Utilization of Endophytic Bacteria Isolated from Legume Root Nodules for Plant Growth Promotion

  • Winston Franz Ríos-Ruiz
  • Renzo Alfredo Valdez-Nuñez
  • Eulogio J. Bedmar
  • Antonio Castellano-HinojosaEmail author
Part of the Sustainable Development and Biodiversity book series (SDEB, volume 23)


For decades, rhizobia were described as the single inhabitant of legume nodules. However, other bacteria, which are not typical rhizobia, are often found within nodules and suggested to affect the behaviour and fitness of the host plant. Here, we highlight their diversity, role in the promotion of legumes growth and in the recuperation of degraded soils. Studies have shown the capacity of Non-Nodular Endophytic Bacteria (NNEB) to stimulate plant growth by direct mechanisms including production of phytohormones such as auxins, facilitation of acquisition of plant resources/nutrients that plants lack such as fixed nitrogen, iron, phosphorous, besides, production of the enzyme 1-aminocyclopropane-1-carboxylate (ACC deaminase) involved in reduction of plant ethylene, etc. Among the indirect mechanisms, those associated to the enhancement of plant growth are production of siderophores, antibiotics and lytic enzymes. Finally, we described greenhouse and field experiments that successfully used NNEB to both increase the growth and yield of legumes and to recover degraded soils.


Legume Plant-growth promotion Nodule Endophytic bacteria Soil 



This study was supported by the ERDF-cofinanced grants PEAGR2012-1968 from Consejería de Economía, Innovación y Ciencia (Junta de Andalucía, Spain). ACH is recipient of a grant of MECD (FPU 2014/01633). The authors thank CONCYTEC (Consejo Nacional de Ciencia y Tecnología) and MINEDU (Ministerio de Educación, Perú) for the financing of projects 8000-2015 and 9500-2015, in recovery of degraded soils, as well as the National University of San Martin.


  1. Abhilash PC, Dubey RK, Tripathi V, Srivastava P, Verma JP, Singh HB (2013) Remediation and management of POPs-contaminated soils in a warming climate: challenges and perspectives. Environ Sci Pollut Res 20:5879–5885. Scholar
  2. Aeron A, Chauhan PS, Dubey RC, Maheshwari DK, Bajpai VK (2015) Root nodule bacteria from Clitoria ternatea L. are putative invasive nonrhizobial endophytes. Can J Microbiol 142:131–142. Scholar
  3. Ahemad M, Khan MS (2011) Insecticide-tolerant and plant growth promoting Bradyrhizobium sp. (Vigna) improves the growth and yield of greengram [Vigna radiata (L.) Wilczek] in insecticide-stressed soils. Symbiosis 54:17–27. Scholar
  4. Alquéres S, Meneses C, Rouws L, Rothballer M, Baldani I, Schmid M, Hartmann A (2013) The bacterial superoxide dismutase and glutathionereductase are crucial for endophytic colonization of rice roots by Gluconacetobacter diazotrophicus PAL5. Mol Plant-Microbe Interact 26:937–945. Scholar
  5. Araújo F, Sérgio A, Figueiredo MVB (2009) Role of plant growth-promoting bacteria in sustainable agriculture. In: Salazar A, Rios I (eds) Sustainable agriculture: technology, planning. Nova Science Publishers, HauppaugeGoogle Scholar
  6. Arone G, Calderón C, Moreno S, Bedmar EJ (2014) Identification of Ensifer strains isolated from root nodules of Medicago hispida grown in association with Zea mays in the Quechua region of the Peruvian Andes. Biol Fertil Soils 50:185–190. Scholar
  7. Arora NK, Kang SC, Maheshwari DK (2001) Isolation of siderophore producing strains of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr Sci 81:673–677Google Scholar
  8. Aserse AA, Räsänen LA, Aseffa F, Hailemariam A, Lindström K (2013) Diversity of sporadic symbionts and nonsymbiotic endophytic bacteria isolated from nodules of woody, shrub, and food legumes in Ethiopia. Appl Microbiol Biotechnol 97:10117–10134. Scholar
  9. Bahroun A, Jousset A, Mhamdi R, Mrabet M, Mhadhbi H (2018) Anti-fungal activity of bacterial endophytes associated with legumes against Fusarium solani: assessment of fungi soil suppressiveness and plant protection induction. Appl Soil Ecol 124:131–148. Scholar
  10. Bai Y, D’Aoust F, Smith DL, Driscoll BT (2002) Isolation of plant-growth-promoting Bacillus strains from soybean root nodules. Can J Microbiol 48:230–238. Scholar
  11. Bao G, Saikkonen K, Wang H, Zhou L, Chen S, Li C, Nan Z (2015) Does endophyte symbiosis resist allelopathic effects of an invasive plant in degraded grassland? Fungal Ecol 17:114–125. Scholar
  12. Barac T, Taghavi S, Borremans B (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583. Scholar
  13. Bashan Y, de-Bashan LE (2010) Microbial Populations of arid lands and their potential for restoration of deserts. In: Dion P. (ed) Soil biology and agriculture in the tropics. Soil biology, vol 21. Springer, BerlinGoogle Scholar
  14. Bashan Y, de-Bashan LE, Prabhu SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33.
  15. Bautista VV, Monsalud R G, Yokota A (2010) Devosia yakushimensis sp. nov., isolated from root nodules of Pueraria lobata (Willd.) Ohwi. Int J Syst Evol Microbiol 60:627–632.
  16. Bautista VV, Monsalud RG, Yokota A (2017) Isolation and Identification of Bacteria from Root Nodules of Philippine Legumes Using 16S rRNA Gene Sequencing. Philipp Agric Sci 100:103–117Google Scholar
  17. Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci USA 110:E1621–E1630. Scholar
  18. Becerra-Castro C, Kidd PS, Rodríguez-Garrido B, Monterroso C, Santos-Ucha P, Prieto-Fernández Á (2013) Phytoremediation of hexachlorocyclohexane (HCH)-contaminated soils using Cytisus striatus and bacterial inoculants in soils with distinct organic matter content. Environ Pollut 178:202–210. Scholar
  19. Beghalem H, Aliliche K, Chriki A, Landoulsi A (2017) Molecular and phenotypic characterization of endophytic bacteria isolated from sulla nodules. Microb Pathog 111:225–231. Scholar
  20. Beijerinck MW, Van Delden A (1902) Ueber die Assimilation des freien Stickstoffs durch Bakterien. Zentralbl Bakteriol B 9:3–43Google Scholar
  21. Berg G, Eberl L, Hartmann A (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 71:4203–4213. Scholar
  22. Bhattacharjee RB, Singh A, Mukhopadhyay SN (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209. Scholar
  23. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350. Scholar
  24. Bisht SC, Mishra PK (2013) Ascending migration of endophytic Bacillus thuringiensis and assessment of benefits to different legumes of NW Himalayas. Eur J Soil Biol 56:56–64. Scholar
  25. Boonsnongcheep P, Prathanturarug S, Takahashi Y, Matsumoto A (2016) Rhizobium puerariae sp. nov., an endophytic bacterium from the root nodules of the medicinal plant Pueraria candollei var. candollei. Int J Syst Evol Microbiol 66:1236–1241. Scholar
  26. Bouchiba Z, Boukhatem ZF, Ighilhariz Z (2017) Diversity of nodular bacteria of Scorpiurus muricatus in western Algeria and their impact on plant growth. Can J Microbiol 63:450–463. Scholar
  27. Boukhatem ZF, Merabet C, Bekki A et al (2016) Nodular bacterial endophyte diversity associated with native Acacia spp. in desert region of Algeria. Afr J Microbiol Res 10:634–645. Scholar
  28. Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37. Scholar
  29. Bulgarelli D, Schlaeppi K, Spaepen S, Loren Ver, van Themaat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. Scholar
  30. Burges A, Epelde L, Blanco F, Becerril JM, Garbisu C (2017) Ecosystem services and plant physiological status during endophyte-assisted phytoremediation of metal contaminated soil. Sci Total Environ 584:329–338. Scholar
  31. Camacho M, Santamaría C, Temprano F, Rodriguez-Navarro DN, Daz A (2001) Co-inoculation with Bacillus sp CECT 450 improves nodulation in Phaseolus vulgaris. Can J Microbiol 47:1058–1062. Scholar
  32. Carvalhais LC, Dennis PG, Fan B et al (2013) Linking plant nutritional status to plant-microbe interactions. PLoS ONE 8:e68555. Scholar
  33. Castellano-Hinojosa A, Bedmar EJ (2017) Methods for Evaluating Plant Growth-Promoting Rhizobacteria Traits. In: Singh HB, Sarma BK, Keswani C (eds) Advances in PGPR Research. CABI international, Oxford, pp 255–274CrossRefGoogle Scholar
  34. Carro L, Spröer C, Alonso P, Trujillo ME (2012) Diversity of Micromonospora strains isolated from nitrogen fixing nodules and rhizosphere of Pisum sativum analyzed by multilocus sequence analysis. Syst Appl Microbiol 35:73–80. Scholar
  35. Carro L, Flores-Félix JD, Cerda-Castillo E (2013) Paenibacillus endophyticus sp. nov., isolated from nodules of Cicer arietinum. Int J Syst Evol Microbiol 63:4433–4438. Scholar
  36. Carro L, Flores-Félix JD, Ramírez-Bahena MH (2014) Paenibacillus lupini sp. nov., isolated from nodules of Lupinus albus. Int J Syst Evol Microbiol 64:3028–3033. Scholar
  37. Carro L, Riesco R, Spröer C, Trujillo ME (2016) Micromonospora ureilytica sp. nov., Micromonospora noduli sp. nov. and Micromonospora vinacea sp. nov., isolated from Pisum sativum nodules. Int J Syst Evol Microbiol 66:3509–3514. Scholar
  38. Carro L, Veyisoglu A, Riesco R, Spröer C, Klenk HP, Sahin N, Trujillo ME (2018) Micromonospora phytophila sp. nov. and Micromonospora luteiviridis sp. nov., isolated as natural inhabitants of plant nodules. Int J Syst Evol Microbiol 68:248–253. Scholar
  39. Castro JLD, Souza MG, Rufini M, Guimarães AA, Rodrigues TL, Moreira FMDS (2017) Diversity and efficiency of rhizobia communities from iron mining areas using cowpea as a trap plant. R Bras Ci Solo 41.
  40. Chen JY, Gu J, Wang ET et al (2014) Wild peanut Arachis duranensis are nodulated by diverse and novel Bradyrhizobium species in acid soils. Syst Appl Microbiol 37:525–532. Scholar
  41. Chinnaswamy A, Coba de la Peña T, Stoll A et al (2018) A nodule endophytic Bacillus megaterium strain isolated from Medicago polymorpha enhances growth, promotes nodulation by Ensifer medicae and alleviates salt stress in alfalfa plants. Ann Appl Biol 172:295–308. Scholar
  42. Chou YJ, Elliott GN, James EK et al (2007) Labrys neptuniae sp. nov., isolated from root nodules of the aquatic legume Neptunia oleracea. Int J Syst Evol Microbiol 57:577–581. Scholar
  43. Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. Scholar
  44. Da Costa EM, Nóbrega RSA, de Carvalho F, Trochmann A, Ferreira LDVM, de Souza Moreira FM (2013) Plant growth promotion and genetic diversity of bacteria isolated from cowpea nodules. Pesq Agropec Bras 48:1275–1284. Scholar
  45. Dary M, Chamber-Pérez MA, Palomares AJ, Pajuelo E (2010) “In situ” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177:323–330. Scholar
  46. De Meyer SE, Willems A (2012) Multilocus sequence analysis of Bosea species and description of Bosea lupini sp. nov., Bosea lathyri sp. nov. and Bosea robiniae sp. nov., isolated from legumes. Int J Syst Evol Microbiol 62:2505–2510. Scholar
  47. De Meyer SE, Coorevits A, Willems A (2012) Tardiphaga robiniae gen. nov., sp. nov., a new genus in the family Bradyrhizobiaceae isolated from Robinia pseudoacacia in Flanders (Belgium). Syst Appl Microbiol 35:205–214. Scholar
  48. De Meyer SE, De Beuf K, Vekeman B, Willems A (2015) A large diversity of non-rhizobial endophytes found in legume root nodules in Flanders (Belgium). Soil Biol Biochem 83:1–11. Scholar
  49. Deng ZS, Zhao LF, Xu L (2011) Paracoccus sphaerophysae sp. nov., a siderophore-producing, endophytic bacterium isolated from root nodules of Sphaerophysa salsula. Int J Syst Evol Microbiol 61:665–669. Scholar
  50. Dhole A, Shelat H, Vyas R, Jhala Y, Bhange M (2016) Endophytic occupation of legume root nodules by nifH-positive non-rhizobial bacteria, and their efficacy in the groundnut (Arachis hypogaea). Ann Microbiol 66:1397–1407. Scholar
  51. Dhole A, Shelat H, Panpatte D (2017) Chryseobacterium indologenes A Novel Root Nodule Endophyte in Vigna radiata. Int J Curr Microbiol App Sci 6:836–844.
  52. Dobbelaere S, Croonenborghs A, Thys A, Vande Broek A, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164. Scholar
  53. Downie JA (2014) Legume nodulation. Curr Biol 24:R184–R190. Scholar
  54. Dubey RK, Tripathi V, Edrisi et al (2017) Role of plant growth-promoting microorganisms in sustainable agriculture and environmental remediation. In: Singh HB, Sarma BK and Keswani C (eds) Advances in PGPR research. CABI international, Oxford, pp 75–126Google Scholar
  55. Egamberdieva D, Wirth SJ, Shurigin VV, Hashem A, Abd-Allah EF (2017) Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Front Microbiol 8:1887.
  56. Erisman JW, Galloway; JN, Dice; NB (2015) Nitrogen: too much of a vital resource. Science Brief. WWF Netherlands, Zeist, The NetherlandsGoogle Scholar
  57. Estrela S, Kerr B, Morris JJ (2016) Transitions in individuality through symbiosis. Curr Opin Microbiol 31:191–198. Scholar
  58. Fan MC, Nan LJ, Zhu YM, Chen WM, Wei GH, Lin YB (2017) Mitsuaria noduli sp. nov., isolated from the root nodules of Robinia pseudoacacia in a lead–zinc mine. Int J Syst Evol Microbiol 68:87–92. Scholar
  59. Fan MC, Guo YQ, Zhang LP, Zhu YM, Chen WM, Lin YB, Wei GH (2018) Herbaspirillum robiniae sp. nov., isolated from root nodules of Robinia pseudoacacia in a lead–zinc mine. Int J Syst Evol Microbiol 68:1300–1306. Scholar
  60. Fernández-González AJ, Martínez-Hidalgo P, Cobo-Díaz J et al (2017) The rhizosphere microbiome of burned holm-oak: potential role of the genus Arthrobacter in the recovery of burned soils. Sci Rep 7:6008. Scholar
  61. Flores-Félix JD, Carro L, Velázquez E, Valverde Á, Cerda-Castillo E, García-Fraile P, Rivas R (2013) Phyllobacterium endophyticum sp. nov., isolated from nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 63:821–826. Scholar
  62. Flores-Félix JD, Carro L, Ramírez-Bahena MH (2014) Cohnella lupini sp. nov., an endophytic bacterium isolated from root nodules of Lupinus albus. Int J Syst Evol Microbiol 64:83–87. Scholar
  63. Fred EB, Baldwin IL, McCoy E (1932) Root-nodule bacteria and leguminous plants. University of Wisconsin, Madison, WisconsinGoogle Scholar
  64. Gamalero E, Glick BR (2011) Mechanisms used by plant growth-promoting bacteria. In: Maheshwari DK (ed) Bacteria in agrobiology. Plant nutrient management, Springer, BerlinGoogle Scholar
  65. García-Fraile P, Velazquez E, Mateos| PF, Martínez-Molina E, Rivas R (2008) Cohnella phaseoli sp. nov., isolated from root nodules of Phaseolus coccineus in Spain, and emended description of the genus Cohnella. Int J Syst Evol Microbiol 58:1855–1859.
  66. García LC, Martínez-Molina E, Trujillo ME (2010) Micromonospora pisi sp. nov., isolated from root nodules of Pisum sativum. Int J Syst Evol Microbiol 60:331–337. Scholar
  67. Gerding M, Oyarzúa P, García L (2017) Diversity and symbiotic effectiveness of Adesmia spp. root nodule bacteria in central and southern Chile. Symbiosis 72:61–72. Scholar
  68. Germaine KJ, Liu X, Cabellos GG, Hogan JP, Ryan D, Dowling DN (2006) Bacterial endophyte-enhanced phytoremediation of the organochlorine herbicide 2, 4-dichlorophenoxyacetic acid. FEMS Microbiol Ecol 57:302–310. Scholar
  69. Ghosh PK, De TK, Maiti TK (2015) Ascorbic acid production in root, nodule and Enterobacter spp. (Gammaproteobacteria) isolated from root nodule of the legume Abrus precatorius L. Biocatal Agric Biotechnol 4:127–134. Scholar
  70. Glick BR (2012) Plant growth-promoting bacteria: mechanism and applications. Scientifica 2012:1–15. Scholar
  71. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39. Scholar
  72. Gresshoff PM, Ferguson BJ. (2017) Molecular signals in nodulation control. Int J Mol Sci 18:125.
  73. Hayashi T, Shimoda Y, Sato S, Tabata S, Imaizumi-Anraku H, Hayashi M (2014) Rhizobial infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of calcium spiking. Plant J 77:146–159. Scholar
  74. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598. Scholar
  75. Herrmann L, Lesueur D (2013) Challenges in formulation and quality of biofertilisers for successful inoculation. Appl Microbiol Biotechnol 97:8859–8873. Scholar
  76. Hoque MS, Broadhurst LM, Thrall PH (2011) Genetic characterization of root-nodule bacteria associated with Acacia salicina and A. stenophylla (Mimosaceae) across south-eastern Australia. Int J Syst Evol Microbiol 61:299–309. Scholar
  77. Ibáñez F, Angelini J, Taurian T, Tonelli ML, Fabra A (2009) Endophytic occupation of peanut root nodules by opportunistic Gammaproteobacteria. Syst Appl Microbiol 32:49–55. Scholar
  78. Ibáñez F, Arroyo ME, Angelini J et al (2014) Non-rhizobial peanut nodule bacteria promote maize (Zea mays L.) and peanut (Arachis hypogaea L.) growth in a simulated crop rotation system. Appl Soil Ecol 84:208–212. Scholar
  79. Imran A, Hafeez FY, Frühling A, Schumann P, Malik KA, Stackebrandt E (2010) Ochrobactrum ciceri sp. nov., isolated from nodules of Cicer arietinum. Int J Syst Evol Microbiol 60:1548–1553. Scholar
  80. Imran AFK, Naveed M, Afzal M (2017) Plant-bacteria synergism: an innovative approach for the remediation of crude oil-contaminated soils. Soil Environ 36:93–113.
  81. Kan FL, Chen ZY, Wang ET, Tian CF, Sui XH, Chen WX (2007) Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in Qinghai-Tibet plateau and in other zones of China. Arch Microbiol 188:103–115. Scholar
  82. Kaschuk G, Alberton O, Hungria M (2010) Three decades of soil microbial biomass studies in Brazilian ecosystems: lessons learned about soil quality and indications for improving sustainability. Soil Biol Biochem 42:1–13. Scholar
  83. Khandelwal SR, Manwar AV, Chaudhari BL, Chincholkar SB (2002) Siderophoregenic bradyrhizobia boost yield of soybean. Appl Biochem Biotechnol 102:155–168. Scholar
  84. Koli DK, Swarnalakshmi K (2017) Isolation and characterization of nodule associated bacteria from chickpea and their potential for plant growth promotion. Int J Curr Microbiol App Sci 6:1992–2004.
  85. Korir H, Mungai NW, Thuita M, Hamba Y, Masso C (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. Scholar
  86. Kong Z, Deng Z, Glick BR, Wei G, Chou M (2017) A nodule endophytic plant growth-promoting Pseudomonas and its effects on growth, nodulation and metal uptake in Medicago lupulina under copper stress. Ann Microbiol 67:49–58. Scholar
  87. Lace B, Ott T (2018) Commonalities and differences in controlling multipartite intracellular infections of legume roots by symbiotic microbes. Plant Cell Physiol 59:661–672. Scholar
  88. Lai WA, Hameed A, Lin SY (2015) Paenibacillus medicaginis sp. nov. a chitinolytic endophyte isolated from a root nodule of alfalfa (Medicago sativa L.). Int J Syst Evol Microbiol 65:3853–3860. Scholar
  89. Leigh GJ (2004) The world’s greatest fix: a history of nitrogen and agriculture. Oxford University Press, NewYorkGoogle Scholar
  90. Leite J, Fischer D, Rouws LFM et al (2017) Cowpea nodules harbor non-rhizobial bacterial communities that are shaped by soil type rather than plant genotype. Front Plant Sci 7:2064. Scholar
  91. Li JH, Wang ET, Chen WF, Chen WX (2008) Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heilongjiang province of China. Soil Biol Biochem 40:238–246. Scholar
  92. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556. Scholar
  93. Martínez-Hidalgo P, Galindo-Villardón P, Trujillo ME, Igual JM, Martínez-Molina E (2014) Micromonospora from nitrogen fixing nodules of alfalfa (Medicago sativa L.). A new promising Plant Probiotic Bacteria. Sci Rep 4:6389.
  94. Martínez-Hidalgo P, Hirsch AM (2017) The nodule microbiome: N2-fixing rhizobia do not live alone. Phytobiomes 1:70–82. Scholar
  95. Mavengere NR, Ellis AG, Le Roux JJ (2014) Burkholderia aspalathi sp. nov., isolated from root nodules of the South African legume Aspalathus abietina Thunb. Int J Syst Evol Microbiol 64:1906–1912. Scholar
  96. Menéndez E, Ramírez-Bahena MH, Carro L (2016) Paenibacillus periandrae sp. nov., isolated from nodules of Periandra mediterranea. Int J Syst Evol Microbiol 66:1838–1843. Scholar
  97. Mhamdi R, Mrabet M, Laguerre G, Tiwari R, Aouani ME (2005) Colonization of Phaseolus vulgaris nodules by Agrobacterium-like strains. Can J Microbiol 51:105–111. Scholar
  98. Mishra PK, Mishra S, Selvakumar G, Kundu S, Shankar-Gupta H (2009) Enhanced soybean (Glycine max L.) plant growth and nodulation by Bradyrhizobium japonicum-SB1 in presence of Bacillus thuringiensis-KR1. Acta Agric Scand BSP Sci 59:189–196. Scholar
  99. Mousavi SA, Willems A, Nesme X, De Lajudie P, Lindström K (2015) Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst Appl Microbiol 38:84–90. Scholar
  100. Mrabet M, Mnasri B, Laguerre G, Aouani ME, Mhamdi R (2006) Agrobacterium strains isolated from root nodules of common bean specifically reduce nodulation by Rhizobium gallicum. FEMS Microbiol Ecol 56:304–309. Scholar
  101. Murset V, Hennecke H, Pessi G (2012) Disparate role of rhizobial ACC deaminase in root-nodule symbioses. Symbiosis 57:43–50. Scholar
  102. Noreen R, Ali SA, Hasan KA, Sultana V, Ara J, Ehteshamul-Haque S (2015) Evaluation of biocontrol potential of fluorescent Pseudomonas associated with root nodules of mungbean. Crop Prot 75:18–24. Scholar
  103. Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546. Scholar
  104. Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T (2010) Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol Fertil Soils 46:807–816. Scholar
  105. Pandya M, Rajput M, Rajkumar S (2015) Exploring plant growth promoting potential of non rhizobial root nodules endophytes of Vigna radiata. Microbiology 84:80–89. Scholar
  106. Pawlik M, Cania B, Thijs S, Vangronsveld J, Piotrowska-Seget Z (2017) Hydrocarbon degradation potential and plant growth-promoting activity of culturable endophytic bacteria of Lotus corniculatus and Oenothera biennis from a long-term polluted site. Environ Sci Pollut Res 24:19640–19652. Scholar
  107. Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial associations with legumes. Crit Rev Plant Sci 34:17–42. Scholar
  108. Philipson MN, Blair ID (1957) Bacteria in clover root tissue. Can J Microbiol 3:125–129. Scholar
  109. Poole P, Ramachandran V, Terpolilli J (2018) Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol. Scholar
  110. Rajendran G, Patel MH, Joshi SJ (2012) Isolation and characterization of nodule-associated Exiguobacterium sp. from the root nodules of fenugreek (Trigonella foenum-graecum) and their possible role in plant growth promotion. Int J Microbiol 693982.
  111. Ramírez-Bahena MH, Tejedor C, Martín I, Velázquez E, Peix A (2013) Endobacter medicaginis gen. nov., sp. nov., isolated from alfalfa nodules in an acidic soil. Int J Syst Evol Microbiol 63:1760–1765.
  112. Rasolomampianina R, Bailly X, Fetiarison R (2005) Nitrogen-fixing nodules from rose wood legume trees (Dalbergia spp.) endemic to Madagascar host seven different genera belonging to α- and β-proteobacteria. Mol Ecol 14:4135–4146. Scholar
  113. Ray SS, Ali MN, Mukherjee S, Chatterjee G, Banerjee M (2017) Elimination and molecular identification of endophytic bacterial contaminants during in vitro propagation of Bambusa balcooa. World J Microbiol Biotechnol 33:31. Scholar
  114. Safronova VI, Kuznetsova IG, Sazanova AL (2015a) Bosea vaviloviae sp. nov., a new species of slow-growing rhizobia isolated from nodules of the relict species Vavilovia formosa (Stev.) Fed. Antonie Van Leeuwenhoek 107:911–920. Scholar
  115. Safronova VI, Kuznetsova IG, Sazanova AL (2015b) Extra-slow-growing Tardiphaga strains isolated from nodules of Vavilovia formosa (Stev.) Fed. Arch Microbiol 197:889–898. Scholar
  116. Safronova V, Belimov A, Sazanova A (2017) Does the Miocene-Pliocene relict legume Oxytropis triphylla form nitrogen-fixing nodules with a combination of bacterial strains? Int J Environ Stud 74:706–714. Scholar
  117. Safronova V, Belimov A, Sazanova A (2018a) Taxonomically different co-microsymbionts of a relict legume Oxytropis popoviana have complementary sets of symbiotic genes and together increase the efficiency of plant nodulation. Mol Plant Microbe Interact MPMI-01-18-0011-R.
  118. Safronova VI, Sazanova AL, Kuznetsova IG (2018b) Phyllobacterium zundukense sp. nov., a novel species of rhizobia isolated from root nodules of the legume species Oxytropis triphylla (Pall.) Pers. Int J Syst Evol Microbiol
  119. Säidï S, Mnasri B, Mhamdi R (2011) Diversity of nodule-endophytic agrobacteria-like strains associated with different grain legumes in Tunisia. Syst Appl Microbiol 34:524–530. Scholar
  120. Saini R, Dudeja SS, Giri R, Kumar V (2015) Isolation, characterization, and evaluation of bacterial root and nodule endophytes from chickpea cultivated in Northern India. J Basic Microbiol 55:74–81. Scholar
  121. Sánchez M, Ramírez-Bahena MH, Peix A, Lorite MJ, Sanjuán J, Velázquez E, Monza J (2014) Phyllobacterium loti sp. nov. isolated from nodules of Lotus corniculatus. Int J Syst Evol Microbiol 64:781–786. Scholar
  122. Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. Scholar
  123. Schoebitz M, López MD, Roldan A (2013) Bioencapsulation of microbial inoculants for better soil–plant fertilization. A review. Agron Sustain Dev 33:751–765. Scholar
  124. Schloter M, Nannipieri P, Sørensen SJ, van Elsas JD (2018) Microbial indicators for soil quality. Biol Fertil Soils 54:1–10. Scholar
  125. Schneijderberg M, Schmitz L, Cheng X, Polman S, Franken C, Geurts R, Bisseling T (2018) A genetically and functionally diverse group of non-diazotrophic Bradyrhizobium spp. colonizes the root endophytic compartment of Arabidopsis thaliana. BMC Plant Biol 18:61.
  126. Selvakumar G, Kundu S, Gupta AD, Shouche YS, Gupta HS (2008) Isolation and characterization of nonrhizobial plant growth promoting bacteria from nodules of Kudzu (Pueraria thunbergiana) and their effect on wheat seedling growth. Curr Microbiol 56:134–139. Scholar
  127. Shah S, Li J, Moffatt BA, Glick BR (1998) Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria. Can J Microbiol 44:833–843CrossRefGoogle Scholar
  128. Shamsheldin A, Abdelkhalek A, Sadowsky MJ (2017) Recent changes to the classification of symbiotic, nitrogen-fixing, legume-associating bacteria: a review. Symbiosis 71:91–109. Scholar
  129. Sheu SY, Chen MH, Liu WY (2015) Burkholderia dipogonis sp. nov., isolated from root nodules of Dipogon lignosus in New Zealand and Western Australia. Int J Syst Evol Microbiol 65:4716–4723. Scholar
  130. Somasegaran P, Hoben HJ (1994) Handbook for rhizobia: methods in legume-Rhizobium technology. Springer Science and Business MediaGoogle Scholar
  131. Souza RD, Ambrosini A, Passaglia LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419. Scholar
  132. Sturz AV, Christie BR, Matheson BG, Nowak J (1997) Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol Fertil Soils 25:13–19. Scholar
  133. Subramanian P, Kim K, Krishnamoorthy R, Sundaram S, Sa T (2015) Endophytic bacteria improve nodule function and plant nitrogen in soybean on co-inoculation with Bradyrhizobium japonicum MN110. Plant Growth Regul 76:327–332. Scholar
  134. Szilagyi-Zecchin VJ, Ikeda AC, Hungria M, Adamoski D, Kava-Cordeiro V, Glienke C, Galli-Terasawa LV (2014) Identification and characterization of endophytic bacteria from corn (Zea mays L.) roots with biotechnological potential in agriculture. AMB Express 4:2–9. Scholar
  135. Tariq M, Hameed S, Yasmeen T, Ali A (2012) Non-rhizobial bacteria for improved nodulation and grain yield of mung bean [Vigna radiata (L.) Wilczek]. Afr J Biotechnol 11:15012.
  136. Tariq M, Hameed S, Yasmeen T, Zahid M, Zafar M (2014) Molecular characterization and identification of plant growth promoting endophytic bacteria isolated from the root nodules of pea (Pisum sativum L.). World J Microbiol Biotechnol 30:719–725. Scholar
  137. Tétard-Jones C, Edwards R (2016) Potential roles for microbial endophytes in herbicide tolerance in plants. Pest Manag Sci 72:203–209. Scholar
  138. Tokala RK, Strap JL, Jung CM et al (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171. Scholar
  139. Tokgöz S (2018) Exploration of soybean nodule microbiome for plant health management. University of NebraskaGoogle Scholar
  140. Trabelsi D, Chihaoui SA, Mhamdi R (2017) Nodules and roots of Vicia faba are inhabited by quite different populations of associated bacteria. Appl Soil Ecol 119:72–79. Scholar
  141. Trujillo ME, Kroppenstedt RM, Fernandez-Molinero C, Schumann P, Martinez-Molina E (2007) Micromonospora lupini sp. nov. and Micromonospora saelicesensis sp. nov., isolated from root nodules of Lupinus angustifolius. Int J Syst Evol Microbiol 57:2799–2804. Scholar
  142. Valverde A, Velazquez E, Gutierrez C, Cervantes E, Ventosa A, Igual JM (2003) Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 53:1979–1983. Scholar
  143. Valverde A, Fterich A, Mahdhi M (2010) Paenibacillus prosopidis sp. nov., isolated from the nodules of Prosopis farcta. Int J Syst Evol Microbiol 60:2182–2186.
  144. Velázquez E, Martínez-Hidalgo P, Carro L, Alonso P, Peix A, Trujillo ME, Martínez-Molina E (2013) Nodular endophytes: an untapped diversity. In: Gonzalez R, Gonzalez-Lopez J (eds). Beneficial plant–microbial interactions: ecology and applications. Taylor and Francis Group, pp 215–235Google Scholar
  145. Velázquez E, Carro L, Flores-Félix JD (2017) The legume nodule microbiome: a source of plant growth-promoting bacteria. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics and Plant Health. Springer, SingaporeGoogle Scholar
  146. Vincent JM (1970) A manual for the practical study of the root-nodule bacteria. Blackwell Scientific Publications, OxfordGoogle Scholar
  147. Wang ET, Tan ZY, Willems A, Fernández-López M, Reinhold-Hurek B, Martínez-Romero E (2002) Sinorhizobium morelense sp. nov., a Leucaena leucocephala-associated bacterium that is highly resistant to multiple antibiotics. Int J Syst Evol Microbiol 52:1687–1693.
  148. 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. Scholar
  149. Wekesa C, Muoma J, Ombori O et al (2017) Genetic characterization of rhizosphere bacteria that inhabit common bean nodules in Western Kenya soils. Appl Microbiol 3:1.
  150. Wei XL, Han MS, Xia CC (2015) Diaphorobacter ruginosibacter sp. nov., isolated from soybean root nodule, and emended description of the genus Diaphorobacter. Arch Microbiol 197:683–692. Scholar
  151. Wigley K, Liu WYY, Khumalo Q, Moot DJ, Brown DS, Ridgway HJ (2015) Effectiveness of three inoculation methods for lucerne (Medicago sativa L.) in two Canterbury soils. N Z J Agric Res 1:10.
  152. Wigley K, Moot D, Wakelin SA, Laugraud A, Blond C, Seth K, Ridgway H (2017) Diverse bacterial taxa inhabit root nodules of lucerne (Medicago sativa L.) in New Zealand pastoral soils. Plant Soil 420:253–262. Scholar
  153. Xu L, Zhang Y, Wang L, Chen W, Wei G (2014) Diversity of endophytic bacteria associated with nodules of two indigenous legumes at different altitudes of the Qilian Mountains in China. Syst Appl Microbiol 37:457–465. Scholar
  154. Xu L, Zhang Y, Li C, Wang X, Liu J, Friman VP (2018) Nocardioides astragali sp. nov., isolated from a nodule of wild Astragalus chrysopterus in northwestern China. Antonie van Leeuwenhoek 1–7.
  155. Yan J, Li Y, Han XZ, Chen WF, Zou WX, Xie Z, Li M (2017a) Agrobacterium deltaense sp. nov., an endophytic bacteria isolated from nodule of Sesbania cannabina. Arch Microbiol 199:1003–1009. Scholar
  156. Yan J, Yan H, Liu LX et al (2017b) Rhizobium hidalgonense sp. nov., a nodule endophytic bacterium of Phaseolus vulgaris in acid soil. Arch Microbiol 199:97–104. Scholar
  157. Yin J, He D, Li X, Zeng X, Tian M, Cheng G (2015) Paenibacillus enshidis sp. nov., isolated from the nodules of Robinia pseudoacacia L. Curr Microbiol 71:321–325. Scholar
  158. Zakhia F, Jeder H, Willems A, Gillis M, Dreyfus B, De Lajudie P (2006) Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH-like gene within the genera Microbacterium and Starkeya. Microb Ecol 51:375–393. Scholar
  159. Zgadzaj R, Garrido-Oter R, Jensen DB, Koprivova A, Schulze-Lefert P, Radutoiu S (2016) Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities. Proc Natl Acad Sci USA 113:E7996–E8005. Scholar
  160. Zhao L, Xu Y, Sun R, Deng Z, Yang W, Wei G (2011) Identification and characterization of the endophytic plant growth prompter Bacillus cereus strain MQ23 isolated from Sophora alopecuroides root nodules. Braz J Microbiol 42:567–575. Scholar
  161. Zhao L, Xu Y, Lai X (2017) Antagonistic endophytic bacteria associated with nodules of soybean (Glycine max L.) and plant growth-promoting properties. Braz J Microbiol 49:269–278. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Winston Franz Ríos-Ruiz
    • 1
  • Renzo Alfredo Valdez-Nuñez
    • 1
  • Eulogio J. Bedmar
    • 2
  • Antonio Castellano-Hinojosa
    • 2
    • 3
    Email author
  1. 1.Universidad Nacional de San Martín–TarapotoTarapotoPerú
  2. 2.Department of Soil Microbiology and Symbiotic SystemsEstación Experimental del Zaidín, CSICGranadaSpain
  3. 3.Pharmacy Faculty, Department of MicrobiologyUniversity of GranadaGranadaSpain

Personalised recommendations