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Rhizobial Inoculants for Sustainable Agriculture: Prospects and Applications

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Biofertilizers for Sustainable Agriculture and Environment

Part of the book series: Soil Biology ((SOILBIOL,volume 55))

Abstract

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.

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References

  • 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 1:17–22

    Google Scholar 

  • 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 12:1–7

    Article  CAS  Google Scholar 

  • Abrar T (2017) Isolation and characterization of rhizobia from rhizosphere and root nodule of cowpea. IJNRIS 4:1–7

    Google Scholar 

  • Afzal A, Bano A (2008) Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum). Inter J Agric Biol 10:85–88

    CAS  Google Scholar 

  • Afzal A, Bano A, Fatima M (2010) Higher soybean yield by inoculation with N-fixing and P-solubilizing bacteria. Agron Sustain Dev 30:487–495

    Article  CAS  Google Scholar 

  • 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 213:72–85

    Article  CAS  Google Scholar 

  • 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 35:9–21

    Google Scholar 

  • Ahemad M, Khan MS (2010) Growth promotion and protection of lentil (Lens esculenta) against herbicide stress by Rhizobium species. Ann Microbiol 60:735–745

    Article  CAS  Google Scholar 

  • 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 20:661–669

    Article  CAS  PubMed  Google Scholar 

  • 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 86:384–388

    Article  CAS  PubMed  Google Scholar 

  • Ahemad M, Khan MS (2011c) Effect of tebuconazole-tolerant and plant growth promoting Rhizobium isolate MRP1 on pea-Rhizobium symbiosis. Sci Hort 129:266–272

    Article  CAS  Google Scholar 

  • Ahemad M, Khan MS (2012) Effects of pesticides on plant growth promoting traits of Mesorhizobium strain MRC4. J Saudi Soc Agric Sci 11:63–71

    CAS  Google Scholar 

  • 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, Pakistan

    Google Scholar 

  • Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181

    Article  CAS  PubMed  Google Scholar 

  • 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 57:578–589

    Article  CAS  PubMed  Google Scholar 

  • 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 29–44

    Chapter  Google Scholar 

  • 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 32:158–166

    Google Scholar 

  • 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 63:170–176

    Article  CAS  PubMed  Google Scholar 

  • 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 51:557–564

    Google Scholar 

  • Ahmed E, Holmstrom SJM (2014) Siderophores in environmental research: roles and applications. Microb Biotechnol 7:196–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 15:415–421

    Article  PubMed  CAS  Google Scholar 

  • 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 263–292

    Chapter  Google Scholar 

  • 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 79:1660–1668

    Article  CAS  PubMed  Google Scholar 

  • 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 66:3393–3398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Falih AMK (2002) Factors affecting the efficiency of symbiotic nitrogen fixation by Rhizobium. Pak J Biol Sci 5:1277–1293

    Article  Google Scholar 

  • 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 5:30–38

    Google Scholar 

  • 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 6:1–12

    Google Scholar 

  • Al-Mughrabi KI (2010) Biological control of fusarium dry rot and other potato tuber diseases using Pseudomonas fluorescens and Enterobacter cloacae. Biol Control 53:280–284

    Article  Google Scholar 

  • Andrews M, Lea PJ, Raven JA, Azevedo RA (2009) Nitrogen use efficiency. 3. Nitrogen fixation: genes and costs. Ann Appl Biol 155:1–13

    Article  CAS  Google Scholar 

  • 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 17

    Google Scholar 

  • 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, Pakistan

    Google Scholar 

  • Argaw A (2016) Effectiveness of Rhizobium inoculation on common bean productivity as determines by inherent soil fertility status. J Crop Sci Biotech 19:311–322

    Article  Google Scholar 

  • 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 7:20

    Article  Google Scholar 

  • 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 27:17–29

    Google Scholar 

  • 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 6:1–16

    Article  Google Scholar 

  • Arkhipova TN, Prinsen EA, Veselov SU, Martinenko EV, Melentiev LV, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315

    Article  CAS  Google Scholar 

  • 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 81:673–677

    Google Scholar 

  • Arshad M, Frankenberger WT Jr (2002) Ethylene: agricultural sources and applications. Ann Bot 90(3):424

    Article  Google Scholar 

  • 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 5:564–570

    CAS  Google Scholar 

  • 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 40:157–162

    CAS  Google Scholar 

  • 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. https://doi.org/10.1016/j.bcab.2015.09.004i

    Article  Google Scholar 

  • 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):17–20

    Google Scholar 

  • 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 47:941–954

    Article  CAS  Google Scholar 

  • 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):791–798

    CAS  Google Scholar 

  • Bano SA, Iqbal SM (2016) Biological nitrogen fixation to improve plant growth and productivity. IJAIR 4(4):15

    Google Scholar 

  • 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):434–438

    Article  CAS  Google Scholar 

  • Bellenger JP, Wichard T, Kustka AB, Kraepiel AML (2008) Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores. Nat Geosci 1:243–246

    Article  CAS  Google Scholar 

  • 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 63:94–104

    Article  Google Scholar 

  • 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 1:5–10

    Google Scholar 

  • 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 36:331–337

    Google Scholar 

  • 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):138–141

    Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350

    Article  CAS  PubMed  Google Scholar 

  • 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 76:4626–4632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 131–145

    Chapter  Google Scholar 

  • Boiero L, Perrig D, Masciarelli O, Penna C, Cassan F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880

    Article  CAS  PubMed  Google Scholar 

  • Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503

    Article  CAS  PubMed  Google Scholar 

  • 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 11:1079–1091

    Article  CAS  PubMed  Google Scholar 

  • 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 37:573–579

    Article  CAS  Google Scholar 

  • Bumunang EW, Babalola OO (2014) Characterization of Rhizobacteria from field grown genetically modified (GM) and non-GM Maizes. Braz Arch Biol Technol 57:1–8

    Article  CAS  Google Scholar 

  • Burgess CM, Smid EJ, Sinderen D (2009) Bacterial vitamin B2, B11 and B12 overproduction: an overview. Int J Food Microbiol 133:1–7

    Article  CAS  PubMed  Google Scholar 

  • Carson KC, Meyer JM, Dillworth MJ (2000) Hydroxamate siderophores of root nodule bacteria. Soil Biol Biochem 32:11–21

    Article  CAS  Google Scholar 

  • 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):28–35

    Article  CAS  Google Scholar 

  • Castellane TCL, Otoboni AMMB, Lemos EGM (2015) Characterization of exopolysaccharides produced by rhizobia species. R Bras Ci Solo 39:1566–1575

    Article  Google Scholar 

  • Castro S, Furlan A, Llanes AA, Luna V (2012) International scholarly research network. ISRN Agronomy. https://doi.org/10.5402/2012/318083

    Article  CAS  Google Scholar 

  • 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 196:160–167

    Article  Google Scholar 

  • Chalk PM, Souza RDF, Urquiaga S, Alves BJR, Boddy RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol Biochem 38:2944–2951

    Article  CAS  Google Scholar 

  • 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 28:86–89

    Google Scholar 

  • Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere competent Mesorhizobium loti MP6 induces root hair curling, inhibits Sclerotinia sclerotiorum and enhances growth of Indian mustard (Brassica campestris). Braz J Microbiol 38:128–130

    Article  Google Scholar 

  • Chaudri AM, Allain CMG, Barbosa-Jefferson VL, Nicholson FA, Chambers BJ, McGrath SP (2000) A study of the impacts of Zn and Cu on two rhizobial species in soils of a long-term field experiment. Plant Soil 221:167–179

    Article  CAS  Google Scholar 

  • Cheung KH, Gu JD (2007) Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior Biodegradation 59:8–15

    Article  CAS  Google Scholar 

  • Chi F, Yang P, Han F, Jing Y, Shen S (2010) Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021. Proteomics 10:1861–1874

    Article  CAS  PubMed  Google Scholar 

  • 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 84:79–88

    Article  Google Scholar 

  • 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):7819–7825

    Article  CAS  Google Scholar 

  • D’Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R–105R

    Article  PubMed  Google Scholar 

  • Dakora FD (2003) Defining new roles for plant and rhizobial molecules in sole and mixed plant cultures involving symbiotic legumes. New Phytol 58:39–49

    Article  CAS  Google Scholar 

  • 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 5:445–452

    Google Scholar 

  • 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 109–127

    Chapter  Google Scholar 

  • Dazzo FB, Yanni YG, Rizk R, Zidan M, Gomaa M, Abu-Baker, Squartini A, Jing Y, Chi F, Shen SH (2005) Recent studies on the Rhizobium cereal association. In: Wang YP, Lin M, Tian ZX, Elmericj C, Newton WE (eds) Biological nitrogen fixation: sustainable agriculture and the environment. Proceedings of the 14th international nitrogen fixation congress. Springer, Dordrecht, pp 379–380

    Chapter  Google Scholar 

  • De Smet I, Zhang H, Inze D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439

    Article  PubMed  CAS  Google Scholar 

  • Denison RF, Kiers ET (2011) Life histories of symbiotic rhizobia and mycorrhizal fungi. Curr Biol 21:R775–R785

    Article  CAS  PubMed  Google Scholar 

  • Deshwal VK, Chaubey A (2014) Isolation and characterization of Rhizobium leguminosarum from root nodule of Pisum sativum L. J Academia Industrial Res 2:464–467

    CAS  Google Scholar 

  • Dhami N, Prasad B (2009) Increase in root nodulation and crop yield of soybean by native Bradyrhizobium japonicum strains. J Plant Sci 6:1–3

    Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Donot F, Fontana A, Baccou JC, Schorr-Galindo S (2012) Microbial exopolysaccharides: main examples of synthesis, excretion, genetics and extraction. Carbohydr Polym 87:951–962

    Article  CAS  Google Scholar 

  • Duan J, Muller KM, Charles TC, Vesely S, Glick BR (2009) 1-Aminocyclopropane-1carboxylate (ACC) deaminase gene in Rhizobium from Southern Saskatchewan. Microbial Ecol 57:423–436

    Article  CAS  Google Scholar 

  • 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 58–66

    Google Scholar 

  • 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 3:721–730

    Google Scholar 

  • 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 33:2104–2119

    Article  CAS  Google Scholar 

  • Fan LM, Maa ZQ, Liang JQ, Li HF, Wangc ET, Wei GH (2011) Characterization of a copper-resistant symbiotic bacterium isolated from Medicago lupulina growing in mine tailings. Bioresour Technol 102:703–709

    Article  CAS  PubMed  Google Scholar 

  • Fatima Z, Bano A, Sial R, Aslam M (2008) Response of chickpea to plant growth regulators on nitrogen fixation and yield. Pak J Bot 40:2005–2013

    CAS  Google Scholar 

  • 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 43:805–809

    Article  CAS  Google Scholar 

  • 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):6–11

    CAS  Google Scholar 

  • 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 40:182–188

    Article  Google Scholar 

  • 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):17–32

    Google Scholar 

  • Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the house of biofilm cells. J Bacteriol 189:7945–7947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 176:876–882

    Article  CAS  Google Scholar 

  • Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):51–56

    Article  Google Scholar 

  • 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):e33977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0038122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.4172/2329-8863

    Article  Google Scholar 

  • Gauri SAK, Bhatt RB, Pant S, Bedi MK, Naglot A (2011) Characterization of Rhizobium isolated from root nodules of Trifolium alexandrinum. J Agric Technol 7:1705–1723

    Google Scholar 

  • Geetha SJ, Joshi SJ (2013) Engineering Rhizobial bioinoculants: a strategy to improve iron nutrition. Sci World J 2013:1–15

    Google Scholar 

  • 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):435–440

    Article  CAS  Google Scholar 

  • Giller KE (2001) Nitrogen fixation in tropical cropping systems. CAB International, Wallingford

    Book  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:15. https://doi.org/10.6064/2012/963401

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1093/jxb/erp175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gontijo JB, Andrade GVS, Baldotto MA, Baldotto LEB (2018) Bioprospecting and selection of growth-promoting bacteria for Cymbidium sp. Orchids Sci Agric 75(5):368–374

    Article  CAS  Google Scholar 

  • Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CCL, Krishnamurthy L (2014) Plant growth promoting rhizobia: challenges and opportunities. Biotechnology 3:1–23

    Google Scholar 

  • 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 9:566–576

    Article  CAS  Google Scholar 

  • Grichko VP, Glick BR (2001) Amelioration of flooding stress by ACC deaminase containing plant growth promoting bacteria. Plant Physiol Biochem 39:11–17

    Article  CAS  Google Scholar 

  • Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2010) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240

    Article  Google Scholar 

  • 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 44:109–114

    Google Scholar 

  • Hafeez FY, Hassan Z, Naeem F, Basher A, Kiran A, Khan SA, Malik KA (2008) Rhizobium leguminosarum bv. viciae strain LC–31: analysis of novel bacteriocin and ACC-deaminase gene(s). In: Dakora FD, Chimphango SBM, Valentine AJ, Elmerich C, Newton WE (eds) Biological nitrogen fixation: towards poverty alleviation through sustainable agriculture. Springer, Dordrecht, pp 247–248

    Chapter  Google Scholar 

  • 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:e0160006

    Article  Google Scholar 

  • Haque MA, Bala P, Azad AK (2014) Performance of lentil varieties as influenced by different Rhizobium inoculations. Bangladesh Agron J 17:41–46

    Article  Google Scholar 

  • 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 32:241–248

    Google Scholar 

  • 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):1–7

    Google Scholar 

  • 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. https://doi.org/10.1080/00380768.2018.1452574

    Article  Google Scholar 

  • 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 155:31–37

    Article  Google Scholar 

  • 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 98:32–39

    Article  CAS  Google Scholar 

  • 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 30:13–17

    CAS  Google Scholar 

  • Hussain MB, Zahir ZA, Asghar HN, Asghar M (2014) Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat? Int J Agric Biol 16:3–13

    CAS  Google Scholar 

  • 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):1681–1689

    CAS  Google Scholar 

  • 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):1213–1222

    CAS  PubMed  Google Scholar 

  • 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 388:211–227

    Article  CAS  Google Scholar 

  • 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 28:891–899

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1038/s41598-017-18632-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.3389/fmicb02593

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 52:473–476

    Article  CAS  Google Scholar 

  • 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 9:1–13

    Article  Google Scholar 

  • Karpagam T, Nagalakshmi PK (2014) Isolation and characterization of phosphate solubilizing microbes from agricultural soil. J Curr Microbiol App Sci 3(3):601–614

    CAS  Google Scholar 

  • 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 38:367–374

    Google Scholar 

  • 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 5:105–112

    Article  Google Scholar 

  • 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 207–220

    Chapter  Google Scholar 

  • Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi—current perspective. Arch Agron Soil Sci 56:73–98

    Article  CAS  Google Scholar 

  • 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 45:27–34

    CAS  Google Scholar 

  • 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 31-62

    Google Scholar 

  • 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):158–159

    Google Scholar 

  • 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 26:1225–1231

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.3389/fpls.2017.00141

    Article  Google Scholar 

  • 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 8:1–12

    Article  Google Scholar 

  • 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 73:327–330

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1007/s11270-011-0944-0

    Article  CAS  Google Scholar 

  • Kulasooriya SA, Ekanayake EMHGS, Kumara RKGK, Bandar AMS (2017) Rhizobial inoculation of Trifolium repens L. in Sri Lanka. J Natn Sci Foundation Sri Lanka 45:361–366

    Article  CAS  Google Scholar 

  • 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 29:591–598

    Article  Google Scholar 

  • 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 2:60–64

    CAS  Google Scholar 

  • Kyei-Boahen S, Slinkard AE, Walley FL (2002) Evaluation of Rhizobial inoculation methods for chickpea. J Agron 94:851–859

    Article  Google Scholar 

  • 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):1616–1626

    Article  CAS  Google Scholar 

  • Leytem AB, Mikkelson RL (2005) The nature of phosphorus in calcareous soils. Better Crops 89:11–13

    Google Scholar 

  • Liu Y, Wu L, Baddeley JA, Watson CA (2011) Models of biological nitrogen fixation of legumes. A review. Agron Sustain Dev 31:155–172

    Article  Google Scholar 

  • 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):e0187947

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lodwig EM, Poole PS (2003) Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci 22:37–38

    Article  CAS  Google Scholar 

  • 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 422:722–726

    Article  CAS  PubMed  Google Scholar 

  • 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):5891–5897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 38:124–130

    Google Scholar 

  • 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 7:784–793

    CAS  Google Scholar 

  • Malisorn K, Prasarn C (2014) Isolation and characterization of Rhizobium spp. from root of legume plants species. Agron J 4:157–160

    Google Scholar 

  • 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):51–54

    Google Scholar 

  • 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 35:1477–1490

    Article  CAS  Google Scholar 

  • 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 62:8–14

    Article  CAS  Google Scholar 

  • 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 132:21–27

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.3390/genes8120360

    Article  CAS  PubMed Central  Google Scholar 

  • 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 5:71

    Article  CAS  Google Scholar 

  • Martyniuk S, Kozieł M, Gałązk A (2018) Response of pulses to seed or soil application of rhizobial inoculants. Ecol Chem Eng S 25:323–329

    CAS  Google Scholar 

  • 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 30:433–439

    Article  CAS  Google Scholar 

  • Masciarelli O, Llanes A, Luna V (2014) A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol Res 169(7–8):609–661

    Article  CAS  PubMed  Google Scholar 

  • Matiru VN, Dakora FD (2005) The rhizosphere signal molecule lumichrome alters seedling development in both legumes and cereals. New Phytol 166:439–444

    Article  CAS  PubMed  Google Scholar 

  • McAdam EL, Reid JB, Foo E (2018) Gibberellins promote nodule organogenesis but inhibit the infection stages of nodulation. J Exp Bot 69:2117–2130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 349:69–87

    Article  CAS  Google Scholar 

  • Mehboob I, Naveed M, Zahir ZA (2009) Rhizobial association with non-legumes: mechanisms and applications. Crit Rev Plant Sci 28:432–456

    Article  CAS  Google Scholar 

  • Mehboob I, Zahir ZA, Arshad M, Tanveer A, Farroq-E-Azam (2011) Growth promoting activities of different Rhizobium sp. in wheat. Pak J Bot 43:1643–1650

    Google Scholar 

  • 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. https://doi.org/10.4172/2155-6202.1000012

    Article  Google Scholar 

  • Mia MD, Shamsuddin ZH, Wahab Z, Marziah M (2005) High yielding and quality banana production through plant growth promoting rhizobacterial (PGPR) inoculation. Fruits 60:179–185

    Article  Google Scholar 

  • 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 47:1008–1015

    Article  Google Scholar 

  • 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 60:799–815

    Article  CAS  Google Scholar 

  • Mohammed H, Sahid IB (2016) Evaluation of Rhizobium inoculation in combination with phosphorus and nitrogen fertilization on groundnut growth and yield. J Agron 15:142–146

    Article  CAS  Google Scholar 

  • 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):705–708

    Article  CAS  Google Scholar 

  • 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 583:475–480

    Article  CAS  PubMed  Google Scholar 

  • 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):1574–1581

    CAS  Google Scholar 

  • 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 22:209–216

    Article  Google Scholar 

  • 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):117–123

    Google Scholar 

  • Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7:869–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 53:1141–1149

    Article  CAS  PubMed  Google Scholar 

  • Naidu VSGR, Panwar JDS, Annapurna K (2004) Effect of synthetic auxins and Azorhizobium caulinodans on growth and yield of rice. Indian J Microbiol 44:211–213

    CAS  Google Scholar 

  • Neubauer U, Furrer G, Kayser A, Schulin R (2000) Siderophores, NTA, and citrate: potential soil amendments to enhance heavy metal mobility in phytoremediation. Int J Phytoremed 2:353–368

    Article  CAS  Google Scholar 

  • Nosheen A, Bano A (2014) Potential of plant growth promoting rhizobacteria and chemical fertilizers on soil enzymes and plant growth. Pak J Bot 46:1521–1530

    Google Scholar 

  • Nyoki D, Ndakidemi PA (2014) Effects of phosphorus and Bradyrhizobium japonicum on growth and chlorophyll content of cowpea. Am J Exp Agric 4:1120–1136

    CAS  Google Scholar 

  • 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 32:241–248

    CAS  Google Scholar 

  • Oldroyd GED (2007) Nodules and hormones. Science 315(5808):52–53

    Article  CAS  PubMed  Google Scholar 

  • 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 44:335–342

    Article  CAS  PubMed  Google Scholar 

  • 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):441–451

    Article  Google Scholar 

  • Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220

    Article  CAS  PubMed  Google Scholar 

  • 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 173:1–9

    Article  CAS  PubMed  Google Scholar 

  • 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):623–627

    Article  Google Scholar 

  • Pierson EA, Weller DM (1994) Use of mixtures of fluorescent pseudomonads to suppress take-all and improve the growth of wheat. J Phytopathol 84:940–947

    Article  Google Scholar 

  • 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 9:57–65

    Article  CAS  Google Scholar 

  • Qurashi AW, Sabri AN (2012) Bacterial exopolysaccharides and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J Microbiol 43:1183–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raja D, Takankhar VJ (2018) Response of liquid biofertilizers (Bradyrhizobium and PSB) on nutrient content in soybean. IJCMAS 7(5):3701–3706

    Google Scholar 

  • Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149

    Article  CAS  PubMed  Google Scholar 

  • 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):1696–1704

    Google Scholar 

  • Ravikumar R (2012) Growth effects of Rhizobium inoculation in some Legume plants. Int J Curr Sci 1:1–6

    Google Scholar 

  • 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 59:1559–1571

    Article  Google Scholar 

  • Raychaudhuri N, Das SK, Chakraborty PK (2005) Symbiotic effectiveness if siderophore overproducing mutant of Mesorhizobium ciceri. Pol J Microbiol 54:37–41

    PubMed  Google Scholar 

  • 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 1–16

    Google Scholar 

  • 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 302:149–161

    Article  CAS  Google Scholar 

  • 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):247–254

    Article  CAS  Google Scholar 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 120:35–43

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodrigues C, Laranjo M, Oliveira S (2006) Effect of heat and pH stress in the growth of chickpea mesorhizobia. Curr Microbiol 53:1–7

    Article  CAS  PubMed  Google Scholar 

  • 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):2037–2050

    Article  CAS  Google Scholar 

  • 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 287:15–21

    Article  CAS  Google Scholar 

  • Rodriguez-Gacio MC, Matilla-Vázquez MA, Matilla AJ (2009) Seed dormancy and ABA signaling: the breakthrough goes on. Plant Signal Behav 4:1035–1048

    Article  CAS  Google Scholar 

  • Rodriguez-Navarro DN, Oliver IM, Contreras MA, Ruiz-Sainz JE (2010) Soybean interactions with soil microbes, agronomical and molecular aspects. Agron Sustain Dev 31:173–190

    Article  CAS  Google Scholar 

  • Rokhzadi A, Toashih V (2011) Nutrient uptake and yield of chickpea (Cicer arietinum L.) inoculated with plant growth promoting rhizobacteria. Aust J Crop Sci 1:44–48

    Google Scholar 

  • 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 41:2568–2572

    Article  CAS  Google Scholar 

  • 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 186:133–145

    Article  Google Scholar 

  • 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):2264–2269

    Article  CAS  Google Scholar 

  • 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 190:7200–7208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 89–112

    Chapter  Google Scholar 

  • 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):253–268

    CAS  Google Scholar 

  • 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 94:109–118

    Google Scholar 

  • 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 23:159–161

    Google Scholar 

  • Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30

    Google Scholar 

  • 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 29:1099–1106

    Article  CAS  PubMed  Google Scholar 

  • 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 34:635–648

    Article  CAS  PubMed  Google Scholar 

  • 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 108:1–13

    Article  Google Scholar 

  • Samavat S, Besharati H, Behboudi K (2011) Interactions of rhizobia cultural filtrates with Pseudomonas fluorescens on bean damping-off control. J Agri Sci Tech 13:965–976

    Google Scholar 

  • 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 18:387–395

    Google Scholar 

  • 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 46:17–26

    Article  CAS  Google Scholar 

  • 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 10:2150–2163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 105:19–24

    Article  CAS  Google Scholar 

  • 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 85:371–381

    Article  CAS  PubMed  Google Scholar 

  • 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):449–454

    Google Scholar 

  • 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 42:155–159

    Article  CAS  Google Scholar 

  • 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):1300–1307

    CAS  PubMed  Google Scholar 

  • 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):342–360

    Google Scholar 

  • Sharma P, Sardana V, Kandola SS (2011) Response of groundnut (Arachis hypogaea L.) to Rhizobium inoculation. Libyan Agric Res Cen J Intl 2:101–104

    Google Scholar 

  • Sharma P, Padh H, Shrivastava N (2013) Hairy root cultures: a suitable biological system for studying secondary metabolic pathways in plants. Eng Life Sci 13:62–75

    Article  CAS  Google Scholar 

  • 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 7:441–447

    Article  CAS  Google Scholar 

  • 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):534–540

    Google Scholar 

  • 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. https://doi.org/10.7717/peerj.1291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh Z, Singh G (2018) Role of Rhizobium in chickpea (Cicer arietinum) production – a review. Agric Rev 39(1):31–39

    Google Scholar 

  • Singh RK, Mishra RPN, Jaiswal HK, Kumar V, Pandev SP, Rao SB, Annapurna K (2006) Isolation and identification of natural endophytic rhizobia from rice (Oryza sativa L.) through rDNA PCR-RFLP and sequence analysis. Curr Microbiol 52:345–349

    Article  CAS  PubMed  Google Scholar 

  • 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 6:1–14

    CAS  Google Scholar 

  • 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):1591–1593

    CAS  Google Scholar 

  • Singha B, Mazumder PB, Pandey P (2016) Characterization of plant growth promoting rhizobia from root nodule of Crotalaria pallida grown in Assam. IJBT 15:210–216

    CAS  Google Scholar 

  • 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 8:1–15

    Google Scholar 

  • Skaar EP (2010) The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6:1–4

    Article  CAS  Google Scholar 

  • Skorupska A, Janczarek M, Marczak M, Mazur A, Krol J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microbiol Cell Fact 5:1–19

    Article  CAS  Google Scholar 

  • Sogut T (2006) Rhizobium inoculation improves yield and nitrogen accumulation in soybean (Glycine max) cultivars better than fertilizer. New Zeal J Crop Hort 34:115–120

    Article  Google Scholar 

  • 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 334:189–197

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.5402/2012/261475

    Article  Google Scholar 

  • 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 21:11632–11639

    Google Scholar 

  • Sridevi M, Mallaiah KV (2009) Phosphate solubilization by Rhizobium strains. Indian J Microbiol 49(1):98–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava LM (2002) Plant growth and development: hormones and environment. Academic, San Diego

    Google Scholar 

  • Stephens JHG, Rask HM (2000) Inoculant production and formulation. Field Crops Res 65:249–258

    Article  Google Scholar 

  • 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 21:958–966

    Article  CAS  PubMed  Google Scholar 

  • Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273

    Article  CAS  PubMed  Google Scholar 

  • Sutherland IW (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9

    Article  CAS  PubMed  Google Scholar 

  • 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 45:914–922

    Article  CAS  PubMed  Google Scholar 

  • 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 3:791–798

    Google Scholar 

  • 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 2013:1–8

    Article  CAS  Google Scholar 

  • Tairo EV, Ndakidemi PA (2013) Bradyrhizobium japonicum inoculation and phosphorus supplementation on growth and chlorophyll accumulation in soybean (Glycine max L.). AJPS 4:2281–2289

    Article  CAS  Google Scholar 

  • Tairo EV, Ndakidemi PA (2014) Macronutrients uptake in soybean as affected by bradyrhizobium japonicum inoculation and phosphorus (p) supplements. AJPS 5:488–496

    Article  CAS  Google Scholar 

  • Tao G, Tian S, Cai M, Xie G (2008) Phosphate solubilizing and mineralizing abilities of bacteria isolated from soils. Pedosphere 18:515–523

    Article  CAS  Google Scholar 

  • Tate RL (1995) Soil microbiology (symbiotic nitrogen fixation). Wiley, New York, pp 307–333

    Google Scholar 

  • 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 10:7585–7591

    Google Scholar 

  • 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 6:1–11

    Article  CAS  Google Scholar 

  • 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 341:209–219

    Article  CAS  Google Scholar 

  • 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 57:29–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 38:493–500

    Article  Google Scholar 

  • 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 60:4163–4166

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 28:99–108

    Article  Google Scholar 

  • Uma C, Sivagurunathan P, Sangeetha D (2013) Performance of Bradyrhizobial isolates under drought conditions. Int J Curr Microbiol App Sci 2:228–232

    Google Scholar 

  • 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 1–22

    Google Scholar 

  • 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 5:148–156

    Article  CAS  Google Scholar 

  • 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):4611–4619

    Article  CAS  Google Scholar 

  • 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 59:850–855

    Article  CAS  PubMed  Google Scholar 

  • Vijayabaskar P, Babinastarlin S, Shankar T, Sivakumar T, Anandapandian KTK (2011) Quantification and characterization of exopolysaccharides from Bacillus subtilis (MTCC 121). Adv Biol Res 5:71–76

    CAS  Google Scholar 

  • Wagner SC (2011) Biological nitrogen fixation. Nat Edu Knowl 2:14

    Google Scholar 

  • 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 46:898–907

    Article  CAS  PubMed  Google Scholar 

  • 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):173–181

    Article  PubMed  CAS  Google Scholar 

  • Wang Q, Liu J, Zhu H (2018) Genetic and molecular mechanisms underlying symbiotic specificity in legume-rhizobium interactions. Front Plant Sci 9:1–8

    Article  Google Scholar 

  • Wani PA, Khan MS (2010) Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem Toxicol 48:3262–3267

    Article  CAS  PubMed  Google Scholar 

  • 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 70:36–45

    Article  CAS  PubMed  Google Scholar 

  • 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 170:283–287

    Article  CAS  Google Scholar 

  • 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 55:33–42

    Article  CAS  PubMed  Google Scholar 

  • 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 43:605–621

    Article  CAS  Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254

    Article  CAS  PubMed  Google Scholar 

  • 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):1547–1555

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.3389/fpls.2017.01961

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 261:144–152

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 11:1935–1939

    Google Scholar 

  • Yang G, Bhuvaneswari TV, Joseph CM, King MD, Phillips DA (2002) Roles for riboflavin in the Sinorhizobium-alfalfa association. Mol Plant-Microbe Interact 5:456–462

    Article  Google Scholar 

  • Yanni YG, Rizk RY, Abd El-Fattah FK, Squartini A, Corich V, Giacomini A, De Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M, Hollingsworth RI, Martinez-Molina E, Mateos P, Velazquez E, Wopereis J, Triplett E, Umali-Gracia M, Anarna JA, Rolfe BG, Ladha JK, Hill J, Mujoo R, Ng PK, Dazzo FB (2001) The beneficial plant growth promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust J Plant Physiol 28:845–870

    CAS  Google Scholar 

  • Zafar-ul-Hye M, Ahmad M, Shahzad SM (2013) Synergistic effect of rhizobia and plant growth promoting rhizobacteria on the growth and nodulation of lentil seedlings under axenic conditions. Soil Environ 32:79–86

    CAS  Google Scholar 

  • 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):798–803

    Google Scholar 

  • 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):958–963

    CAS  PubMed  Google Scholar 

  • Zahir ZA, Shah MK, Naveed M, Akhter MJ (2010) Substrate dependent auxin production by Rhizobium phaseoli improves the growth and yield of Vigna radiata L. under salt stress conditions. J Microbiol Biotechnol 20:1288–1294

    Article  CAS  PubMed  Google Scholar 

  • 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):45–52

    Article  CAS  Google Scholar 

  • 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 6:45–50

    Article  Google Scholar 

  • 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 23:79–86

    Article  Google Scholar 

  • 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 98:1–11

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Soil Science, University College of Agriculture and Environmental Sciences, The Islamia University of Bahawalpur, Bahawalpur, Pakistan

    Iqra Naseer, Maqshoof Ahmad, Iqra Ahmad &  Najm-ul-Seher

  2. University of Agriculture Faisalabad, Sub-campus Burewala, Vehari, Pakistan

    Sajid Mahmood Nadeem

  3. Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad, Pakistan

    Zahir Ahmad Zahir

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  1. Iqra Naseer
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  1. Department of Botany, Swami Shraddhanand College University of Delhi, New Delhi, India

    Bhoopander Giri

  2. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Ram Prasad

  3. College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei, China

    Qiang-Sheng Wu

  4. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Ajit Varma

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Naseer, I., Ahmad, M., Nadeem, S.M., Ahmad, I., Najm-ul-Seher, Zahir, Z.A. (2019). Rhizobial Inoculants for Sustainable Agriculture: Prospects and Applications. In: Giri, B., Prasad, R., Wu, QS., Varma, A. (eds) Biofertilizers for Sustainable Agriculture and Environment . Soil Biology, vol 55. Springer, Cham. https://doi.org/10.1007/978-3-030-18933-4_11

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