Potential of Rhizosphere Bacteria for Improving Rhizobium-Legume Symbiosis

  • Ijaz Mehboob
  • Muhammad Naveed
  • Zahir A. Zahir
  • Angela Sessitsch


About 60 % of the earth’s available nitrogen is fixed via biological nitrogen fixation (BNF). Being a major contributor to BNF, Rhizobium-legume symbiosis can provide well over half of the biological source of fixed nitrogen. Actually, Rhizobium-legume symbiosis results in the formation of nodules on legume roots where rhizobia fix nitrogen from the atmosphere. But nodulation and nitrogen fixation is a complex process and is dependent on the compatibility and potential of both partners of Rhizobium-legume symbiosis under variable soil and environmental conditions. Although, some selected efficient and effective traits of rhizobia and legumes have shown encouraging results, there is a need of consistent positive influence on nodulation and nitrogen fixation to maximize the growth and yield of legumes under variable conditions. Hence, the use of means capable of improving both the legume growth and the growth and function of symbiotic rhizobia is essential. Co-inoculation of Rhizobium species with favorably interacting traits of plant growth-promoting rhizobacteria (PGPR) is considered an applied, cost-effective, efficient, and environment-friendly approach to further improve legume growth and productivity under variable conditions because they can provide broad spectrum mechanisms of actions and improve reliability of inocula without genetic engineering. In addition, these PGPR when used in combination with rhizobia have also shown the strategies for dealing with stressful conditions like salinity, pH, temperature, drought, heavy metal, and pathogens which could further impose limitations on the capacity of Rhizobium-legume symbiosis. This chapter highlights various PGPR traits compatible with specific legume rhizobia and their phytostimulatory mechanisms contributing to augmentation in rhizobial growth and function for growth and yield enhancement of legumes under variable conditions.


Nitrogen Fixation Common Bean Rhizobial Strain Biological Nitrogen Fixation Nodule Occupancy 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are thankful to Hafiz Muhammad Haroon for his help in drawing Fig. 12.1.


  1. Abdel-Wahab AFM, Mekhemar GAA, Badawi FSF, Shehata HS (2008) Enhancement of nitrogen fixation, growth and productivity of Bradyrhizobium-lupinus symbiosis via co-inoculation with rhizobacteria in different soil types. J Agric Sci Mansoura Univ 33:469–484Google Scholar
  2. Abeles FD, Morgan PW, Saltveit MEJ (1992) Ethylene in plant biology, 2nd edn. Academic, San DiegoGoogle Scholar
  3. Adeseoye AO, Torbert HA, Kloepper JW (2010) Increased plant uptake of nitrogen from 15N-dependent fertilizer using plant growth-promoting rhizobacteria. Appl Soil Ecol 46:54–58Google Scholar
  4. Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth-promoting activities. Microbiol Res 163:73–181Google Scholar
  5. Ahmad M, Zahir ZA, Asghar HN, Asghar M (2011) Inducing salt tolerance in mung bean through co-inoculation with rhizobia and plant-growth-promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate-deaminase. Can J Microbiol 57:578–589PubMedGoogle Scholar
  6. Ahmad M, Zahir ZA, Asghar HN, Arshad M (2012) The combined application of rhizobial strains and plant growth promoting rhizobacteria improves growth and productivity of mung bean (Vigna radiata L.) under salt-stressed conditions. Ann Microbiol 62:1321–1330Google Scholar
  7. 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 50:361–372Google Scholar
  8. Alagawadi AR, Gaur AC (1988) Associative effect of Rhizobium and phosphate-solubilizing bacteria on the yield and nutrient uptake of chickpea. Plant Soil 105:241–246Google Scholar
  9. Anandham R, Sridar R, Nalayini P, Poonguzhali S, Madhaiyan M, Tongmin S (2007) Potential for plant growth promotion in groundnut (Arachis hypogaea L.) cv. ALR-2 by co-inoculation of sulfur-oxidizing bacteria and Rhizobium. Microbiol Res 162:139–153PubMedGoogle Scholar
  10. Andrade D, De Leij FAAM, Lynch JM (1998) Plant mediated interactions between Pseudomonas fluorescens, Rhizobium leguminosarum and arbuscular mycorrhizae on pea. Lett Appl Microbiol 26:311–316Google Scholar
  11. Arshad M, Frankenberger WT Jr (1991) Microbial production of plant hormones. Plant Soil 133:1–8Google Scholar
  12. Arshad M, Frankenberger WT Jr (2002) Ethylene: agricultural sources and applications. Kluwer Academic Publishers, New YorkGoogle Scholar
  13. Atieno M, Herrmann L, Okalebo R, Lesueur D (2012) Efficiency of different formulations of Bradyrhizobium japonicum and effect of co- inoculation of Bacillus subtilis with two different strains of Bradyrhizobium japonicum. World J Microbiol Biotechnol 28:2541–2550PubMedGoogle Scholar
  14. Babar SM, Mirza MS, Bano A, Malik KA (2007) Co-inoculation of chickpea with rhizobium isolates from roots and nodules and phytohormone producing Enterobacter strains. Aust J Agric Res 47:1008–1015Google Scholar
  15. 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. Ann Agric Sci 56:17–25Google Scholar
  16. Bai Y, Pan B, Charles TC, Smith DL (2002a) Co-inoculation dose and root zone temperature for plant growth promoting rhizobacteria on soybean [Glycine max (L.) Merr] grown in soil-less media. Soil Biol Biochem 34:1953–1957Google Scholar
  17. Bai Y, Souleimanov A, Smith DL (2002b) An inducible activator produced by a Serratia proteamaculans strain and its soybean growth-promoting activity under greenhouse conditions. J Exp Bot 53:149–502Google Scholar
  18. Bai Y, Zhou X, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1781Google Scholar
  19. Bakker PAHM, Van Peer R, Schippers B (1991) Suppression of soil-borne plant pathogens by fluorescent Pseudomonas: mechanisms and prospects. In: Beemster ABR, Bollewn M, Gerirch Ruissen MA, Schippers B, Tempel A (eds) Biotic interactions and soil-borne diseases. Elsevier, Amsterdam, pp 221–230Google Scholar
  20. Barea JM, Andrade G, Bianciotto V, Dowling D, Lohrke S, Bontante PO, Gara F, Azcon-Aguilar C (1998) Impact on arbuscular mycorrhiza formation of Pseudomonas strains used as inoculants for biocontrol of soil-borne fungal plant pathogens. Appl Environ Microbiol 64:2304–2307PubMedGoogle Scholar
  21. Barea JM, Pozo MJ, Azcon A, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778PubMedGoogle Scholar
  22. Barka AE, Nowk J, Clement C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with plant growth promoting rhizobacteria Burkholderia phytofermans strain PsJN. Appl Environ Microbiol 72:7246–7252Google Scholar
  23. Bashan Y (1998) Inoculants of plant growth promoting bacteria for use in agriculture. Biotechnol Adv 16:729–770Google Scholar
  24. Bashan Y, de-Bashan LE (2005) Bacterial plant growth-promotion. In: Hillel D (ed) Encyclopedia of soils in the environment, vol 1. Elsevier, OxfordGoogle Scholar
  25. Beijerinck MW (1901) Ueber oligonitrophile Mikroben, Zentral-blatt fur Bakteriologie. Parasitenkunde, Infektionskrankheiten und Hygiene Abteilungen II 7:561–582Google Scholar
  26. Belimov AA, Kojemiakov PA, Chuvarliyeva CV (1995) Interaction between barley and mixed cultures of nitrogen-fixing and phosphate-solubilizing bacteria. Plant Soil 17:29–37Google Scholar
  27. Berggren I, Alstrom S, van Vuurde JWL, Martensson AM (2005) Rhizoplane colonisation of peas by Rhizobium leguminosarum bv. viceae and a deleterious Pseudomonas putida. FEMS Microbiol Ecol 52:71–78PubMedGoogle Scholar
  28. Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180Google Scholar
  29. Brown ME (1974) Seed and root bacterization. Annu Rev Phytopathol 12:181–197Google Scholar
  30. Bucio JL, Cuevas CC, Calderon EH, Becerra CV, Rodriguez RF, Rodriguez LIM, Cantero EV (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20:207–217Google Scholar
  31. Budezikiewicz H (1997) Siderophore of fluorescent Pseudomonas L. Nat Foresche 52C:413–420Google Scholar
  32. Burdman S, Volpin H, Kigel J, Kapulnik Y, Okon Y (1996) Promotion of nod gene inducers and nodulation in common bean (Phaseolus vulgaris) roots inoculated with Azospirillum brasilense Cd. Appl Environ Microbiol 62:3030–3033PubMedGoogle Scholar
  33. Burdman S, Kigel J, Okon Y (1997) Effects of Azospirillum brasilense on nodulation and growth of common bean (Phaseolus vulgaris L.). Soil Biol Biochem 29:923–929Google Scholar
  34. Burns TA, Bishop JRPE, Israel DW (1981) Enhanced nodulation of leguminous plant roots by mixed cultures of Azotobacter vinelandii and Rhizobium. Plant Soil 62:399–412Google Scholar
  35. Burris RH (1994) Biological nitrogen fixation – past and future. In: Hegazi NA, Fayez M, Monib M (eds) Nitrogen fixation with non-legumes. American University in Cairo Press, Cairo, pp 1–11Google Scholar
  36. Camacho M, Santamaria C, Temprano F, Rodriguez-Navarro DN, Daza A (2001) Co-inoculation with Bacillus sp. CECT 450 improves nodulation in Phaseolus vulgaris L. Can J Microbiol 47:1058–1062PubMedGoogle Scholar
  37. 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 45:28–35Google Scholar
  38. Castro-Sowinski S, Herschkovitz Y, Okon Y, Jurkevitch E (2007) Effects of inoculation with plant growth-promoting rhizobacteria on resident rhizosphere microorganisms. FEMS Microbiol Lett 276:1–11PubMedGoogle Scholar
  39. Chandra R, Pareek RP (2002) Effect of rhizobacteria in urdbean and lentil. Indian J Pulse Res 15:152–155Google Scholar
  40. Chanway CP, Hynes RK, Nelson LM (1989) Plant growth-promoting rhizobacteria: effects on growth and nitrogen fixation of lentil (Lens esculenta Moench) and pea (Pisum sativum L.). Soil Biol Biochem 21:511–517Google Scholar
  41. Chebotar VK, Asis CA Jr, Akao S (2001) Production of growth-promoting substances and high colonization ability of rhizobacteria enhance the nitrogen fixation of soybean when coinoculated with Bradyrhizobium japonicum. Biol Fertil Soils 34:427–432Google Scholar
  42. Crowley DE, Reid CPPP, Szaniszlo PJ (1998) Utilization of microbial siderophore in iron acquisition by oat. Plant Physiol 87:680–685Google Scholar
  43. Dardanelli MS, de Cordoba FJF, Espuny MR, Carvajal MAR, Diaz MES, Serrano AMG, OkonY MM (2008) Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biol Biochem 40:2713–2721Google Scholar
  44. Dary M, Chamber M, Palomares A, Pajuelo E (2010) “In situ” phytostabilization of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177:323–330PubMedGoogle Scholar
  45. 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 3:373–385Google Scholar
  46. Dashti N, Zhang F, Hynes R, Smith DL (1997) Application of plant growth-promoting rhizobacteria to soybean [Glycine max (L.) Merr.] increases protein and dry matter yield under shot season conditions. Plant Soil 188:33–41Google Scholar
  47. Dashti N, Zhang F, Hynes R, Smith DL (1998) Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean [Glycine max (L.) Merr.] under short season conditions. Plant Soil 200:205–213Google Scholar
  48. Dashti N, Prithiviraj B, Zhou X, Hynes RK, Smith DL (2000) Combined effects of plant growth‐promoting rhizobacteria and genistein on nitrogen fixation in soybean at suboptimal root zone temperatures. J Plant Nutr 23:593–604Google Scholar
  49. Dashti N, Khanafer M, El-Nemr I, Sorkhok N, Ali N, Radwan S (2009) The potential of oil-utilizing bacterial consortia associated with legume root nodules for cleaning oily soils. Chemosphere 74:1354–1359PubMedGoogle Scholar
  50. de Freitas JR, Gupta VVSR, Germida JJ (1993) Influence of Pseudomonas syringae R25 and Pseudomonas putida R105 on the growth and nitrogen fixation (acetylene reduction activity) of pea (Pisum sativum L.) and field bean (Phaseolus vulgaris L.). Biol Fertil Soils 16:215–220Google Scholar
  51. Deanand BJ, Patil AB, Kulkaarni JH, Algawadi AR (2002) Effect of plant growth promoting rhizobacteria on growth and yield of pigeon pea (Cajanus cajan L.) by application of plant-growth promoting rhizobacteria. Microbiol Res 159:371–394Google Scholar
  52. del Gallo M, Fabbri P (1991) Effect of soil organic matter on chickpea inoculated with Azospirillum brasilense and Rhizobium leguminosarum bv. ciceri. Plant Soil 137:171–175Google Scholar
  53. Derylo M, Skorupska A (1993) Enhancement of symbiotic nitrogen fixation by vitamin-secreting fluorescent Pseudomonas. Plant Soil 54:211–217Google Scholar
  54. Dobbelaere S, Okon Y (2007) The plant growth-promoting effect and plant responses. In: Elmerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanobacterial association. Springer, Dordrecht, pp 145–170Google Scholar
  55. Duffy BK, Defago G (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol 65:2429–2438PubMedGoogle Scholar
  56. Dutta S, Mishra AK, Dileep Kumar BS (2008) Induction of systemic resistance against fusarial wilt in pigeon pea through interaction of plant growth promoting rhizobacteria and rhizobia. Soil Biol Biochem 40:452–461Google Scholar
  57. Egamberdieva D, Berg G, Lindström K, Räsänen LA (2010) Co-inoculation of Pseudomonas spp. with Rhizobium improves growth and symbiotic performance of fodder galega (Galega orientalis Lam.). Eur J Soil Biol 46:269–272Google Scholar
  58. Elkoca E, Kantar F, Sahin F (2008) Influence of nitrogen fixing and phosphorus solubilising bacteria on the nodulation, plant growth and yield of chickpea. J Plant Nutr 31:157–171Google Scholar
  59. 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 33:2104–2119Google Scholar
  60. El-Sawy WA, Mekhemar GAA, Kandil BAA (2006) Comparative assessment of growth and yield responses of two peanut genotypes to inoculation with Bradyrhizobium conjugated with cyanobacteria or rhizobacteria. Minufiya J Agric Res 31:1031–1049Google Scholar
  61. Engqvist LG, Martensson A, Orlowska E, Turnau K, Belimov AA, Borisov AY, Gianinazzi-Pearson V (2006) For a successful pea production on polluted soils, inoculation with beneficial microbes requires active interaction between the microbial components and the plant. Acta Agric Scand Sect B Soil Plant Sci 56:9–16Google Scholar
  62. Esteve de Jensen C, Pereick JA, Graham PH (2002) Integrated management strategies of bean root rot with Bacillus subtilis and Rhizobium in Minnesota. J Field Crops Res 74:107–115Google Scholar
  63. 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 49:29–36Google Scholar
  64. Figueiredo MVB, Martinez CR, Burity HA, Chanway CP (2008) Plant growth-promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean (Phaseolus vulgaris L.). World J Microbiol Biotechnol 24:1187–1193Google Scholar
  65. 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 348:245–254Google Scholar
  66. Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394–401PubMedGoogle Scholar
  67. Fuhrmann J, Wollum AG (1989) Nodulation competition among Bradyrhizobium japonicum strains as influenced by rhizosphere bacteria and iron availability. Biol Fertil Soils 7:108–112Google Scholar
  68. Garcia JAL, Probanza A, Ramos B, Barriuso J, Mañero FJG (2004a) Effects of inoculation with plant growth promoting rhizobacteria (PGPRs) and Sinorhizobium fredii on biological nitrogen fixation, nodulation and growth of Glycine max cv. Osumi. Plant Soil 267:143–153Google Scholar
  69. Garcia JAL, Probanza A, Ramos B, Flores JJC, Mañero FJG (2004b) Effects of plant growth promoting rhizobacteria (PGPRS) on the biological nitrogen fixation, nodulation, and growth of Lupinus albus L. cv. Multolupa. Eng Life Sci 4:71–77Google Scholar
  70. Geurts R, Bisseling T (2002) Rhizobium nod factor perception and signaling. Plant Cell 14:S239–S249PubMedGoogle Scholar
  71. Glick BR, Pentrose DM, Li J (1998) A model for lowering plant ethylene concentration by plant growth promoting rhizobacteria. J Theor Biol 190:63–68PubMedGoogle Scholar
  72. Goel AK, Sindhu SS, Dadarwal KR (2000) Pigment diverse mutants of Pseudomonas sp.: inhibition of fungal growth and stimulation of growth of Cicer arietinum. Biol Plant 43:563–569Google Scholar
  73. Goel AK, Sindhu SS, Dadarwal KR (2001) Seed bacterization with fluorescent Pseudomonas enhances the synthesis of flavonoid-like compounds in chickpea (Cicer arietinum L.). Physiol Mol Biol Plants 6:195–198Google Scholar
  74. Goel AK, Sindhu SS, Dadarwal KR (2002) Stimulation of nodulation and plant growth of chickpea (Cicer arietinum L.) by Pseudomonas pp. antagonistic to fungal pathogens. Biol Fertil Soils 36:391–396Google Scholar
  75. Grattan SR, Grieve CM (1999) Mineral nutrient acquisition and response of plants grown in saline environments. In: Pessarakli M (ed) Handbook of plant and crop stress. Marcel Dekker Press Inc, New York, pp 203–229Google Scholar
  76. Groppa MD, Zawoznik MS, Tomaro ML (1998) Effects of co-inoculation with Bradyrhizobium japonicum and Azospirillum brasilense on soybean plants. Eur J Soil Biol 34:75–80Google Scholar
  77. Guinazu LB, Andres JA, Del Papa MF, Pistorio M, Rosas SB (2010) Response of alfalfa (Medicago sativa L.) to single and mixed inoculation with phosphate-solubilizing bacteria and Sinorhizobium meliloti. Biol Fertil Soils 46:185–190Google Scholar
  78. Gull M, Hafeez FY, Saleem M (2004) Phosphorus uptake and growth promotion of chickpea by co-inoculation of mineral phosphate solubilizing bacteria and a mixed rhizobial culture. Aust J Exp Agric 44:623–628Google Scholar
  79. Gunasekaran S, Balachandar D, Mohanasundaram K (2004) Studies on synergism between Rhizobium, plant growth promoting rhizobacteria (PGPR) and phosphate solubilizing bacteria in black gram. In: Kannaiyan S, Kumar K, Govimdarajan K (eds) Biofertilizer technology for rice based cropping system. Scientific Publ, Jodhpur, pp 269–273Google Scholar
  80. 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(11):3–117Google Scholar
  81. Hadi F, Bano A (2010) Effect of diazotrophs (Rhizobium and Azatebactor) on growth of maize (Zea mays L.) and accumulation of lead (Pb) in different plant parts. Pak J Bot 42:4363–4370Google Scholar
  82. Hamaoui B, Abbadi JM, Burdman S, Rashid A, Sarig S, Okon Y (2001) Effects of inoculation with Azospirillum brasilense on chickpeas (Cicer arietinum) and faba beans (Vicia faba) under different growth conditions. Agronomie 21:553–560Google Scholar
  83. Hameeda B, Harini G, Rupela OP, Kumar Rao JVDK, Reddy G (2010) Biological control of chickpea collar rot by co-inoculation of antagonistic bacteria and compatible rhizobia. Indian J Microbiol 50:419–424PubMedGoogle Scholar
  84. Handelsman J, Raffel S, Mester EH, Wunderlich L, Grau CR (1990) Biological control of damping-off of alfalfa seedlings with Bacillus cereus UW85. Appl Environ Microbiol 56:713–718PubMedGoogle Scholar
  85. Holguin G, Glick BR (2001) Expression of the ACC deaminase gene from Enterobacter cloacae UW4 in Azospirillum brasilense. Microb Ecol 41:281–288PubMedGoogle Scholar
  86. Hubbell DH, Kidder G (2009) Biological nitrogen fixation. Univ Fla IFAS Ext Publ SL16:1–4Google Scholar
  87. Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res 65:151–164Google Scholar
  88. Ibekwe AM, Angle JS, Chaney RL, Vonberkum P (1997) Enumeration and nitrogen fixation potential of Rhizobium leguminosarum biovar trifolii grown in soil with varying pH values and heavy metal concentrations. Agric Ecosyst Environ 61:103–111Google Scholar
  89. Iqbal MA, Khalid M, Shahzad SM, Ahmad M, Soleman N, Akhtar N (2012) Integrated use of Rhizobium leguminosarum, plant growth promoting rhizobacteria and enriched compost for improving growth, nodulation and yield of lentil (Lens culinaris Medik). Chilean J Agric Res 72:104–110Google Scholar
  90. Iruthayathas EE, Gunasekaran S, Vlassak K (1983) Effect of combined inoculation of Azospirillum and Rhizobium on nodulation and N2 fixation of winged bean and soybean. Sci Hortic 20:231–240Google Scholar
  91. Jadhav RS, Thaker NV, Desai A (1994) Involvement of the siderophore of cowpea Rhizobium in the iron nutrition of the peanut. World J Microbiol Biotechnol 10:360–361Google Scholar
  92. Janisiewicz WJ (1996) Ecological diversity, niche overlap, and coexistence of antagonists used in developing mixtures for biocontrol of postharvest diseases of apples. Phytopathology 86:473–479Google Scholar
  93. Juge C, Prévost D, Bertrand A, Bipfubusa M, Chalifour F-P (2012) Growth and biochemical responses of soybean to double and triple microbial associations with Bradyrhizobium, Azospirillum and arbuscular mycorrhizae. Appl Soil Ecol 61:147–157Google Scholar
  94. Khammas KM, Ageron E, Grimont PAD, Kaisar P (1989) Azospirillum irakense sp. nov., a nitrogen fixing bacterium associated with rice roots and rhizosphere soil. Res Microbiol 140:679–693PubMedGoogle Scholar
  95. Khan MS, Zaidi A, Aamil M (2002) Biocontrol of fungal pathogens by the use of plant growth promoting rhizobacteria and nitrogen fixing microorganisms. Indian J Bot Soc 81:255–263Google Scholar
  96. Khot GG, Tauro P, Dadarwal KR (1996) Rhizobacteria from chickpea (Cicer arietinum L.) rhizosphere effective in wilt control and promote nodulation. Indian J Microbiol 36:217–222Google Scholar
  97. Khurana SA, Sharma P (2000) Effect of dual inoculation of phosphate solubilizing bacteria, Bradyrhizobium sp. (Cicer) and phosphorus on nitrogen fixation and yield of chickpea. Indian J Pulses Res 13:66–67Google Scholar
  98. Kloepper JW (1993) Plant growth promoting rhizobacteria as biological control agents. In: Metting FB Jr (ed) Soil microbial ecology. Dekker, New York, pp 255–274Google Scholar
  99. Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacteria inocula for enhancing crop productivity. Trends Biotechnol 7:39–43Google Scholar
  100. Knight TJ, Langston-Unkefer PJ (1988) Enhancement of symbiotic dinitrogen fixation by a toxin-releasing plant pathogen. Science 241:951–954PubMedGoogle Scholar
  101. Kumar R, Chandra R (2008) Influence of PGPR and PSB on Rhizobium leguminosarum bv. viciae strain competition and symbiotic performance in lentil. World J Agric Sci 4:297–301Google Scholar
  102. Kumar J, Sing NB, van Rheenen HA, Johansen C, Asthana AN, Ali M, Agrawal SC, Pandey RL, Verma MM, Gaur RB, Satyanarayana A, Patil MS, Rahman MM, Saxena NP, Haware MP, Wightman JA (1997) Growing chickpea in India. International Crops Research Institute for the Semi-Arid Tropics/Indian Council of Agricultural Research, Patancheru/New Delhi, p 602Google Scholar
  103. Kumar BSD, Berggfren I, Martensson AM (2001) Potential for improving pea production by co-inoculation with fluorescent Pseudomonas and Rhizobium. Plant Soil 229:25–34Google Scholar
  104. Lee W, Wood TK, Chen W (2006) Engineering TCE-degrading rhizobacteria for heavy metal accumulation and enhanced TCE degradation. Biotechnol Bioeng 95:399–403PubMedGoogle Scholar
  105. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, Denarie J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784PubMedGoogle Scholar
  106. Lian B, Prithiviraj B, Souleimanov A, Smith DL (2001) Evidence for the production of chemical compounds analogous to nod factor by the silicate bacterium Bacillus circulans GY92. Microbiol Res 156:289–292PubMedGoogle Scholar
  107. Linderman RG (1994) Role of VAM fungi in biocontrol. In: Pfleger FL, Linderman RG (eds) Mycorrhizae and plant health. APS Press, St Paul, pp 1–26Google Scholar
  108. Loper JE, Henkels MD (1999) Utilization of heterologous siderophore enhances level of iron available to Pseudomonas putida in rhizosphere. Appl Environ Microbiol 65:5357–5363PubMedGoogle Scholar
  109. Machackova I, Chavaux N, Dewitte W, Onckelen HV (1997) Diurnal fluctuations in ethylene formation in Chenopodium rubrum. Plant Physiol 113:981–985PubMedGoogle Scholar
  110. Magalhaes FM, Baldani JI, Souto SM, Kuykendall JR, Dobereiner J (1983) A new acid-tolerant Azospirillum species. An Acad Bras Cienc 55:417–430Google Scholar
  111. Malik DK, Sindhu SS (2008) Transposon-derived mutants of Pseudomonas strains altered in indole acetic acid production: effect on nodulation and plant growth in green gram (Vigna radiata L.). Physiol Mol Biol Plant 14:315–320Google Scholar
  112. Malik DK, Sindhu SS (2011) Production of indole acetic acid by Pseudomonas sp.: effect of coinoculation with Mesorhizobium sp. Cicer on nodulation and plant growth of chickpea (Cicer arietinum). Physiol Mol Biol Plant 17:25–32Google Scholar
  113. Marek-Kozaczuk M, Skorupska A (2001) Production of B-group vitamins by plant growth-promoting Pseudomonas fluorescens strain 267 and the importance of vitamins in the colonization and nodulation of red clover. Biol Fertil Soils 33:146–151Google Scholar
  114. Marek-Kozaczuk M, Derylo M, Skorupska A (1996) Tn5 insertion mutants of Pseudomonas sp. 267 defective in siderophore production and their effect on clover (Trifolium pratense) nodulated with Rhizobium leguminosarum bv. trifolii. Plant Soil 179:269–274Google Scholar
  115. Marek-Kozaczuk M, Kopcinska J, Lotocka B, Golinowski W, Skorupska A (2000) Infection of clover by plant growth promoting Pseudomonas fluorescens strain 267 and Rhizobium leguminosarum bv. trifolii studied by mTn5-gusA. Antonie van Leeuwenhock 78:1–11Google Scholar
  116. Martinez-Toledo MV, Salmeron V, Gonzalez-Lopez J (1991) Biological characteristics of Azotobacter spp. in natural environments. Trends Soil Sci 1:15–23Google Scholar
  117. Masalha J, Kosegarten H, Elmaci O, Mengal K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fertil Soils 30:433–439Google Scholar
  118. Matsukuma S, Okuda T, Watanabe J (1994) Isolation of actinomycetes from pine litter layers. Actinomycetologica 8:57–65Google Scholar
  119. McLoughlin TJ, Owens PA, Alt SG (1985) Competition studies with fast growing Rhizobium japonicum strains. Can J Microbiol 31:220–223Google Scholar
  120. Medeot DB, Paulucci NS, Albornoz AI, Fumero MV, Bueno MA, Garcia MB, Woelke MR, Okon Y, Dardanelli MS (2010) Plant growth promoting rhizobacteria improving the legume-rhizobia symbiosis. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer, Berlin, pp 473–494Google Scholar
  121. Medina A, Probanza A, Gutierrez Manero FJ, Azcon R (2003) Interactions of arbuscular-mycorrhizal fungi and Bacillus strains and their effects on plant growth, microbial rhizosphere activity (thymidine and leucine incorporation) and fungal biomass (ergosterol and chitin). Appl Soil Ecol 22:15–28Google Scholar
  122. Mehboob I, Naveed M, Zahir ZA (2009) Rhizobial association with non-legumes: mechanisms and applications. Crit Rev Plant Sci 28:432–456Google Scholar
  123. Mirza BS, Mirza MS, Bano A, Malik KA (2007) Co-inoculation of chickpea with Rhizobium isolates from roots and nodules and phytohormone-producing Enterobacter strains. Aust J Exp Agric 47:1008–1015Google Scholar
  124. Mishra PK, Mishra S, Selvakumar G, Bisht JK, Kundu S, Gupta HS (2009a) Coinoculation 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 25:753–761Google Scholar
  125. Mishra PK, Mishra S, Selvakumar G, Kundu S, Gupta HS (2009b) Enhanced soybean (Glycine max L.) plant growth and nodulation by Bradyrhizobium japonicum-SB1 in presence of Bacillus thuringiensis-KR1. Acta Agric Scand Sect B Soil Plant Sci 59:189–196Google Scholar
  126. Mishra PK, Bisht SC, Ruwari P, Joshi GK, Singh G, Bisht JK, Bhatt JC (2011) Bioassociative effect of cold tolerant Pseudomonas spp. and Rhizobium leguminosarum-PR1 on iron acquisition, nutrient uptake and growth of lentil (Lens culinaris L.). Eur J Soil Biol 47:35–43Google Scholar
  127. Mishra PK, Bisht SC, Mishra S, Selvakumar G, Bisht JK, Gupta HS (2012) Coinoculation of rhizobium leguminosarum-pr1 with a cold tolerant Pseudomonas sp. improves iron acquisition, nutrient uptake and growth of field pea (Pisum sativum L.). J Plant Nutr 35:243–256Google Scholar
  128. Molla AH, Shamsuddin ZH, Halimi MS, Morziah M, Puteh AB (2001a) Potential for enhancement of root growth and nodulation of soybean co-inoculated with Azospirillum and Bradyrhizobium in laboratory systems. Soil Biol Biochem 33:457–463Google Scholar
  129. Molla AH, Shamsuddin ZH, Saud HM (2001b) Mechanism of root growth and promotion of nodulation in vegetable soybean by Azospirillum brasilense. Commun Soil Sci Plant Anal 32:2177–2187Google Scholar
  130. Okazaki T, Takahashi K, Kizuka M, Enokita R (1995) Studies on actinomycetes isolated from plant leaves. Annu Rep Sankyo Res Lab 47:97–106Google Scholar
  131. Okon Y, Itzigsohn R (1995) The development of Azospirillum as a commercial inoculant for improving crop yields. Biotechnol Adv 13:415–424PubMedGoogle Scholar
  132. Okon Y, Itzigsohn R, Burdman S, Hampel M (1995) Advances in agronomy and ecology of the Azospirillum/plant association. In: Tikhonovich IA, Provarov NA, Romanov VI, Newton WE (eds) Nitrogen fixation: fundamentals and applications. Kluwer Academic Publishers, Dordrecht, pp 635–640Google Scholar
  133. Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546PubMedGoogle Scholar
  134. Pan B, Vessey JK, Smith DL (2002) Response of field-grown soybean to co-inoculation with the plant growth promoting rhizobacteria Serratia proteamaculans or Serratia liquefaciens, and Bradyrhizobium japonicum pre-incubated with genistein. Eur J Agron 17:143–153Google Scholar
  135. Pankaj K, Bansal RK, Dabur KR (2011) Effect of rhizobacteria as seedling inoculation on root-knot nematode and plant growth in rice-nursery. Indian J Nematol 41:41–46Google Scholar
  136. Parmer N, Dadarwal KR (1999) Stimulation of nitrogen fixation and induction of flavonoid like compounds by rhizobacteria. J Appl Microbiol 86:36–44Google Scholar
  137. Parniske M, Downie JA (2003) Plant biology: locks, keys and symbioses. Nature 425:569–570PubMedGoogle Scholar
  138. 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 53:287–292Google Scholar
  139. Paul S, Verma OP (1999) Influence of combined inoculation of Azotobacter and Rhizobium on the yield of chickpea. Indian J Microbiol 39:249–251Google Scholar
  140. Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant Soil 174:2–28Google Scholar
  141. Pierson EA, Weller DM (1994) Use of mixtures of fluorescent pseudomonads to suppress take-all and improve the growth of wheat. Phytopathology 84:940–947Google Scholar
  142. Plazinski J, Rolfe BG (1985) Influence of Azospirillum strains on the nodulation of clovers by Rhizobium strains. Appl Environ Microbiol 49:984–989PubMedGoogle Scholar
  143. Podile AR, Laxmi VDV (1998) Seed bacterization with Bacillus subtilis AF 1 increases phenylalanine ammonia-lyase and reduces the incidence of fusarial wilt in pigeonpea. J Phytopathol 146:255–259Google Scholar
  144. Polonenko DR, Kloepper JW, Scher FM (1993) Nodulation promotion bacteria and use thereof. European Patent EP0227336Google Scholar
  145. Prevost D, Drouin P, Laberge S, Bertrand A, Cloutier J, Levesque G (2003) Cold-adapted rhizobia for nitrogen fixation in temperate regions. Can J Bot 81:1153–1161Google Scholar
  146. 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 28:124–129Google Scholar
  147. Radwan SS, Dashti N, El-Nemr I (2005) Enhancing the growth of Vicia faba plants by microbial inoculation to improve their phytoremediation potential for oily desert areas. Int J Phytoremediation 7:19–32PubMedGoogle Scholar
  148. Radwan SS, Dashti N, El-Nemr I, Khanafer M (2007) Hydrocarbon utilization by nodule bacteria and plant growth-promoting rhizobacteria. Int J Phytoremediation 9:475–486PubMedGoogle Scholar
  149. Rai R (1983) Efficacy of associative N2-fixation by streptomycin-resistant mutants of Azospirillum brasilense with genotypes of chickpea Rhizobium strains. J Agric Sci 100:75–80Google Scholar
  150. Rajendran G, Sing F, Desai AJ, Archana G (2008) Enhanced growth and nodulation of pigeon pea by co-inoculation of Bacillus strains with Rhizobium spp. Bioresour Technol 99:544–550Google Scholar
  151. Rautela LS, Chandra R, Pareek RP (2001) Enhancing Rhizobium inoculum efficiency in urdbean by co-inoculation of Azotobacter chroococcum and Bacillus sp. Indian J Pulses Res 14:133–137Google Scholar
  152. Raverker KP, Konde BK (1988) Effect of Rhizobium and Azospirillum lipoferum inoculation on the nodulation, yield and nitrogen uptake of peanut cultivars. Plant Soil 106:249–252Google Scholar
  153. Reddy ASR, Babu JS, Reddy MCS, Khan MM, Rao MM (2011) Integrated nutrient management in pigeon pea (Cajanus cajana). Int J Appl Biol Pharm Technol 2:467–470Google Scholar
  154. Redmond JW, Batle M, Djjordjevic MA, Innes RW, Keumpel PL, Rolfe BG (1986) Flavones induce expression of nodulation genes in Rhizobium. Nature (London) 323:63–635Google Scholar
  155. Reid MS (1995) Ethylene in plant growth, development and senescence. In: Davies PJ (ed) Plant hormone: physiology biochemistry and molecular biology. Kluwer Academic Publishers, Dordrecht, pp 486–508Google Scholar
  156. Reinhold B, Hurek T, Fendrik I, Pot B, Gillis M, Kersters K, Thielemans S, De Ley J (1987) Azospirillum halopraeferens sp. nov., a nitrogen-fixing organism associated with roots of Kallar Grass (Leptochloa fusca (L.) Kunth). Int J Syst Bacteriol 37:43–51Google Scholar
  157. 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 119:341–351Google Scholar
  158. 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 RhizobiumAzospirillum coinoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in Cuba. Plant Soil 312:25–37Google Scholar
  159. Requena BN, Jimenez I, Toro M, Barea JM (1997) Interactions between plant growth promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in Mediterranean semi-arid ecosystem. New Phytol 136:667–677Google Scholar
  160. Richardson AE, Barea JM, McNeil AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339Google Scholar
  161. Rodelas B, Gonzales Lopez J, Martinez Toledo MV, Pozo C, Salmeron V (1999) Influence of Rhizobium/Azotobacter and Rhizobium/Azospirillum combined inoculation on mineral composition of faba bean (Vicia faba L.). Biol Fertil Soils 29:165–169Google Scholar
  162. Rosas SB, Andres JA, Rovera M, Correa NS (2006) Phosphate-solubilizing Pseudomonas putida can influence the rhizobia-legume symbiosis. Soil Biol Biochem 38:3502–3505Google Scholar
  163. 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 coinoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in Cuba. Plant Soil 312:25–37Google Scholar
  164. Rudresh DL, Shivaprakash MK, Prasad RD (2005) Effect of combined application of Rhizobium, phosphate solubilizing bacterium and Trichoderma spp. on growth, nutrient uptake and yield of chickpea (Cicer aritenium L.). Appl Soil Ecol 28:139–146Google Scholar
  165. Russelle MP (2008) Biological dinitrogen fixation in agriculture. In: Schepers JS, Raun WR (eds) Nitrogen in agricultural systems, 2nd edn. Agronomy monograph 22. American Society of Agronomy, Madison, pp 281–359Google Scholar
  166. Salem S, Saidi S, Chihaoui S-A, Mhamdi R (2012) Inoculation of Phaseolus vulgaris, Medicago laciniata and Medicago polymorpha with Agrobacterium sp. strain 10C2 may enhance nodulation and shoot dry weight but does not affect host range specificity. Ann Microbiol 62:1811–1817Google Scholar
  167. Samavat S, Samavat S, Besharati H, Behboudi K (2011) Interaction of rhizobia cultural filtrates with Pseudomonas fluorescens on Bean Damping-off control. J Agric Sci Technol 13:965–976Google Scholar
  168. Schlaman HR, Okker RJH, Lugtenberg BJJ (1992) Regulation of nodulation gene expression by nod D in rhizobia. J Bacteriol 174:5177–5182PubMedGoogle Scholar
  169. Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Annu Rev Genet 32:33–57PubMedGoogle Scholar
  170. Schulze J (2004) How are nitrogen fixation rates regulated in legumes? J Plant Nutr Soil Sci 167:125–137Google Scholar
  171. 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.). Lett Appl Microbiol 42:155–159PubMedGoogle Scholar
  172. Shweta B, Maheshwari DK, Dubey RC, Arora DS, Bajpal VK, Kang SC (2008) Beneficial effects of fluorescent pseudomonads on seed germination, growth promotion, and suppression of charcoal rot in groundnut (Arachis hypogea L.). J Microbiol Biotechnol 18:1578–1583PubMedGoogle Scholar
  173. Siddiqui IA, Ali NI, Zaki MJ, Shaukat SS (2001) Evaluation of Aspergillus species for the biocontrol of Meloidogyne javanica in mungbean. Nematol Medit 29:115–121Google Scholar
  174. Sindhu SS, Dadarwal KR (2001) Chitinolytic and cellulolytic Pseudomonas sp. antagonistic to fungal pathogen enhances nodulation by Mesorhizobium sp. Cicer in chickpea. Microbiol Res 156:353–358PubMedGoogle Scholar
  175. Sindhu SS, Gupta SK, Dadarwal KR (1999) Antagonistic effect of Pseudomonas spp. on pathogenic fungi and enhancement of growth of green gram (Vigna radiate). Biol Fertil Soils 29:62–68Google Scholar
  176. Sindhu SS, Suneja S, Goel AK, Parmar N, Dadarwal KR (2002) Plant growth promoting effects of Pseudomonas sp. on coinoculation with Mesorhizobium sp. Cicer strain under sterile and “wilt sick” soil conditions. Appl Soil Ecol 19:57–64Google Scholar
  177. 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 57:715–726Google Scholar
  178. Sivaramaiah N, Malik DK, Sindhu SS (2007) Improvement in symbiotic efficiency of chickpea (Cicer arietinum) by coinoculation of Bacillus strains with Mesorhizobium sp. Cicer. Indian J Microbiol 47:51–56PubMedGoogle Scholar
  179. Soe KM, Bhromsiri A, Karladee D, Yamakawa T (2012) Effects of endophytic actinomycetes and Bradyrhizobium japonicum strains on growth, nodulation, nitrogen fixation and seed weight of different soybean varieties. Soil Sci Plant Nutr 58:319–325Google Scholar
  180. Spaepen S, Vanderleyden J, Remans R (2007) Indol-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448PubMedGoogle Scholar
  181. Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annu Rev Microbiol 54:257–288PubMedGoogle Scholar
  182. Srinivasan M, Holl EB, Petersen DJ (1996) Influence of indole acetic acid producing Bacillus isolates on the nodulation of Phaseolus vulgaris by Rhizobium etli under gnotobiotic conditions. Can J Microbiol 42:1006–1014Google Scholar
  183. Srinivasan M, Petersen DJ, Holl FB (1997) Nodulation of Phaseolus vulgaris by Rhizobium etli in the presence of Bacillus. Can J Microbiol 43:1–8Google Scholar
  184. 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 16:5919–5926Google Scholar
  185. Star L, Matan O, Dardanelli MS, Kapulnik Y, Burdman S, Okon Y (2012) The Vicia sativa spp. nigra – Rhizobium leguminosarum bv. viciae symbiotic interaction is improved by Azospirillum brasilense. Plant Soil 356:165–174Google Scholar
  186. Tarrand JJ, Krieg NR, Dobereiner J (1978) A taxonomic study of the Azospirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. Nov. and Azospirillum brasilense sp. nov. Can J Microbiol 24:967–980PubMedGoogle Scholar
  187. Tate RL (1995) Soil microbiology (symbiotic nitrogen fixation). Wiley, New York, pp 307–333Google Scholar
  188. Tchebotar VK, Kang UG, Asis CA Jr, Akao S (1998) The use of GUS-reporter gene to study the effect of Azospirillum-Rhizobium coinoculation on nodulation of white clover. Biol Fertil Soils 27:349–352Google Scholar
  189. Tilak KVBR, Ranganayaki N, Manoharachari C (2006) Synergistic effects of plant-growth promoting rhizobacteria and Rhizobium on nodulation and nitrogen fixation by pigeon pea (Cajanus cajan). Eur J Soil Sci 57:67–71Google Scholar
  190. 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 Wyec108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171PubMedGoogle Scholar
  191. Tsigie A, Tilak KVBR, Saxena AK (2011) Field response of legumes to inoculation with plant growth-promoting rhizobacteria. Biol Fertil Soils 47:971–974Google Scholar
  192. Tsigie A, Tilak KVBR, Anil KS (2012) Field response of legumes to inoculation with plant growth-promoting rhizobacteria. Biol Fertil Soils 47:971–974Google Scholar
  193. Valverde A, Burgos A, Fiscella T, Rivas R, Velazquez E, Rodriguez-Barrueco C, Cervantes E, Chamber M, Igual JM (2006) Differential effects of coinoculations with Pseudomonas jessenii PS06 (a phosphate-solubilizing bacterium) and Mesorhizobium ciceri C-2/2 strains on the growth and seed yield of chickpea under greenhouse and field conditions. Plant Soil 287:43–50Google Scholar
  194. Vargas LK, Lisboa BB, Schlindwein G, Granada CE, Giongo A, Beneduzi A, Passaglia A, Luciane-Maria P (2009) Occurrence of plant growth-promoting traits in clover-nodulating rhizobia strains isolated from different soils in rio grande do sul state. Rev Bras Ciênc Solo 33:1227–1235Google Scholar
  195. Verma 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 43:605–621Google Scholar
  196. Vessey JK, Buss TJ (2002) Bacillus cereus UW85 inoculation effects on growth, nodulation and N-accumulation in grain legumes, controlled environment studies. Can J Plant Sci 82:282–290Google Scholar
  197. Vijila K, Jebaraj S (2008) Studies on the improvement of Rhizobium-green gram [Vigna radiata (L.) Wilczek] symbiosis in low nutrient, acid stress soils. Legume Res 31:126–129Google Scholar
  198. 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 251:47–54Google Scholar
  199. Vivas A, Marulanda A, Ruiz-Lozana JM, Barea JM, Azcon R (2003) Influence of a Bacillus sp. on physiological activities of two arbuscular mycorrhizal fungi and on plant responses to PEG-induced drought stress. Mycorrhiza 13:249–256PubMedGoogle Scholar
  200. Vivas A, Barea JM, Biro B, Azcon R (2006) Effectiveness of autochthonous bacterium and mycorrhizal fungus on Trifolium growth, symbiotic development and soil enzymatic activities in Zn contaminated soil. J Appl Microbiol 100:587–598PubMedGoogle Scholar
  201. Volpin H, Burman S, Castro-Sowinski S, Kapulink Y, Okon Y (1996) Inoculation with Azospirillum increased exudation of rhizobial nod-gene inducers by alfalfa roots. Mol Plant Microbe Interact 5:388–394Google Scholar
  202. 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 55:315–323Google Scholar
  203. 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 170:283–287Google Scholar
  204. Wasule DL, Wadyalkar SR, Buldeo AN (2003) Effect of phosphate solubilizing bacteria on role of Rhizobium on nodulation by soybean. In: Velazquez E (ed) First international meeting on microbial phosphate solubilization, Salamanca, Spain. Springer, Dordrecht, pp 139–142Google Scholar
  205. Weller DM (2007) Pseudomonas biological control agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256PubMedGoogle Scholar
  206. Yadegari M, Rahmani HA, Noormohammadi G, Ayneband A (2008) Evaluation of bean (Phaseolus vulgaris) seed inoculation with Rhizobium phaseoli and plant growth-promoting rhizobacteria on yield and yield components. Pak J Biol Sci 11:1935–1939PubMedGoogle Scholar
  207. Yahalom E, Okon Y, Dovrat A (1987) Azospirillum effects on susceptibility to Rhizobium nodulation and on nitrogen fixation of several forage legumes. Can J Microbiol 33:510–514Google Scholar
  208. Yahalom E, Okon Y, Dovrat A (1990) Possible mode of action of Azospirillum brasilense strain on the root morphology and nodule formation in burr medic (Medicago polymorpha). Can J Microbiol 36:10–14Google Scholar
  209. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189Google Scholar
  210. Yuming B, Xiaomin Z, Smith DL (2003) Enhanced soybean plant growth resulting from co-inoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1778Google Scholar
  211. Yuttavanichakul W, Lawongsa P, Wongkaew S, Teaumroong N, Boonkerd N, Nomura N, Tittabutr P (2012) Improvement of peanut rhizobial inoculant by incorporation of plant growth promoting rhizobacteria (PGPR) as biocontrol against the seed borne fungus, Aspergillus niger. Biol Control 63:87–97Google Scholar
  212. Zahir ZA, Zafar-ul-Hye M, Sajjad S, Naveed M (2011) Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for coinoculation with Rhizobium leguminosarum to improve growth, nodulation, and yield of lentil. Biol Fertil Soils 47:457–465Google Scholar
  213. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Rev 63:968–989Google Scholar
  214. Zaidi A, Khan MS, Amil M (2003) Interactive effect of rhizotrophic microorganisms on yield and nutrient uptake of chickpea (Cicer arietinum L.). Eur J Agron 19:15–21Google Scholar
  215. Zaidi A, Khan MS, Aamil M (2004) Bioassociative effect of rhizospheric microorganisms on growth, yield, and nutrient uptake of green gram. J Plant Nutr 27:601–612Google Scholar
  216. Zhang F, Dashti N, Hynes RK, Smith DL (1996) Plant growth promoting rhizobacteria and soybean [Glycine max (L.) Merr.] nodulation and nitrogen fixation at suboptimal root zone temperatures. Ann Bot 77:453–460Google Scholar
  217. Zhang F, Dashti N, Hynes RK, Smith DL (1997) Plant growth-promoting rhizobacteria and soybean [Glycine max (L.) Merr.] nodulation and nitrogen fixation at suboptimal root zone temperatures. Ann Bot 77:452–459Google Scholar

Copyright information

© Springer India 2013

Authors and Affiliations

  • Ijaz Mehboob
    • 1
  • Muhammad Naveed
    • 1
    • 2
  • Zahir A. Zahir
    • 1
  • Angela Sessitsch
    • 2
  1. 1.Institute of Soil and Environmental SciencesUniversity of AgricultureFaisalabadPakistan
  2. 2.Bioresources UnitAIT Austrian Institute of Technology GmbHTullnAustria

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