and phosphorus uptake of chickpea (Cicer arietinum L.) in Shoa Robit area. J Biofert Biopest 3:5. CrossRefGoogle Scholar
  176. Mia MD, Shamsuddin ZH, Wahab Z, Marziah M (2005) High yielding and quality banana production through plant growth promoting rhizobacterial (PGPR) inoculation. Fruits 60:179–185CrossRefGoogle Scholar
  177. Mirza BS, Mirza MS, Bano A, Malik KA (2007) Coinoculation of chickpea with Rhizobium isolates from roots and nodules and phytohormones-producing Enterobacter strains. Austr J Exp Agr 47:1008–1015CrossRefGoogle Scholar
  178. Mishra P, Bisht K, Jeevanandan K, Kumar S, Bisht JK, Bhatt JC (2014) Synergistic effect of inoculating plant growth-promoting Pseudomonas spp. and Rhizobium leguminosarum-FB1 on growth and nutrient uptake of raj mash (Phaseolus vulgaris L.). Arch Agron Soil Sci 60:799–815CrossRefGoogle Scholar
  179. Mohammed H, Sahid IB (2016) Evaluation of Rhizobium inoculation in combination with phosphorus and nitrogen fertilization on groundnut growth and yield. J Agron 15:142–146CrossRefGoogle Scholar
  180. Monteiro NK, Aranda-Selverio G, Exposti DTD, Silva MLC, Lemos EGM, Campanharo JC, Silveira JLM (2012) Caracterização química dos géis produzidos pelas bactérias diazotróficas Rhizobium tropici e Mesorhizobium sp. Química Nova 35(4):705–708CrossRefGoogle Scholar
  181. Morrone D, Chambers J, Lowry L, Kim G, Anterola A, Bender K, Peters RJ (2009) Gibberellin biosynthesis in bacteria: separate ent-copalyl diphosphate and entkaurene synthases in Bradyrhizobium japonicum. FEBS Lett 583:475–480PubMedCrossRefGoogle Scholar
  182. Mouradi M, Farissi M, Khadraji A, Makoudi B, Ghoulam C (2018) Biochemical and antioxidant proprieties associated with the adaptation of faba bean (Vicia faba L.) rhizobia symbiosis to phosphorus deficit. J Mater Environ Sci 9(5):1574–1581Google Scholar
  183. 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. Eur J Agron 22:209–216CrossRefGoogle Scholar
  184. Mujahidy SKMDJ, Hassan M, Rahman M, Rashid ANM (2013) Isolation and characterization of Rhizobium spp. and determination of their potency for growth factor production. IRJOB 4(7):117–123Google Scholar
  185. Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7:869–885PubMedPubMedCentralCrossRefGoogle Scholar
  186. Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can J Microbiol 53:1141–1149PubMedCrossRefGoogle Scholar
  187. Naidu VSGR, Panwar JDS, Annapurna K (2004) Effect of synthetic auxins and Azorhizobium caulinodans on growth and yield of rice. Indian J Microbiol 44:211–213Google Scholar
  188. 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 2:353–368CrossRefGoogle Scholar
  189. Nosheen A, Bano A (2014) Potential of plant growth promoting rhizobacteria and chemical fertilizers on soil enzymes and plant growth. Pak J Bot 46:1521–1530Google Scholar
  190. Nyoki D, Ndakidemi PA (2014) Effects of phosphorus and Bradyrhizobium japonicum on growth and chlorophyll content of cowpea. Am J Exp Agric 4:1120–1136Google Scholar
  191. Ogutcu H, Algur OF, Elkoca E, Kantar F (2008) The determination of symbiotic effectiveness of Rhizobium strains isolated from wild chickpea collected from high altitudes in Erzurum. Turk J Agric For 32:241–248Google Scholar
  192. Oldroyd GED (2007) Nodules and hormones. Science 315(5808):52–53PubMedCrossRefGoogle Scholar
  193. Owino WO, Manabe Y, Mathooko FM, Kubo Y, Inaba A (2006) Regulatory mechanisms of ethylene biosynthesis in response to various stimuli during maturation and ripening in fig fruit (Ficus carica L.). Plant Physiol Biochem 44:335–342PubMedCrossRefGoogle Scholar
  194. Patel A, Vyas RV, Mankad M, Subhash N (2017) Isolation and biochemical characterization of rhizobia from rice rhizosphere and their effect on rice growth promotion. Int J Pure App BioSci 5(4):441–451CrossRefGoogle Scholar
  195. Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220PubMedCrossRefGoogle Scholar
  196. Paulucci NS, Gallarato LA, Reguera YB, Vicario JC (2015) Arachis hypogaea PGPR isolated from Argentine soil modifies its lipids components in response to temperature and salinity. Microbiol Res 173:1–9PubMedCrossRefGoogle Scholar
  197. Picazevicz AAC, Kusdra JF, Moreno ADL (2017) Maize growth in response to Azospirillum brasilense, Rhizobium tropici, molybdenum and nitrogen. Rev Bras Eng Agric Ambient 21(9):623–627CrossRefGoogle Scholar
  198. Pierson EA, Weller DM (1994) Use of mixtures of fluorescent pseudomonads to suppress take-all and improve the growth of wheat. J Phytopathol 84:940–947CrossRefGoogle Scholar
  199. Prabha C, Maheshwari DK, Bajpai VK (2013) Diverse role of fast growing rhizobia in growth promotion and enhancement of psoralen content in Psoralea corylifolia. Phcog Mag 9:57–65CrossRefGoogle Scholar
  200. Qurashi AW, Sabri AN (2012) Bacterial exopolysaccharides and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J Microbiol 43:1183–1191PubMedPubMedCentralCrossRefGoogle Scholar
  201. Raja D, Takankhar VJ (2018) Response of liquid biofertilizers (Bradyrhizobium and PSB) on nutrient content in soybean. IJCMAS 7(5):3701–3706Google Scholar
  202. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149PubMedCrossRefGoogle Scholar
  203. Rao BP, Sudharsan K, Reshma CH, Sekaran G, Mandal AB (2013) Characterization of exopolysaccharide from Bacillus amyloliquefaciens BPRGS for its Bioflocculant activity. Int J Sci Eng Res 4(10):1696–1704Google Scholar
  204. Ravikumar R (2012) Growth effects of Rhizobium inoculation in some Legume plants. Int J Curr Sci 1:1–6Google Scholar
  205. Rawat AK, Rao DLN, Sahu RK (2013) Effect of soybean inoculation with Bradyrhizobium and wheat inoculation with Azotobacter on their productivity and N turnover in a Vertisol. Arch Agron Soil Sci 59:1559–1571CrossRefGoogle Scholar
  206. Raychaudhuri N, Das SK, Chakraborty PK (2005) Symbiotic effectiveness if siderophore overproducing mutant of Mesorhizobium ciceri. Pol J Microbiol 54:37–41PubMedGoogle Scholar
  207. Raymond K, Dertz EM (2004) Biochemical and physical properties of siderophores. In: Crosa JM, Mey AM, Pyne SM (eds) Iron transport in Bacteria. ASM, Washington, DC, pp 1–16Google Scholar
  208. Remans R, Beebe S, Blair M, Manrique G, Tovar E, Rao I, Croonenborghs A, Torres-Gutierrez R, El-Howeity M, Michiels J, Vanderleyden J (2007) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161CrossRefGoogle Scholar
  209. Rfaki A, Nassiri L, Ibijbijen J (2015) Isolation and characterization of phosphate solubilizing bacteria from the rhizosphere of faba bean (Vicia faba L.) in meknes region, Morocco. BMRJ 6(5):247–254CrossRefGoogle Scholar
  210. Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996PubMedPubMedCentralCrossRefGoogle Scholar
  211. Roberts R, Jackson RW, Mauchline TH, Hirsh PR, Shaw LJ, Doring TF et al (2017) Is there sufficient Ensifer and Rhizobium species diversity in UK farmland soils to support red clover (Trifolium pretense), white clover (T. repens), lucerne (Medicago sativa) and black medic (M. lupulina)? Appl Soil Ecol 120:35–43PubMedPubMedCentralCrossRefGoogle Scholar
  212. Rodrigues C, Laranjo M, Oliveira S (2006) Effect of heat and pH stress in the growth of chickpea mesorhizobia. Curr Microbiol 53:1–7PubMedCrossRefGoogle Scholar
  213. Rodrigues AC, Vendruscolo CT, Moreira ADS (2015) Rhizobium tropici exopolysaccharides as carriers improve the symbiosis of cowpea-Bradyrhizobium Paenibacillus. Afr J Microbiol Res 9(37):2037–2050CrossRefGoogle Scholar
  214. Rodriguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21CrossRefGoogle Scholar
  215. Rodriguez-Gacio MC, Matilla-Vázquez MA, Matilla AJ (2009) Seed dormancy and ABA signaling: the breakthrough goes on. Plant Signal Behav 4:1035–1048CrossRefGoogle Scholar
  216. Rodriguez-Navarro DN, Oliver IM, Contreras MA, Ruiz-Sainz JE (2010) Soybean interactions with soil microbes, agronomical and molecular aspects. Agron Sustain Dev 31:173–190CrossRefGoogle Scholar
  217. Rokhzadi A, Toashih V (2011) Nutrient uptake and yield of chickpea (Cicer arietinum L.) inoculated with plant growth promoting rhizobacteria. Aust J Crop Sci 1:44–48Google Scholar
  218. Romdhane SB, Trabelsi M, Aouani ME, Lajudie P, Mhamdi R (2009) The diversity of rhizobia nodulating chickpea (Cicer arietinum) under water deficiency as a source of more efficient inoculants. Soil Biol Biochem 41:2568–2572CrossRefGoogle Scholar
  219. Ronner E, Franke AC, Vanlauwe B, Dianda M, Edeh E, Ukem B, Bala A, van Heerwaarden J, Giller KE (2016) Understanding variability in soybean yield and response to P-fertilizer and rhizobium inoculants on farmers’ fields in northern Nigeria. Field Crops Res 186:133–145CrossRefGoogle Scholar
  220. Routray S, Khanna V (2018) Characterization of rhizobacteria for multiple plant growth promoting traits from mung bean rhizosphere. Int J Curr Microbiol App Sci 7(1):2264–2269CrossRefGoogle Scholar
  221. Ryu RJ, Patten CL (2008) Aromatic amino acid-dependent expression of indole-3 pyruvate decarboxylase is regulated by TyrR in Enterobacter cloacae UW5. J Bacteriol 190:7200–7208PubMedPubMedCentralCrossRefGoogle Scholar
  222. Sadowsky MJ (2005) Soil stress factors influencing symbiotic nitrogen fixation. In: Werner D, Newton WE (eds) Nitrogen fixation in agriculture, forestry and the environment. Springer, Dordrecht, pp 89–112CrossRefGoogle Scholar
  223. Saghafi D, Ghorbanpour M, Lajayer BA (2018) Efficiency of Rhizobium strains as plant growth promoting rhizobacteria on morpho-physiological properties of Brassica napus L. under salinity stress. J Soil Sci Plant Nutr 18(1):253–268Google Scholar
  224. Saha D, Purkayastha GD, Ghosh A, Isha M, Saha A (2012) Isolation and characterization of two new Bacillus subtilis strains from the rhizosphere of eggplant as potential biocontrol agents. J Plant Pathol 94:109–118Google Scholar
  225. Sahai P, Chandra R (2011) Co-inoculation effect of liquid and carrier inoculants of Mesorhizobium ciceri and PGPR on nodulation, nutrient uptake and yield of chickpea. J Food Legumes 23:159–161Google Scholar
  226. Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30Google Scholar
  227. Saidi S, Chebil S, Gtari M, Mhamdi R (2013) Characterization of root-nodule bacteria isolated from Vicia faba and selection of plant growth promoting isolates. World J Microbiol Biotechnol 29:1099–1106PubMedCrossRefPubMedCentralGoogle Scholar
  228. Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotechnol 34:635–648PubMedCrossRefGoogle Scholar
  229. Salvagiotti F, Cassman KG, Specht JE, Walters DT, Weiss A, Dobermann A (2008) Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crops Res 108:1–13CrossRefGoogle Scholar
  230. Samavat S, Besharati H, Behboudi K (2011) Interactions of rhizobia cultural filtrates with Pseudomonas fluorescens on bean damping-off control. J Agri Sci Tech 13:965–976Google Scholar
  231. Samavat S, Samavat S, Mafakheri S, Shakouri MJ (2012) Promoting common bean growth and nitrogen fixation by the co-inoculation of Rhizobium and Pseudomonas fluorescens isolates. Bulg J Agric Sci 18:387–395Google Scholar
  232. Sandhya V, Ali SKZ, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol Fertil Soils 46:17–26CrossRefGoogle Scholar
  233. Santaella C, Schue M, Berge O, Heulin T, Achouak W (2008) The exopolysaccharide of Rhizobium sp. YAS34 is not necessary for biofilm formation on Arabidopsis Thaliana and Brassica napus roots but contributes to root colonization. Environ Microbiol 10:2150–2163PubMedPubMedCentralCrossRefGoogle Scholar
  234. Seneviratne I, Gunaratne S, Bandara T, Weerasundara L, Rajakaruna N, Seneviratne G, Vithanage M (2016) Plant growth promotion by Bradyrhizobium japonicum under heavy metal stress. S Afr J Bot 105:19–24CrossRefGoogle Scholar
  235. Sgroy V, Cassan F, Masciarelli O, Del Papa MF, Lagares A, Luna V (2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biotechnol 85:371–381PubMedCrossRefGoogle Scholar
  236. Shah AH, Naz I, Ahmad H, Khokhar SN, Khan K (2016) Impact of zinc solubilizing bacteria on zinc contents of wheat. American Eurasian J Agric Environ Sci 16(3):449–454Google Scholar
  237. 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 (Vigna radiata L.). Appl Microbiol 42:155–159CrossRefGoogle Scholar
  238. Shaharoona B, Jamro GM, Zahir ZA, Arshad M, Memon KS (2007) Effectiveness of various Pseudomonas sp., and Burkholderia caryophylli containing ACC-deaminase for improving growth and yield (Triticum aestivum L.). J Microbiol Biotechnol 17(8):1300–1307PubMedGoogle Scholar
  239. Shamsuddin H, Tan Z, Zuan K, Radziah O, Khairuddin AR, Habib SH, Halimi MS (2014) Isolation and characterization of rhizobia and plant growth-promoting rhizobacteria and their effects on growth of rice seedlings. AJABS 9(3):342–360Google Scholar
  240. Sharma P, Sardana V, Kandola SS (2011) Response of groundnut (Arachis hypogaea L.) to Rhizobium inoculation. Libyan Agric Res Cen J Intl 2:101–104Google Scholar
  241. Sharma P, Padh H, Shrivastava N (2013) Hairy root cultures: a suitable biological system for studying secondary metabolic pathways in plants. Eng Life Sci 13:62–75CrossRefGoogle Scholar
  242. Shengepallu MD, Gaikwad RT, Chavan VA, Anand YR (2018) Isolation and characterization of nitrogen fixing bacteria from babchi (Psoralea corylifolia L.) and testing them for plant growth promotion traits in vitro. Int J Curr Microbiol App Sci 7:441–447CrossRefGoogle Scholar
  243. Shurigin V, Davranov K, Abdiev A (2015) Screening of salt tolerant rhizobia for improving growth and nodulation of chickpea (Cicer arietinum) under arid soil conditions of Uzbekistan. J Biol Chem Res 32(2):534–540Google Scholar
  244. Simonsen AK, Han S, Rekret P, Rentschler CS, Heath KD, Stinchcombe JR (2015) Short-term fertilizer application alters phenotypic traits of symbiotic nitrogen fixing bacteria. PeerJ 3:e1291. CrossRefPubMedPubMedCentralGoogle Scholar
  245. Singh Z, Singh G (2018) Role of Rhizobium in chickpea (Cicer arietinum) production – a review. Agric Rev 39(1):31–39Google Scholar
  246. 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 52:345–349PubMedCrossRefGoogle Scholar
  247. Singh RP, Shelke GM, Kumar A, Jha PN (2015) Biochemistry and genetics of ACC deaminase: a weapon to stress ethylene produced in plants. Front Microbiol 6:1–14Google Scholar
  248. Singh A, Sachan AK, Pathak RK, Srivastava S (2018) Study on the effects of PSB and Rhizobium with their combinations on nutrients concentration and uptake of chickpea (Cicer arietinum L.). J Pharmacogn Phytochem 7(1):1591–1593Google Scholar
  249. Singha B, Mazumder PB, Pandey P (2016) Characterization of plant growth promoting rhizobia from root nodule of Crotalaria pallida grown in Assam. IJBT 15:210–216Google Scholar
  250. Sistani NR, Kaul H, Desalegn G, Wienkoop S (2017) Rhizobium impacts on seed productivity quality and protection of Pisum sativum upon disease stress caused by Didymella pinodes: phenotypic, proteomic and metabolomics traits. Front Plant Sci 8:1–15Google Scholar
  251. Skaar EP (2010) The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6:1–4CrossRefGoogle Scholar
  252. Skorupska A, Janczarek M, Marczak M, Mazur A, Krol J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microbiol Cell Fact 5:1–19CrossRefGoogle Scholar
  253. Sogut T (2006) Rhizobium inoculation improves yield and nitrogen accumulation in soybean (Glycine max) cultivars better than fertilizer. New Zeal J Crop Hort 34:115–120CrossRefGoogle Scholar
  254. Solano RB, Garcıa JAL, Garcia-Villaraco A, Algar E, Garcia-Cristobal J, Manero FJG (2010) Siderophore and chitinase producing isolates from the rhizosphere of Nicotiana glauca Graham enhance growth and induce systemic resistance in Solanum ycopersicum L. Plant Soil 334:189–197CrossRefGoogle Scholar
  255. Solomon T, Lalit MP, Tsige A (2012) Effects of inoculation by Bradyrhizobium japonicum strains on nodulation nitrogen fixation and yield of soybean (Glycine max L) varieties on nitisols of bako, western Ethiopia. ISRN 2012:8. CrossRefGoogle Scholar
  256. Soumaya T, Sana DF, Faysal BJ, Imran H (2016) Effect of Rhizobium inoculation on growth and nutrient uptake of sulla (Hedysarum coronarium L.) grown in calcareous soil of northern Tunisia. Romanian Biotechnol Lett 21:11632–11639Google Scholar
  257. Sridevi M, Mallaiah KV (2009) Phosphate solubilization by Rhizobium strains. Indian J Microbiol 49(1):98–102PubMedPubMedCentralCrossRefGoogle Scholar
  258. Srivastava LM (2002) Plant growth and development: hormones and environment. Academic, San DiegoGoogle Scholar
  259. Stephens JHG, Rask HM (2000) Inoculant production and formulation. Field Crops Res 65:249–258CrossRefGoogle Scholar
  260. Suarez R, Wong A, Ramirez M, Barraza A, Orozco MC, Cevallos MA, Lara M, Hernandez 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 21:958–966PubMedCrossRefGoogle Scholar
  261. Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273PubMedCrossRefGoogle Scholar
  262. Sutherland IW (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9PubMedCrossRefGoogle Scholar
  263. Suzuki A, Akune M, Kogiso M, Imagama Y, Osuki K, Uchiumi T, Higashi S, Han SY, Yoshida S, Asami TM, Abe M (2004) Control of nodule number by the phytohormone abscisic acid in the roots of two leguminous species. Plant Cell Physiol 45:914–922PubMedCrossRefGoogle Scholar
  264. Sylvie B, Patrick AN (2009) Effects of Rhizobium inoculation, lime and molybdenum on photosynthesis and chlorophyll content of Phaseolus vulgaris L. Afr J Microbiol Res 3:791–798Google Scholar
  265. Tagore GS, Namdeo SL, Sharma SK, Kumar N (2013) Effect of Rhizobium and phosphate solubilizing bacterial inoculants on symbiotic traits, nodule leghemoglobin, and yield of chickpea genotypes. Int J Agron 2013:1–8CrossRefGoogle Scholar
  266. Tairo EV, Ndakidemi PA (2013) Bradyrhizobium japonicum inoculation and phosphorus supplementation on growth and chlorophyll accumulation in soybean (Glycine max L.). AJPS 4:2281–2289CrossRefGoogle Scholar
  267. Tairo EV, Ndakidemi PA (2014) Macronutrients uptake in soybean as affected by bradyrhizobium japonicum inoculation and phosphorus (p) supplements. AJPS 5:488–496CrossRefGoogle Scholar
  268. Tao G, Tian S, Cai M, Xie G (2008) Phosphate solubilizing and mineralizing abilities of bacteria isolated from soils. Pedosphere 18:515–523CrossRefGoogle Scholar
  269. Tate RL (1995) Soil microbiology (symbiotic nitrogen fixation). Wiley, New York, pp 307–333Google Scholar
  270. Tavasolee A, Aliasgharzad N, SalehiJouzani G, Mardi M, Asgharzadeh A (2011) Interactive effects of Arbuscular mycorrhizal fungi and rhizobial strains on chickpea growth and nutrient content in plant. Afr J Biotechnol 10:7585–7591Google Scholar
  271. Tena W, Wolde-Meskel E, Walley F (2016) Symbiotic efficiency of native and exotic rhizobium strains nodulating lentil (Lens culinaris Medik.) in soils of Southern Ethiopia. Agronomy 6:1–11CrossRefGoogle Scholar
  272. Thamer S, Schadler M, Bonte D (2011) Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant. Plant Soil 341:209–219CrossRefGoogle Scholar
  273. Thies JE, Singleton PW, Bohlool BB (1991) Modeling symbiotic performance of introduced rhizobia in the field by use of indices of indigenous population size and nitrogen status of the soil. Appl Environ Microbiol 57:29–37PubMedPubMedCentralGoogle Scholar
  274. Thies JE, Bohlool BB, Singleton PW (1992) Environmental effects on competition for nodule occupancy between introduced and indigenous rhizobia and among introduced strains. Can J Microbiol 38:493–500CrossRefGoogle Scholar
  275. Triplett EW, Breil BT, Splitter GA (1994) Expression of tfx and sensitivity to the rhizobial antipeptide trifolitoxin in a taxonomically distinct group of α-proteobacteria including the animal pathogen Brucella abortus. Appl Environ Microbiol 60:4163–4166PubMedPubMedCentralGoogle Scholar
  276. Turan M, Ataoglu N, Sahin F (2006) Evaluation of the capacity of phosphate solubilizing bacteria and fungi on different forms of phosphorus in liquid culture. J Sustain Agr 28:99–108CrossRefGoogle Scholar
  277. Uma C, Sivagurunathan P, Sangeetha D (2013) Performance of Bradyrhizobial isolates under drought conditions. Int J Curr Microbiol App Sci 2:228–232Google Scholar
  278. 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, Boca Raton, Florida, pp 1–22Google Scholar
  279. Verma JP, Yadav J, Tiwari KN (2010) Application of Rhizobium sp. BHURC01and plant growth promoting rhizobacteria on nodulation, plant biomass and yield of chickpea (Cicer arietinum L.). Int J Agric Res 5:148–156CrossRefGoogle Scholar
  280. Victor A, Angulo G, Bonomi HR, Posadas DM, Serer MI, Torres AG, Zorreguiet A, Goldbauma FA (2013) Identification and characterization of RibN, a novel family of riboflavin transporters from Rhizobium leguminosarum and other Proteobacteria. J Bacteriol 195(20):4611–4619CrossRefGoogle Scholar
  281. Vidal C, Chantreuil C, Berge O, Maure L, Escarree J, Bena G, Brunel B, Marel JC (2009) Mesorhizobium metallidurans sp. nov., a metal-resistant symbiont of Anthyllis vulneraria growing on metallicolous soil in Languedoc France. Int J Syst Evol Microbiol 59:850–855PubMedCrossRefPubMedCentralGoogle Scholar
  282. Vijayabaskar P, Babinastarlin S, Shankar T, Sivakumar T, Anandapandian KTK (2011) Quantification and characterization of exopolysaccharides from Bacillus subtilis (MTCC 121). Adv Biol Res 5:71–76Google Scholar
  283. Wagner SC (2011) Biological nitrogen fixation. Nat Edu Knowl 2:14Google Scholar
  284. Wang C, Knill E, Glick BR, Defago G (2000) Effect of transferring 1-aminocyclopropane 1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth promoting and disease suppressive capacities. Can J Microbiol 46:898–907PubMedCrossRefPubMedCentralGoogle Scholar
  285. 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(3):173–181PubMedCrossRefGoogle Scholar
  286. Wang Q, Liu J, Zhu H (2018) Genetic and molecular mechanisms underlying symbiotic specificity in legume-rhizobium interactions. Front Plant Sci 9:1–8CrossRefGoogle Scholar
  287. Wani PA, Khan MS (2010) Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem Toxicol 48:3262–3267PubMedCrossRefPubMedCentralGoogle Scholar
  288. Wani PA, Khan MS, Zaidi A (2007a) Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by green gram plants. Chemosphere 70:36–45PubMedCrossRefPubMedCentralGoogle Scholar
  289. Wani PA, Khan MS, Zaidi A (2007b) Synergistic effects of the inoculation with nitrogen fixing and phosphate solubilizing rhizobacteria on the performance of field grown chickpea. J Plant Nutr Soil Sci 170:283–287CrossRefGoogle Scholar
  290. Wani PA, Khan MS, Zaidi A (2008) Effect of metal-tolerant plant growth promoting Rhizobium on the performance of pea grown in metal-amended soil. Arch Environ Contam Toxicol 55:33–42PubMedCrossRefPubMedCentralGoogle Scholar
  291. Werma JP, Yadav J, Tiwari KN (2012) Enhancement of nodulation and yield of chickpea by co-inoculation of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria in eastern Uttar Pradesh. Commun Soil Sci Plant Anal 43:605–621CrossRefGoogle Scholar
  292. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254PubMedCrossRefPubMedCentralGoogle Scholar
  293. White JP, Prell J, Ramachandran VK, Poole PS (2009) Characterization of a γ-aminobutyric acid transport system of Rhizobium leguminosarum bv. viciae 3841. J Bacteriol 191(5):1547–1555PubMedCrossRefPubMedCentralGoogle Scholar
  294. Wienkoop S, Sistani NR, Kaul HP, Desalegn G (2017) Rhizobium impacts on seed productivity, quality, and protection of Pisum sativum upon disease stress caused by Didymella pinodes: phenotypic, proteomic, and metabolomic traits. Front Plant Sci 8:1961. CrossRefPubMedPubMedCentralGoogle Scholar
  295. Wolde-meskel E, van Heerwaaarden J, Abdulkadir B, Kassa S, Aliyi I, Degefu T, Wakweya K, Kanampiu F, Ciller KC (2018) Additive yield response of chickpea (Cicer arietinum L.) to rhizobium inoculation and phosphorus fertilizer across smallholder farms in Ethiopia. Agric Ecosyst Environ 261:144–152PubMedPubMedCentralCrossRefGoogle Scholar
  296. Yadegari M, Mehrab M, Rahmani H, Noormohammadi G, Ayneband A (2010) Evaluation of bean (Phaseolus vulgaris) seeds inoculation with Rhizobium phaseoli and plant growth promoting rhizobacteria on yield and yield components. PJBS 11:1935–1939Google Scholar
  297. Yang G, Bhuvaneswari TV, Joseph CM, King MD, Phillips DA (2002) Roles for riboflavin in the Sinorhizobium-alfalfa association. Mol Plant-Microbe Interact 5:456–462CrossRefGoogle Scholar
  298. 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 28:845–870Google Scholar
  299. 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 32:79–86Google Scholar
  300. Zahedi H, Abbasi S, Sadeghipour O, Akbari R (2013) Effect of plant growth promoting rhizobacteria (PGPR) on physiological parameters and nitrogen content of soybean grown under different irrigation regimes. Res Crops 14(3):798–803Google Scholar
  301. Zahir ZA, Munir A, Asghar HN, Shaharoona B, Arshad M (2008) Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18(5):958–963PubMedGoogle Scholar
  302. 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 20:1288–1294PubMedCrossRefGoogle Scholar
  303. Zahir ZA, Ahmad M, Hilger TH, Dar A, Malik SR, Abbas G, Rasche F (2018) Field evaluation of multistrain biofertilizer for improving the productivity of different mungbean genotypes. Soil Environ 37(1):45–52CrossRefGoogle Scholar
  304. Zaman S, Mazid MA, Kabir G (2011) Effect of Rhizobium inoculant on nodulation, yield and yield traits of chickpea (Cicer arietinum l.) in four different soils of greater Rajshahi. J Life Earth Sci 6:45–50CrossRefGoogle Scholar
  305. Zhang S, Reddy MS, Kloepper JW (2002) Development of assays for assessing induced systemic resistance by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol Control 23:79–86CrossRefGoogle Scholar
  306. Zhang W, Wang HW, Wan XX, Xie XG, Siddikee A, Xu RS, Da CC (2016) Enhanced nodulation of peanut when co-inoculated with fungal endophyte Phomopsis liquidambari and bradyrhizobium. Plant Physiol Biochem 98:1–11PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Iqra Naseer
    • 1
  • Maqshoof Ahmad
    • 1
  • Sajid Mahmood Nadeem
    • 2
  • Iqra Ahmad
    • 1
  • Najm-ul-Seher
    • 1
  • Zahir Ahmad Zahir
    • 3
  1. 1.Department of Soil ScienceUniversity College of Agriculture and Environmental Sciences, The Islamia University of BahawalpurBahawalpurPakistan
  2. 2.University of Agriculture Faisalabad, Sub-campus BurewalaVehariPakistan
  3. 3.Institute of Soil and Environmental SciencesUniversity of AgricultureFaisalabadPakistan

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