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Bacteria-Inducing Legume Nodules Involved in the Improvement of Plant Growth, Health and Nutrition

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Abstract

Bacteria-inducing legume nodules are known as rhizobia and belong to the class Alphaproteobacteria and Betaproteobacteria. They promote the growth and nutrition of their respective legume hosts through atmospheric nitrogen fixation which takes place in the nodules induced in their roots or stems. In addition, rhizobia have other plant growth-promoting mechanisms, mainly solubilization of phosphate and production of indoleacetic acid, ACC deaminase and siderophores. Some of these mechanisms have been reported for strains of rhizobia which are also able to promote the growth of several nonlegumes, such as cereals, oilseeds and vegetables. Less studied are the mechanisms that have the rhizobia to promote the plant health; however, these bacteria are able to exert biocontrol of some phytopathogens and to induce the plant resistance. In this chapter, we revised the available data about the ability of the legume nodule-inducing bacteria for improving the plant growth, health and nutrition of both legumes and nonlegumes. These data showed that rhizobia meet all the requirements of sustainable agriculture to be used as bio-inoculants allowing the total or partial replacement of chemicals used for fertilization or protection of crops.

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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 Agri Biol 1:7–12

    Google Scholar 

  • Abd-Alla MH (1998) Growth and siderophore production in vitro of Bradyrhizobium (Lupin) strains under iron limitation. Eur J Soil Biol 34:99–104

    Article  CAS  Google Scholar 

  • Abd-Alla MH, El-Enany AWE, Nafady NA, Khalaf DM, Morsy FM (2014) Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol Res 169:49–58

    Article  CAS  PubMed  Google Scholar 

  • Abhilash PC, Dubey RK, Tripathi V, Gupta VK, Singh HB (2016) Plant growth-promoting microorganisms for environmental sustainability. Trends Biotechnol 34:847–850

    Article  CAS  PubMed  Google Scholar 

  • Abril A, Zurdo-Piñeiro JL, Peix A, Rivas R, Velázquez E (2007) Solubilization of phosphate by a strain of Rhizobium leguminosarum bv. Trifolii isolated from Phaseolus vulgaris in El Chaco Arido soil (Argentina). In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Developments in plant and soil sciences, vol 102. Springer, Dordrecht, pp 135–138

    Chapter  Google Scholar 

  • Ahmad M, Zahir ZA, Asghar HN, Asghar M (2011a) Inducing salt tolerance in mung bean through coinoculation with rhizobia and plant-growth-promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 57:578–589

    Article  CAS  PubMed  Google Scholar 

  • Ahmad M, Zahir ZA, Asghar HN, Asghar M (2011b) The combined application of rhizobial strains and plant growth promoting rhizobacteria improves growth and productivity of mung bean (Vigna radiata L.) under salt-stressed conditions. Ann Microbiol 62:1321–1330

    Article  CAS  Google Scholar 

  • Ahmad M, Zahir ZA, Khalid M, Nazli F, Arshad M (2013) Efficacy of Rhizobium and Pseudomonas strains to improve physiology, ionic balance and quality of mung bean under salt-affected conditions on farmer’s fields. Plant Physiol Biochem 63:170–176

    Article  CAS  PubMed  Google Scholar 

  • Ahnia H, Bourebaba Y, Durán D, Boulila F, Palacios JM, Rey L, Ruiz-Argüeso T, Boulila A, Imperial J (2018) Bradyrhizobium algeriense sp. nov., a novel species isolated from effective nodules of Retama sphaerocarpa from Northeastern Algeria. Syst Appl Microbiol 41:333–339

    Article  PubMed  Google Scholar 

  • Akhtar MS, Siddiqui ZA (2008) Biocontrol of a root-rot disease complex of chickpea by Glomus intraradices, Rhizobium sp. and Pseudomonas striata. Crop Prot 27:410–417

    Article  Google Scholar 

  • Akhtar MS, Shakeel U, Siddiqui ZA (2010) Biocontrol of Fusarium wilt by Bacillus pumilus, Pseudomonas, Alcaligenes and Rhizobium sp. on lentil. Turk J Biol 34:1–7

    Google Scholar 

  • Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers 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-Ani RA, Adhab MA, Mahdi MH, Abood HM (2012) Rhizobium japonicum as a biocontrol agent of soybean root rot disease caused by Fusarium solani and Macrophomina phaseolina. Plant Protect Sci 48:149–155

    Article  Google Scholar 

  • Ali Q, Zahir ZA, Asghar HN, Jamil A (2017) Inoculation with rhizobial consortium for improving the growth, yield and quality of maize under salt-stressed conditions. Pak J Agric Sci 54:97–105

    Google Scholar 

  • Alikhani HA, Saleh-Rastin N, Antoun H (2007) Phosphate solubilization activity of rhizobia native to Iranian soils. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Developments in plant and soil sciences, vol 102. Springer, Dordrecht, pp 35–41

    Chapter  Google Scholar 

  • Angus AA, Lee A, Lum MR, Shehayeb M, Hessabi R, Fujishige NA, Yerrapragada S, Kano S, Song N, Yang P, Estrada de los Santos P, de Faria SM, Dakora FD, Weinstock G, Hirsch AM (2013) Nodulation and effective nitrogen fixation of Macroptilium atropurpureum (siratro) by Burkholderia tuberum, a nodulating and plant growth promoting beta-proteobacterium, are influenced by environmental factors. Plant Soil 369:543–562

    Article  CAS  Google Scholar 

  • Ansari PG, Rao DLN (2014) Soybean rhizobia in Indian soils: populations, host specificity and competitiveness. Proc Natl Acad Sci, India Section B: Biol Sci 84:457–464

    Article  Google Scholar 

  • Antoun H, Bordeleau LM, Gagnon C (1978) Antagonisme entre Rhizobium meliloti at Fusarium oxysporum en relation avec lefficacite symbiotique. Can J Plant Sci 58:75–78

    Article  Google Scholar 

  • Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57–67

    Article  CAS  Google Scholar 

  • Araújo J, Díaz-Alcántara CA, Velázquez E, Urbano B, González-Andrés F (2015) Bradyrhizobium yuanmingense related strains form nitrogen-fixing symbiosis with Cajanus cajan L. in Dominican Republic and are efficient biofertilizers to replace N fertilization. Sci Hortic 192:421–428

    Article  Google Scholar 

  • Araújo J, Flores-Félix JD, Igual JM, Peix A, González-Andrés F, Díaz-Alcántara CA, Velázquez E (2017) Bradyrhizobium cajani sp. nov. isolated from nodules of Cajanus cajan. Int J Syst Evol Microbiol 67:2236–2241

    Article  PubMed  CAS  Google Scholar 

  • Ardley JK, Parker MA, De Meyer SE, Trengove RD, O’Hara GW, Reeve WG, Yates RJ, Dilworth MJ, Willems A, Howieson JG (2012) Microvirga lupini sp. nov., Microvirga lotononidis sp. nov. and Microvirga zambiensis sp. nov. are alphaproteobacterial root-nodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int J Syst Evol Microbiol 62:2579–2588

    Article  CAS  PubMed  Google Scholar 

  • Arfaoui A, Sifi B, Boudabous A, Hadrami IE, Chérif M (2006) Identification of Rhizobium isolates possessing antagonistic activity against Fusarium oxysporum f. sp. ciceris, the causal agent of Fusarium wilt of chickpea. J Plant Pathol 88:67–75

    CAS  Google Scholar 

  • Arfaoui A, El Hadrami A, Mabrouk Y, Sifi B, Boudabous A, El Hadrami I, Daayf F, Chérif M (2007) Treatment of chickpea with Rhizobium isolates enhances the expression of phenylpropanoid defense-related genes in response to infection by Fusarium oxysporum f. sp. ciceris. Plant Physiol Biochem 45:470–479

    Article  CAS  PubMed  Google Scholar 

  • Arora NK, Kang SC, Maheshwari DK (2001) Isolation of siderophore-producing strains of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr Sci 81:673–677

    Google Scholar 

  • Aserse AA, Woyke T, Kyrpides NC, Whitman WB, Lindström K (2017) Draft genome sequences of Bradyrhizobium shewense sp. nov. ERR11T and Bradyrhizobium yuanmingense CCBAU 10071T. Stand Genomic Sci 12:74

    Article  PubMed  PubMed Central  Google Scholar 

  • Babudieri B (1950) Natura delle cosidette “S-formen” delle leptospire. Loro identificazione con Hyphomicrobium vulgare Stutzer e Hartleb. Studio di quest. Ultimo germe. R.C. 1st Supplement Sanita Roma 13:580–591

    Google Scholar 

  • Bai B, Suri VK, Kumar A, Choudhary AK (2017) Tripartite symbiosis of Pisum–Glomus–Rhizobium leads to enhanced productivity, nitrogen and phosphorus economy, quality, and biofortification in garden pea in a Himalayan acid alfisol. J Plant Nutr 40:600–613

    Article  CAS  Google Scholar 

  • Balasundaran V, Sarbhoy A (1988) Inhibition of plant pathogenic fungi by Rhizobium japonicum. Indian Phytopathol 41:128–130

    Google Scholar 

  • Bardin SD, Huang H-C, Pinto J, Amundsen EJ, Erickson RS (2004) Biological control of Pythium damping-off of pea and sugar beet by Rhizobium leguminosarum bv. Viceae. Can J Bot 82:291–296

    Article  Google Scholar 

  • Barros LRN, Barbosa de Oliveira L, Barros Magalhães W, Oliveira Médici L, Pimentel C (2018) Interaction of biological nitrogen fixation with sowing nitrogen fertilization on common bean in the two seasons of cultivation in Brazil. J Plant Nutr 41:774–781

    Article  CAS  Google Scholar 

  • Beijerinck MW (1888) Cultur des Bacillus radicicola aus den Knöllchen. Bot Ztg 46:740–750

    Google Scholar 

  • Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  CAS  PubMed  Google Scholar 

  • Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18

    Article  CAS  PubMed  Google Scholar 

  • Berg G, Köberl M, Rybakova D, Müller H, Grosch R, Smalla K (2017) Plant microbial diversity is suggested as the key to future biocontrol and health trends. FEMS Microbiol Ecol 93. https://doi.org/10.1093/femsec/fix050

  • Berraho EL, Lesueur D, Diem HG, Sasson A (1997) Iron requirement and siderophore production in Rhizobium ciceri during growth on an iron-deficient medium. World J Microbiol Biotechnol 13:501–510

    Article  CAS  Google Scholar 

  • Bertrand A, Dhont C, Bipfubus M, Chalifour FP, Drouin P, Beauchamp CJ (2015) Improving salt stress responses of the symbiosis in alfalfa using salt-tolerant cultivar and rhizobial strain. Appl Soil Ecol 87:108–117

    Article  Google Scholar 

  • Bhattacharjee S, Sharma GD (2012) Effect of dual inoculation of arbuscular mycorrhiza and rhizobium on the chlorophyll, nitrogen and phosphorus contents of pigeon pea (Cajanus cajan L.). Adv Microbiol 2:561–564

    Article  CAS  Google Scholar 

  • Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107

    Article  CAS  PubMed  Google Scholar 

  • Boiero L, Perrig D, Masciarelli O, Penna C, Cassán 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 

  • Bournaud C, Moulin L, Cnockaert M, Faria S, Prin Y, Severac D, Vandamme P (2017) Paraburkholderia piptadeniae sp. nov. and Paraburkholderia ribeironis sp. nov., two root-nodulating symbiotic species of Piptadenia gonoacantha in Brazil. Int J Syst Evol Microbiol 67:432–440

    Article  CAS  PubMed  Google Scholar 

  • Brígido C, Glick BR, Oliveira S (2017) Survey of plant growth-promoting mechanisms in native Portuguese chickpea Mesorhizobium isolates. Microb Ecol May 73:900–915

    Article  Google Scholar 

  • Bünger W, Grönemeyer JL, Sarkar A, Reinhold-Hurek B (2018) Bradyrhizobium ripae sp. nov., a nitrogen-fixing symbiont isolated from nodules of wild legumes in Namibia. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.002955

    Article  PubMed  Google Scholar 

  • Carson KC, Dilworth MJ, Glenn AR (1992) Siderophore production and iron transport in Rhizobium leguminosarum bv. viciae MNF710. J Plant Nutr 15:2203–2220

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Catroux G, Hartmann A, Revellin C (2001) Trends in rhizobial inoculant production and use. Plant Soil 230:21–30

    Article  CAS  Google Scholar 

  • Cerezini P, Harumi Kuwano B, Barbosa dos Santos M, Terassi F, Hungria M, Nogueira MA (2016) Strategies to promote early nodulation in soybean under drought. Field Crops Res 196:160–167

    Article  Google Scholar 

  • Chabot R, Antoun H, Cescas MP (1996) Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar. phaseoli. Plant Soil 184:311–321

    Article  CAS  Google Scholar 

  • Chakraborty U, Chakraborty BN (1989) Interaction of Rhizobium leguminosarum and Fusarium solani f. sp. pisi on pea affecting disease development and phytoalexin production. Can J Bot 67:1698–1701

    Article  CAS  Google Scholar 

  • Chakraborty U, Purkayastha RP (1984) Role of rhizobitoxine in protecting soybean roots from Macrophomina phaseolina infection. Can J Microbiol 30:285–289

    Article  CAS  PubMed  Google Scholar 

  • Challougui I, Chibou FM, Saadani O, Jebara M, Jebara SH (2015) Impact of dual inoculation with Rhizobium and PGPR on growth and antioxidant status of Vicia faba L. under copper stress. Compt Rend Biol 338:241–254

    Article  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 38:124–130

    Article  Google Scholar 

  • Checcucci A, DiCenzo GC, Bazzicalupo M, Mengoni A (2017) Trade, diplomacy, and warfare: the quest for elite rhizobia inoculant strains. Front Microbiol 8:2207

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen WM, James EK, Prescott AR, Kierans M, Sprent JI (2003) Nodulation of Mimosa spp. by the beta-proteobacterium Ralstonia taiwanensis. Mol Plant-Microbe Interact 16:1051–1061

    Article  CAS  PubMed  Google Scholar 

  • Chen WH, Yang SH, Li ZH, Zhang XX, Sui XH, Wang ET, Chen WX, Chen WF (2017) Ensifer shofinae sp. nov., a novel rhizobial species isolated from root nodules of soybean (Glycine max). Syst Appl Microbiol 40:144–149

    Article  PubMed  Google Scholar 

  • Conn HJ (1938) Taxonomic relationships of certain non-sporeforming rods in soil. J Bacteriol 36:320–321

    Google Scholar 

  • Cordeiro AB, Ribeiro RA, Helene LCF, Hungria M (2017) Rhizobium esperanzae sp. nov., a N2-fixing root symbiont of Phaseolus vulgaris from Mexican soils. Int J Syst Evol Microbiol 67:3937–3945

    Article  CAS  PubMed  Google Scholar 

  • Crespo Flores G, Ramírez JF, González PJ, Hernández I (2014) Co-inoculation of Rhizobium strains and one of the arbuscular mycorrhizal fungus on Stylosanthes guianensis cv. CIAT-184. Cuban J Agric Sci 48:297–300

    Google Scholar 

  • da Conceição Jesus E, de Almeida Leite R, do Amaral Bastos R, da Silva Aragão OO, Araújo AD (2018) Co-inoculation of Bradyrhizobium stimulates the symbiosis efficiency of Rhizobium with common bean. Plant Soil 425:201–215

    Article  CAS  Google Scholar 

  • da Piedade Melo A, Lopes Olivares F, Oliveira Médici L, Torres-Neto A, Barros Dobbss L, Pasqualoto Canellas L (2017) Mixed rhizobia and Herbaspirillum seropedicae inoculations with humic acid-like substances improve water-stress recovery in common beans. Chem Biol Techn Agric 4:6

    Article  CAS  Google Scholar 

  • Dahale SK, Prashanthi SK, Krishnaraj PU (2016) Rhizobium mutant deficient in mineral phosphate solubilization activity shows reduced nodulation and plant growth in green gram. Proc Natl Acad Sci, India Section B: Biol Sci 86:723–734

    Article  CAS  Google Scholar 

  • Dar GH, Zargar MY, Beigh GM (1997) Biocontrol of Fusarium root rot in the common bean (Phaseolus vulgaris L.) by using symbiotic Glomus mosseae and Rhizobium leguminosarum. Microb Ecol 34:74–80

    Article  Google Scholar 

  • Das K, Prasanna R, Saxena AK (2017) Rhizobia: a potential biocontrol agent for soilborne fungal pathogens. Folia Microbiol 62:425–435

    Article  CAS  Google Scholar 

  • Datta C, Basu PS (2000) Indole acetic acid production by a Rhizobium species from root nodules of a leguminous shrub, Cajanus cajan. Microbiol Res 155:123–127

    Article  CAS  PubMed  Google Scholar 

  • Datta B, Chakrabartty PK (2014) Siderophore biosynthesis genes of Rhizobium sp. isolated from Cicer arietinum L. 3 Biotech 4:391–401

    Article  PubMed  Google Scholar 

  • de Lajudie P, Laurent-Fulele WA, Torck U, Coopman R, Collins MD, Kersters K, Dreyfus B, Gillis M (1998) Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int J Syst Bacteriol 48:1277–1290

    Article  PubMed  Google Scholar 

  • de Matos GF, Zilli JE, de Araújo JLS, Parma MM, Melo IS, Radl V, Baldani JI, Rouws LFM (2017) Bradyrhizobium sacchari sp. nov., a legume nodulating bacterium isolated from sugarcane roots. Arch Microbiol 199:1251–1258

    Article  PubMed  CAS  Google Scholar 

  • de Oliveira Longatti SM, Marra LM, de Souza Moreira FM (2013) Evaluation of plant growth-promoting traits of Burkholderia and Rhizobium strains isolated from Amazon soils for their co-inoculation in common bean. Afr J Microbiol Res 7:948–959

    Article  CAS  Google Scholar 

  • Thakur D, Kaushal R, Shyam V (2014) Phosphate solubilising microorganisms: role in phosphorus nutrition of crop plants-a review. Agric Rev 35:159–171

    Article  Google Scholar 

  • Defez R, Andreozzi A, Dickinson M, Charlton A, Tadini L, Pesaresi P, Bianco C (2017) Improved drought stress response in alfalfa plants nodulated by an IAA over-producing Rhizobium strain. Front Microbiol 8:2466

    Article  PubMed  PubMed Central  Google Scholar 

  • Demissie N, Degefu T, Ergena A, Ojiewo C (2018) Phenotypic characteristics of rhizobial and non-rhizobial isolates recovered from root nodules of chickpea (Cicer arietinum L.) grown in Ethiopia. Afr J Microbiol Res 12:73–85

    Article  CAS  Google Scholar 

  • Deshwal VK, Dubey RC, Maheshwari DK (2003a) Isolation of plant growth-promoting strains of Bradyrhizobium (Arachis) sp. with biocontrol potential against Macrophomina phaseolina causing charcoal rot of peanut. Curr Sci 84:443–448

    Google Scholar 

  • Deshwal V, Pandey P, Kang S, Maheshwari D (2003b) Rhizobia as a biological control agent against soil borne plant pathogenic fungi. Indian J Exp Biol 41:1160–1164

    CAS  PubMed  Google Scholar 

  • Diez-Mendez A, Menéndez E, García-Fraile P, Celador-Lera L, Rivas R, Mateos PF (2015) Rhizobium cellulosilyticum as a co-inoculant enhances Phaseolus vulgaris grain yield under greenhouse conditions. Symbiosis 67:135–141

    Article  CAS  Google Scholar 

  • Dobritsa AP, Samadpour M (2016) Transfer of eleven species of the genus Burkholderia to the genus Paraburkholderia and proposal of Caballeronia gen. nov. to accommodate twelve species of the genera Burkholderia and Paraburkholderia. Int J Syst Evol Microbiol 66:2836–2846

    Article  CAS  PubMed  Google Scholar 

  • Dreyfus B, Garcia JL, Gillis M (1988) Characterization of Azorhizobium caulinodans gen. nov., sp. nov., a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata. Int J Syst Bacteriol 38:89–98

    Article  CAS  Google Scholar 

  • Duan J, Müller KM, Charles TC, Vesely S, Glick BR (2009) 1-aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from southern Saskatchewan. Microb Ecol 57:423–436

    Article  CAS  PubMed  Google Scholar 

  • Dubey RC, Maheshwari DK, Kumar H, Choure K (2010) Assessment of diversity and plant growth promoting attributes of rhizobia isolated from Cajanus cajan L. African J Biotechnol 9:8619–8629

    CAS  Google Scholar 

  • Dutta S, Mishra AK, Kumar BSD (2008) Induction of systemic resistance against fusarial wilt in pigeon pea through interaction of plant growth promoting rhizobacteria and rhizobia. Soil Biol Biochem 40:452–461

    Article  CAS  Google Scholar 

  • Eberl L, Vandamme P (2016) Members of the genus Burkholderia: good and bad guys. F1000 Res 5:1007

    Article  Google Scholar 

  • Egamberdieva D, Berg G, Lindström K, Räsänen LA (2010) Co-inoculation of Pseudomonas spp. with Rhizobium improves growth and symbiotic performance of fodder galega (Galega orientalis Lam.). Eur J Soil Biol 46:269–272

    Article  CAS  Google Scholar 

  • Egamberdieva D, Jabborova D, Berg G (2016a) Synergistic interactions between Bradyrhizobium japonicum and the endophyte Stenotrophomonas rhizophila and their effects on growth, and nodulation of soybean under salt stress. Plant Soil 405:35–45

    Article  CAS  Google Scholar 

  • Egamberdieva D, Li L, Lindström K, Räsänen LA (2016b) A synergistic interaction between salt-tolerant Pseudomonas and Mesorhizobium strains improves growth and symbiotic performance of liquorice (Glycyrrhiza uralensis Fish.) under salt stress. Appl Microbiol Biotechnol 100:2829–2841

    Article  CAS  PubMed  Google Scholar 

  • Egamberdieva D, Reckling M, Wirtha S (2017) Biochar-based Bradyrhizobium inoculum improves growth of lupin (Lupinus angustifolius L.) under drought stress. Eur J Soil Biol 78:38–42

    Article  CAS  Google Scholar 

  • Ekimova GA, Fedorov DN, Tani A, Doronina NV, Trotsenko YA (2018) Distribution of 1-aminocyclopropane-1-carboxylate deaminase and D-cysteine desulfhydrase genes among type species of the genus Methylobacterium. Antonie Van Leeuwenhoek. https://doi.org/10.1007/s10482-018-1061-5

    Article  CAS  PubMed  Google Scholar 

  • El-Akhal MR, Rincón A, Coba de la Peña T, Lucas MM, El Mourabit N, Barrijal S, Pueyo JJ (2013) Effects of salt stress and rhizobial inoculation on growth and nitrogen fixation of three peanut cultivars. Plant Biol (Stuttg) 15:415–421

    Article  CAS  Google Scholar 

  • Elbadry M, Taha RM, Eldougdoug KA, Gamal-Eldin H (2006) Induction of systemic resistance in faba bean (Vicia faba L.) to bean yellow mosaic potyvirus (BYMV) via seed bacterization with plant growth promoting rhizobacteria. J Plant Dis Protect 113:247–251

    Article  Google Scholar 

  • Estevez de Jensen C, Percich JA, Graham PH (2002) Integrated management strategies of bean root rot with Bacillus subtilis and Rhizobium in Minnesota. Field Crops Res 74:107–115

    Article  Google Scholar 

  • Faghire M, Mandri B, Oufdou K, Bargaz A, Ghoulam C, Ramírez-Bahena MH, Velázquez E, Peix A (2012) Identification at the species and symbiovar levels of strains nodulating Phaseolus vulgaris in saline soils of the Marrakech region (Morocco) and analysis of the otsA gene putatively involved in osmotolerance. Syst Appl Microbiol 35:156–164

    Article  CAS  PubMed  Google Scholar 

  • Fatnassi IC, Chiboub M, Saadani O, Jebara M, Jebara SH (2015) Phytostabilization of moderate copper contaminated soils using co-inoculation of Vicia faba with plant growth promoting bacteria. J Basic Microbiol 55:303–311

    Article  CAS  PubMed  Google Scholar 

  • Flores-Félix JD, Menéndez E, Rivera LP, Marcos-García M, Martínez-Hidalgo P, Mateos PF, Martínez-Molina E, Velázquez E, García-Fraile P, Rivas R (2013) 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 

  • Flores-Félix JD, Marcos-García M, Silva LR, Menéndez E, Martínez-Molina E, Mateos PF, Velázquez E, García-Fraile P, Andrade P, Rivas R (2015) Rhizobium as plant probiotic for strawberry production under microcosm conditions. Symbiosis 67:25–32

    Article  CAS  Google Scholar 

  • Flores-Félix JD, Velázquez E, García-Fraile P, González-Andrés F, Silva LR, Rivas R (2018) Rhizobium and Phyllobacterium bacterial inoculants increase bioactive compounds and quality of strawberries cultivated in field conditions. Food Res Int 111:416–422

    Article  PubMed  CAS  Google Scholar 

  • Frank B (1889) Ueber die Pilzsymbiose der Leguminosen. Bet Dtsch Bot Ges 7:332–346

    Google Scholar 

  • Fukami J, de la Osa C, Ollero FJ, Megías M, Hungria M (2017) Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress. Funct Plant Biol 45:328–339

    Article  CAS  Google Scholar 

  • Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750

    Article  PubMed  Google Scholar 

  • Ganesan S, Kuppusamy RG, Sekar R (2007) Integrated management of stem rot disease (Sclerotium rolfsii) of groundnut (Arachis hypogaea L.) using Rhizobium and Trichoderma harzianum (ITCC-4572). Turk J Agric For 31:103–108

    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:e33977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao P, Guo Y, Li Y, Duan T (2018a) Effects of dual inoculation of AMF and rhizobium on alfalfa (Medicago sativa) root rot caused by Microdochium tabacinum. Australas Plant Pathol 47:195–203

    Article  CAS  Google Scholar 

  • Gao P, Li Y, Guo Y, Duan T (2018b) Co-inoculation of lucerne (Medicago sativa) with an AM fungus and a Rhizobium reduces occurrence of spring black stem and leaf spot caused by Phoma medicaginis. Crop Pasture Sci 69:933–943

    Article  Google Scholar 

  • García-Fraile P, Carro L, Robledo M, Ramírez-Bahena MH, Flores-Félix JD, Fernández MT, Mateos PF, Rivas R, Igual JM, Martínez-Molina E, Peix A, Velázquez E (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:e38122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garrity GM, Bell JA, Lilburn T (2005) Family VII. Bradyrhizobiaceae fam. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, second edition, vol. 2 (the Proteobacteria), part C (the Alpha-, Beta-, Delta-, and Epsilonproteobacteria). Springer, New York, pp 438–443

    Google Scholar 

  • Ge JC, Yoon SK, Choi NJ (2017) Using canola oil biodiesel as an alternative fuel in diesel engines: a review. Appl Sci 7:881

    Article  CAS  Google Scholar 

  • Ghosh PK, De TK, Maiti TK (2015) Production and metabolism of indole acetic acid in root nodules and symbiont (Rhizobium undicola) isolated from root nodule of aquatic medicinal legume Neptunia oleracea Lour. J Bot 2015. ID 575067

    Google Scholar 

  • Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Laxmipathi Gowda CL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech 5:355–377

    Article  PubMed  Google Scholar 

  • Granada CE, Arruda L, Brito Lisboa B, Passaglia LMP, Vargas LK (2014) Diversity of native rhizobia isolated in South Brazil and their growth promotion effect on white clover (Trifolium repens) and rice (Oryza sativa) plants. Biol Fertility Soils 50:123–132

    Article  CAS  Google Scholar 

  • Gross DC, Vidaver AK (1978) Bacteriocin-like substances produced by Rhizobium japonicum and other slow-growing rhizobia. Appl Environ Microbiol 36:936–943

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gutiérrez-Zamora ML, Martínez-Romero E (2001) Natural endophytic association between Rhizobium etli and maize (Zea mays L.). J Biotechnol 91:117–126

    Article  PubMed  Google Scholar 

  • Hafeez FY, Naeem FI, Naeem R, Zaidi AH, Malik KA (2005) Symbiotic effectiveness and bacteriocin production by Rhizobium leguminosarum bv. viciae isolated from agriculture soils in Faisalabad. Environ Exp Botany 54:142–147

    Article  CAS  Google Scholar 

  • Haro H, Sanon KB, Le Roux C, Duponnois R, Traoré AS (2018) Improvement of cowpea productivity by rhizobial and mycorrhizal inoculation in Burkina Faso. Symbiosis 74:107–120

    Article  Google Scholar 

  • Hasan M, Bano A, Hassan SG, Iqbal J, Awan U, Rong-ji D, Khan KA (2014) Enhancement of rice growth and production of growth-promoting phytohormones by inoculation with Rhizobium and other rhizobacteria. World Appl Sci J 31:1734–1743

    Google Scholar 

  • Helene LCF, Delamuta JRM, Ribeiro RA, Hungria M (2017) Bradyrhizobium mercantei sp. nov., a nitrogen-fixing symbiont isolated from nodules of Deguelia costata (syn. Lonchocarpus costatus). Int J Syst Evol Microbiol 67:1827–1834

    Article  CAS  PubMed  Google Scholar 

  • Hellriegel and Wilfarth H (1888) Untersuchungen über die stickstoffnahrung der gramineen und leguminosen. Beilageheft zu der Zeitschrift des Vereins Rübenzucker-Industrie Deutschen Reiches 1–234

    Google Scholar 

  • Hemid M, Abdel-Waha AA, El-Enany E, Allam N, David N, Khalaf M, Morsy FM (2014) Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol Res 169:49–58

    Article  CAS  Google Scholar 

  • Hemissi I, Mabrouk Y, Abdi N, Bouraoui M, Saidi M, Sifi B (2011) Effects of some Rhizobium strains on chickpea growth and biological control of Rhizoctonia solani. Afr J Microbiol Res 5:4080–4090

    CAS  Google Scholar 

  • Hemmat Jou MH, Besalatpour AA (2018) Interactive effects of co-inoculation of Bradyrhizobium japonicum strains and mycorrhiza species on soybean growth and nutrient contents in plant. J Plant Nutr 41:10–18

    Article  CAS  Google Scholar 

  • Htwe AZ, Moh SM, Moe K, Yamakawa T (2018) Effects of co-inoculation of Bradyrhizobium japonicum SAY3-7 and Streptomyces griseoflavus P4 on plant growth, nodulation, nitrogen fixation, nutrient uptake, and yield of soybean in a field condition. Soil Sci Plant Nutr 64:222–229

    Article  CAS  Google Scholar 

  • Hungria M, Nogueira MA, Silva Araújo R (2013) Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biol Fertil Soils 49:791–801

    Article  Google Scholar 

  • Imen H, Neila A, Adnane B, Manel B, Mabrouk Y, Saidi M, Bouaziz S (2015) Inoculation with phosphate solubilizing Mesorhizobium strains improves the performance of chickpea (Cicer arietinum L.) under phosphorus deficiency. J Plant Nutr 38:1656–1671

    Article  CAS  Google Scholar 

  • Jarvis BDW, van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-Marel JC, Gillis M (1997) Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Bacteriol 47:895–898

    Article  Google Scholar 

  • Jiao YS, Yan H, Ji ZJ, Liu YH, Sui XH, Zhang XX, Wang ET, Chen WX, Chen WF (2015) Phyllobacterium sophorae sp. nov., a symbiotic bacterium isolated from root nodules of Sophora flavescens. Int J Syst Evol Microbiol 65:399–406

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Gómez A, Flores-Félix JD, García-Fraile P, Mateos PF, Menéndez E, Velázquez E, Rivas R (2018) Probiotic activities of Rhizobium laguerreae on growth and quality of spinach. Sci Rep 8:295

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jordan DC (1982) Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int J Syst Bacteriol 32:136–139

    Article  Google Scholar 

  • Kaur S, Khanna V (2016) Evaluation of synergistic potential of plant growth promoting rhizobacteria with Rhizobium in mungbean (Vigna radiata L.). J Appl Nat Sci 8:995–998

    Article  CAS  Google Scholar 

  • Kelemu S, Thomas RJ, Moreno CX, Ocampo GI (1995) Strains of Bradyrhizobium from tropical forage legumes inhibit Rhizoctonia solani AG-1 in vitro. Australas Plant Pathol 24:168–172

    Article  Google Scholar 

  • Khandelwal S, Manwar AV, Chaudhari BL, Chincholkar SB (2002) Siderophoregenic Bradyrhizobia boost yield of soybean. Appl Biochem Biotechnol 102:155–168

    Article  PubMed  Google Scholar 

  • Khanna V, Sharma P (2011) Potential for enhancing lentil (Lens culinaris) productivity by co-inoculation with PSB, plant growth-promoting rhizobacteria and Rhizobium. Indian J Agric Sci 81:932–934

    Google Scholar 

  • Kohlmeier MG, Yudistira H, Zhang XL, Fristensky B, Levin DB, Sparling R, Oresnik IJ (2015) Draft genome sequence of the bacteriocin-producing Bradyrhizobium japonicum strain FN1. Genome Announc 3:e00812–e00815

    Article  PubMed  PubMed Central  Google Scholar 

  • Kong Z, Glick BR, Duan J, Ding S, Tian J, McConkey BJ, Wei G (2015) Effects of 1-aminocyclopropane-1-carboxylate (ACC) deaminase-overproducing Sinorhizobium meliloti on plant growth and copper tolerance of Medicago lupulina. Plant Soil 391:383–398

    Article  CAS  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 8:443

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar PR, Ram MR (2012) Production of indole acetic acid by Rhizobium isolates from Vigna trilobata (L) Verdc. African J Microbiol Res 6:5536–5541

    Google Scholar 

  • Kumar H, Bajpai VK, Dubey RC, Maheshwari DK, Kang SC (2010) Wilt disease management and enhancement of growth and yield of Cajanus cajan (L) var. Manak by bacterial combinations amended with chemical fertilizer. Crop Prot 29:591–598

    Article  Google Scholar 

  • Kumar H, Dubey RC, Maheshwari DK (2011) Effect of plant growth promoting rhizobia on seed germination, growth promotion and suppression of Fusarium wilt of fenugreek (Trigonella foenum-graecum L.). Crop Prot 30:1396–1403

    Article  Google Scholar 

  • Laranjo M, Alexandre A, Oliveira S (2014) Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. Microbiol Res 169:2–17

    Article  PubMed  Google Scholar 

  • Leggett M, Diaz-Zorita M, Koivunen M, Bowman R, Pesek R, Stevenson C, Leister T (2017) Soybean response to inoculation with Bradyrhizobium japonicum in the United States and Argentina. Agron J 109:1031–1038

    Article  Google Scholar 

  • Lesueur D, Diem HG, Meyer JM (1993) Iron requirement and siderophore production in Bradyrhizobium strains isolated from Acacia mangium. J Appl Bacteriol 74:675–682

    Article  CAS  Google Scholar 

  • Lin DX, Wang ET, Tang H, Han TX, He YR, Guan SH, Chen WX (2008) Shinella kummerowiae sp. nov., a symbiotic bacterium isolated from root nodules of the herbal legume Kummerowia stipulacea. Int J Syst Evol Microbiol 58:1409–1413

    Article  CAS  PubMed  Google Scholar 

  • Lynch D, O’Brien J, Welch T, Clarke P, Ócuıv P, Crosa JH, O’Connell M (2001) Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J Bacteriol 183:2576–2585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma W, Sebestianova SB, Sebestian J, Burd GI, Guinel FC, Glick BR (2003) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Antonie Van Leeuwenhoek 83:285–291

    Article  CAS  PubMed  Google Scholar 

  • Ma W, Charles TC, Glick BR (2004) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Appl Environ Microbiol 70:5891–5897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mabrouk Y, Mejri S, Belhadj O (2016) Biochemical mechanisms of induced resistance by rhizobial lipopolysaccharide in pea against crenate broomrape. Braz J Bot 39:107–114

    Article  Google Scholar 

  • Malajczuk N, Pearce M, Litchfield RT (1984) Interactions between Phytophthora cinnamomi and Rhizobium isolates. Trans Br Mycol Soc 82:491–500

    Article  Google Scholar 

  • Marcos-García M, Menéndez E, Ramírez-Bahena MH, Mateos PF, Peix Á, Velazquez E, Rivas R (2017) Mesorhizobium helmanticense sp. nov., isolated from Lotus corniculatus nodules. Int J Syst Evol Microbiol 67:2301–2305

    Article  PubMed  CAS  Google Scholar 

  • Martínez R, Espejo A, Sierra M, Ortiz-Bernad I, Correa D, Bedmar E, López-Jurado M, Porres JM (2015) Co-inoculation of Halomonas maura and Ensifer meliloti to improve alfalfa yield in saline soils. Appl Soil Ecol 87:81–86

    Article  Google Scholar 

  • Martins da Costa E, Azarias Guimarães A, Pereira Vicentin R, de Almeida Ribeiro PR, Ribas Leão AC, Balsanelli E, Lebbe L, Aerts M, Willems A, de Souza Moreira FM (2017) Bradyrhizobium brasilense sp. nov., a symbiotic nitrogen-fixing bacterium isolated from Brazilian tropical soils. Arch Microbiol 199:1211–1221

    Article  CAS  PubMed  Google Scholar 

  • Martins da Costa E, Azarias Guimarães A, Soares de Carvalho T, Louzada Rodrigues T, de Almeida Ribeiro PR, Lebbe L, Willems A, de Souza Moreira FM (2018) Bradyrhizobium forestalis sp. nov., an efficient nitrogen-fixing bacterium isolated from nodules of forest legume species in the Amazon. Arch Microbiol 200:743–752

    Article  CAS  PubMed  Google Scholar 

  • Martinuz A, Schouten A, Menjivar RD, Sikora RA (2012) Effectiveness of systemic resistance toward Aphis gossypii (Hom., Aphididae) as induced by combined applications of the endophytes Fusarium oxysporum Fo162 and Rhizobium etli G12. Biol Control 62:206–212

    Article  Google Scholar 

  • Maynaud G, Willems A, Soussou S, Vidal C, Mauré L, Moulin L, Cleyet-Marel JC, Brunel B (2012) Molecular and phenotypic characterization of strains nodulating Anthyllis vulneraria in mine tailings, and proposal of Aminobacter anthyllidis sp. nov., the first definition of Aminobacter as legume-nodulating bacteria. Syst Appl Microbiol 35:65–72

    Article  CAS  PubMed  Google Scholar 

  • McKevith B (2005) Nutritional aspects of oilseeds. Nutr Bull 30:13–26

    Article  Google Scholar 

  • Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663

    Article  CAS  PubMed  Google Scholar 

  • Menéndez E, Ramirez-Bahena MH, Peix A, Tejedor C, Mulas R, González-Andrés F, Martínez-Molina E, Velázquez E (2016) Analysis of cultivable endophytic bacteria in roots of maize in a soil from León province in mainland Spain. In: González-Andrés F, James E (eds) Biological nitrogen fixation and beneficial plant-microbe interaction. Springer, Cham, pp 45–53

    Chapter  Google Scholar 

  • Meng L, Zhang A, Wang F, Han X, Wang D, Li S (2015) Arbuscular mycorrhizal fungi and Rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front Plant Sci 6:339

    PubMed  PubMed Central  Google Scholar 

  • Michel DC, Passos SR, Simões-Araújo JL, Baraúna AC, da Silva K, Parma MM, Melo IS, De Meyer SE, O’Hara G, Zilli JE (2017) Bradyrhizobium centrolobii and Bradyrhizobium macuxiense sp. nov. isolated from Centrolobium paraense grown in soil of Amazonia, Brazil. Arch Microbiol 199:657–664

    Article  CAS  PubMed  Google Scholar 

  • Minamisawa K (1989) Comparison of extracellular polysaccharide composition, rhizobitoxine production, and hydrogenase phenotype among various strains of Bradyrhizobium japonicum. Plant Cell Physiol 30:877–884

    Article  CAS  Google Scholar 

  • Mohamad R, Willems A, Le Quéré A, Maynaud G, Pervent M, Bonabaud M, Dubois E, Cleyet-Marel JC, Brunel B (2017) Mesorhizobium delmotii and Mesorhizobium prunaredense are two new species containing rhizobial strains within the symbiovar anthyllidis. Syst Appl Microbiol 40:135–143

    Article  PubMed  Google Scholar 

  • Mondal HK, Mehta S, Kaur H, Gera R (2017) Characterization of abiotic stress tolerant rhizobia as PGPR of mothbean, clusterbean and mungbean grown in hyper-arid zone of Rajasthan. Int J Bio-Res & Stress Manag 8:309–315

    Article  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411:948–950. Erratum in: Nature 412:926

    Article  CAS  PubMed  Google Scholar 

  • Mousavi SA, Österman J, Wahlberg N, Nesme X, Lavire C, Vial L, Paulin L, De Lajudie P, Lindström K (2014) Phylogeny of the Rhizobium-Allorhizobium-Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Syst Appl Microbiol 37:208–215

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Mulas D, García-Fraile P, Carro L, Ramírez-Bahena MH, Casquero P, Velázquez E, González-Andrés F (2011) Distribution and efficiency of Rhizobium leguminosarum strains nodulating Phaseolus vulgaris in Northern Spanish soils: selection of native strains that replace conventional N fertilization. Soil Biol Biochem 43:2283–2293

    Article  CAS  Google Scholar 

  • Nambiar PTC, Sivaramakrishnan S (1987) Detection and assay of siderophores in cowpea rhizobia (Bradyrhizobium) using radioactive Fe (59Fe). Lett Appl Microbiol 4:37–40

    Article  CAS  Google Scholar 

  • Nascimento FX, Brígido C, Glick BR, Oliveira S (2012) ACC deaminase genes are conserved among Mesorhizobium species able to nodulate the same host plant. FEMS Microbiol Lett 336:26–37

    Article  CAS  PubMed  Google Scholar 

  • Nascimento FX, Rossi MJ, Soares CR, McConkey BJ, Glick BR (2014) New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS One 9:e99168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nascimento FX, Rossi MJ, Glick BR (2018) Ethylene and 1-Aminocyclopropane-1-carboxylate (ACC) in plant-bacterial interactions. Front Plant Sci 9:114

    Article  PubMed  PubMed Central  Google Scholar 

  • Naveed M, Hussain MB, Mehboob I, Zahir ZA (2017) Rhizobial amelioration of drought stress in legumes. In: Zaidi A, Khan M, Musarrat J (eds) Microbes for legume improvement. Springer, Cham, pp 341–365

    Chapter  Google Scholar 

  • Nimnoi P, Pongsilp N, Lumyong S (2014) Co-inoculation of soybean (Glycine max) with actinomycetes and Bradyrhizobium japonicum enhances plant growth, nitrogenase activity and plant nutrition. J Plant Nutr 37:432–446

    Article  CAS  Google Scholar 

  • Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF (1996) Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J Microbiol 42:279–283

    Article  CAS  PubMed  Google Scholar 

  • Oliveira RS, Carvalho P, Marques G, Ferreira L, Nunes M, Rocha I, Ma Y, Carvalho MF, Vosátka M, Freitas H (2017) Increased protein content of chickpea (Cicer arietinum L.) inoculated with arbuscular mycorrhizal fungi and nitrogen-fixing bacteria under water deficit conditions. Sci Food Agric 97:4379–4385

    Article  CAS  Google Scholar 

  • Omar SA, Abd-Alla MH (1998) Biocontrol of fungal root rot diseases of crop plants by the use of rhizobia and bradyrhizobia. Folia Microbiol 43:431–437

    Article  CAS  Google Scholar 

  • Ormeño E, Torres R, Mayo J, Rivas R, Peix A, Velázquez E, Zúñiga D (2007) Phaseolus lunatus is nodulated by a phosphate solubilizing strain of Sinorhizobium meliloti in a Peruvian soil. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate Solubilization. Springer, Heidelberg, pp 143–147

    Chapter  Google Scholar 

  • Othman H, Tamimi SM (2016) Characterization of rhizobia nodulating faba bean plants isolated from soils of Jordan for plant growth promoting activities and N2 fixation potential. Int J Adv Res Biol Sci 3:20–27

    CAS  Google Scholar 

  • Ozkoc I, Deliveli MH (2001) In vitro inhibition of the mycelial growth of some root rot fungi by Rhizobium leguminosarum biovar phaseoli isolates. Turk J Biol 25:435–445

    Google Scholar 

  • Patel HN, Chakraborty RN, Desai SB (1988) Isolation and partial characterization of phenolate siderophore from Rhizobium leguminosarum IARI 102. FEMS Microbiol Lett 56:131–134

    Article  CAS  Google Scholar 

  • Patil A, Kale A, Ajane G, Sheikh R, Patil S (2017) Plant growth-promoting Rhizobium: mechanisms and biotechnological prospective. In: Hansen A, Choudhary D, Agrawal P, Varma A (eds) Rhizobium biology and biotechnology. Soil Biology, vol 50. Springer, Cham, pp 105–134

    Chapter  Google Scholar 

  • Peix A, Rivas-Boyero AA, Mateos PF, Rodríguez-Barrueco C, Martınez-Molina E, Velázquez E (2001) Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorhizobium mediterraneum under growth chamber conditions. Soil Biol Biochem 33:103–110

    Article  CAS  Google Scholar 

  • Pimentel D, Patzek TW (2005) Ethanol production using corn, switchgrass, and wood; biodiesel production using soybean and sunflower. Nat Resour 14:65–76

    Article  CAS  Google Scholar 

  • Prasanna R, Ramakrishnan B, Simranjit K, Ranjan K, Kanchan A, Hossain F, Nain L (2017) Cyanobacterial and rhizobial inoculation modulates the plant physiological attributes and nodule microbial communities of chickpea. Arch Microbiol 199:1311–1323

    Article  CAS  PubMed  Google Scholar 

  • Priyanka M, Wati L (2017) Screening of rhizobial isolates from Vigna radiata for plant growth promoting traits. Res Crops 18:190–195

    Article  Google Scholar 

  • Qureshi MA, Shakir MA, Iqbal A, Akhtar N, Khan A (2011) Co-inoculation of phosphate solubilizing bacteria and rhizobia for improving growth and yield of mungbean (Vigna radiata L.). J Anim Plant Sci 21:491–497

    CAS  Google Scholar 

  • Rabie GH (1998) Induction of fungal disease resistance in Vicia faba by dual inoculation with Rhizobium leguminosarum and vesicular-arbuscular mycorrhizal fungi. Mycopathologia 141:159–166

    Article  CAS  PubMed  Google Scholar 

  • Radl V, Simões-Araújo JL, Leite J, Passos SR, Martins LM, Xavier GR, Rumjanek NG, Baldani JI, Zilli JE (2014) Microvirga vignae sp. nov., a root nodule symbiotic bacterium isolated from cowpea grown in semi-arid Brazil. Int J Syst Evol Microbiol 64:725–730

    Article  PubMed  Google Scholar 

  • Rangel WM, de Oliveira Longatti SM, Ferreira PAA, Bonaldi DS, Guimarães AA, Thijs S, Weyens N, Vangronsveld J, Moreira FMS (2017) Leguminosae native nodulating bacteria from a gold mine as-contaminated soil: multi-resistance to trace elements, and possible role in plant growth and mineral nutrition. Int J Phytoremediation 19:925–936

    Article  CAS  PubMed  Google Scholar 

  • Reimann S, Hauschild R, Hildebrandt U, Sikora RA (2008) Interrelationships between Rhizobium etli G12 and Glomus intraradices and multitrophic effects in the biological control of the root-knot nematode Meloidogyne incognita on tomato. J Plant Dis Protect 115:108–113

    Article  Google Scholar 

  • Reitz M, Rudolph K, Schröder I, Hoffmann-Hergarten S, Hallmann J, Sikora RA (2000) Lipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida. Appl Environ Microbiol 66:3515–3518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Remigi P, Zhu J, Young JPW, Masson-Boivin C (2016) Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 24:63–75

    Article  CAS  PubMed  Google Scholar 

  • Ren CG, Bai YJ, Kong CC, Bian B, Xie ZH (2016) Synergistic interactions between salt-tolerant rhizobia and arbuscular mycorrhizal fungi on salinity tolerance of Sesbania cannabina plants. J Plant Growth Regul 35:1098–1107

    Article  CAS  Google Scholar 

  • Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E (2002) A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl Environ Microbiol 68:5217–5222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivas R, Peix A, Mateos PF, Trujillo ME, Martínez-Molina E, Velázquez E (2006) Biodiversity of populations of phosphate solubilizing rhizobia that nodulates chickpea in different Spanish soils. Plant Soil 287:23–33

    Article  CAS  Google Scholar 

  • Robleto EA, Scupham AJ, Triplett EW (1997) Trifolitoxin production in Rhizobium etli strain CE3 increases competitiveness for rhizosphere growth and root nodulation of Phaseolus vulgaris in soil. Mol Plant-Microbe Interact 10:228–233

    Article  Google Scholar 

  • Robleto EA, Borneman J, Triplett EW (1998) Effects of bacterial antibiotic production on rhizosphere microbial communities from a culture independent perspective. Appl Env Microbiol 64:5020–5022

    CAS  Google Scholar 

  • Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotech Adv 17:319–339

    Article  Google Scholar 

  • Rubio-Canalejas A, Celador-Lera L, Cruz-González X, Menéndez E, Rivas R (2016) Rhizobium as potential biofertilizer of Eruca Sativa. In: González-Andrés F, James E (eds) Biological nitrogen fixation and beneficial plant-microbe interaction. Springer, Heidelberg, pp 213–220

    Chapter  Google Scholar 

  • Saber WIA, Abd El-Hai KM, Ghoneem KM (2009) Synergistic effect of Trichoderma and Rhizobium on both biocontrol of chocolate spot disease and induction of nodulation, physiological activities and productivity of Vicia faba. Res J Microbiol 4:286–300

    Article  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 18:253–268

    CAS  Google Scholar 

  • Saha M, Sarkar S, Sarkar B, Kumar B, Bhattacharjee SS, Tribedi P (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollution Res 23:3984–3999

    Article  CAS  Google Scholar 

  • Samago TY, Anniye EW, Dakora FD (2018) Grain yield of common bean (Phaseolus vulgaris L.) varieties is markedly increased by rhizobial inoculation and phosphorus application in Ethiopia. Symbiosis 75:245–255

    Article  PubMed  PubMed Central  Google Scholar 

  • Sannazzaro AI, Torres Tejerizo G, Fontana MF, Cumpa Velásquez LM, Hansen LH, Pistorio M, Estrella MJ (2018) Mesorhizobium sanjuanii sp. nov., isolated from nodules of Lotus tenuis in the saline-alkaline lowlands of flooding Pampa, Argentina. Int J Syst Evol Microbiol 68:2936–2942

    Article  CAS  PubMed  Google Scholar 

  • Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda Mdel C, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  CAS  PubMed  Google Scholar 

  • Sawana A, Adeolu M, Gupta RS (2014) Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 5:429

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schwinghamer EA, Brockwell J (1978) Competitive advantage of bacteriocin and phage-producing strains of Rhizobium trifolii in mixed culture. Soil Biol Biochem 10:383–387

    Article  CAS  Google Scholar 

  • Shaban WI, El-Bramawy MA (2011) Impact of dual inoculation with Rhizobium and Trichoderma on damping off, root rot diseases and plant growth parameters of some legumes field crop under greenhouse conditions. Int Res J Agric Sci Soil Sci 1:98–108

    Google Scholar 

  • Sharma SR, Rao NK, Gokhale TS, Ismail S (2013) Isolation and characterization of salt-tolerant rhizobia native to the desert soils of United Arab Emirates. Emirates J Food Agric 25:102–108

    Article  Google Scholar 

  • Shinde BP, Thakur J (2016) The effect of co-inoculation of pea plants with arbuscular mycorrhizal fungi and rhizobium on the nodulation, growth and productivity. Int J Bioassays 10:4954–4957

    Google Scholar 

  • Siddiqui IA, Ehteshamul-Haque S, Zaki MJ, Ghaffar A (2000) Greenhouse evaluation of rhizobia as biocontrol agent of root-infecting fungi in okra. Acta Agrobot 53:13–22

    Article  Google Scholar 

  • Siddiqui ZA, Baghel G, Akhtar MS (2007) Biocontrol of Meloidogyne javanica by Rhizobium and plant growth-promoting rhizobacteria on lentil. World J Microbiol Biotechnol 23:435–441

    Article  CAS  Google Scholar 

  • Singh PK, Singh M, Vyas D (2010) Biocontrol of fusarium wilt of chickpea using arbuscular mycorrhizal fungi and Rhizobium leguminosarum biovar. Caryologia 63:349–353

    Article  Google Scholar 

  • Skerman VBD, McGowan V, Sneath PHA (1980) Approved lists of bacterial names. Int J Syst Bacteriol 30:225–420

    Article  Google Scholar 

  • Soliman AS, Shanan NT, Massoud ON, Swelim DM (2012) Improving salinity tolerance of Acacia saligna (Labill.) plant by arbuscular mycorrhizal fungi and Rhizobium inoculation. African J Biotechnol 11:1259–1266

    Article  CAS  Google Scholar 

  • Sridevi M, Mallaiah KV, Yadav NCS (2007) Phosphate solubilization by Rhizobium isolates from Crotalaria species. J Plant Sci 2:635–639

    Article  CAS  Google Scholar 

  • Staudinger C, Mehmeti-Tershani V, Gil-Quintana E, Gonzalez EM, Hofhansl F, Bachmann G, Wienkoop S (2016) Evidence for a rhizobia-induced drought stress response strategy in Medicago truncatula. J Proteome 136:202–213

    Article  CAS  Google Scholar 

  • Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonça-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266

    Article  PubMed  Google Scholar 

  • Subramanian P, Ramasamy KK, Sundaram KS, 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

    Article  CAS  Google Scholar 

  • Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tajini F, Trabelsi M, Drevon JJ (2011) Co-inoculation with Glomus intraradices and Rhizobium tropici CIAT899 increases P use efficiency for N2 fixation in the common bean (Phaseolus vulgaris L.) under P deficiency in hydroaeroponic culture. Symbiosis 53:123

    Article  CAS  Google Scholar 

  • Tan KZ, Radziah O, Halimi MS, Khairuddin AR, Shamsuddin ZH (2015) Assessment of plant growth-promoting rhizobacteria (PGPR) and rhizobia as multi-strain biofertilizer on growth and N2 fixation of rice plant. Austr J Crop Sci 9:1257–1264

    CAS  Google Scholar 

  • Tarafder HK, Dey A, Dasgupta S (2016) Co-inoculation of phosphate solubilizing bacteria and rhizobia for improving growth and yield of mungbean (Vigna radiata L.). Asian J Soil Sci 11:207–212

    Article  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 

  • Thakur D, Kaushal R, Shyam V (2014) Phosphate solubilising microorganisms: role in phosphorus nutrition of crop plants-a review. Agric Rev 35:159–171

    Article  Google Scholar 

  • Triplett EW, Barta TM (1987) Trifolitoxin production and nodulation are necessary for the expression of superior nodulation competitiveness by Rhizobium leguminosarum bv. Trifolii strain T24 on clover. Plant Physiol 85:335–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trujillo ME, Willems A, Abril A, Planchuelo AM, Rivas R, Ludeña D, Mateos PF, Martínez-Molina E, Velázquez E (2005) Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71:1318–1327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tu JC (1978) Protection of soybean from severe Phytophthora root rot by Rhizobium. Physiol Plant Pathol 12:233–240

    Article  Google Scholar 

  • Ullah S, Khan MY, Asghar HN, Akhtar MJ, Zahir ZA (2017) Differential response of single and co-inoculation of Rhizobium leguminosarum and Mesorhizobium ciceri for inducing water deficit stress tolerance in wheat. Ann Microbiol 67:739–749

    Article  Google Scholar 

  • Validation List no. 107 (2006) Int J Syst Evol Microbiol 56:1–6

    Article  Google Scholar 

  • Valverde A, Velázquez E, Fernández-Santos F, Vizcaíno N, Rivas R, Mateos PF, Martínez-Molina E, Igual JM, Willems A (2005) Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int J Syst Evol Microbiol 55:1985–1989

    Article  CAS  PubMed  Google Scholar 

  • Vandamme P, Coenye T (2004) Taxonomy of the genus Cupriavidus: a tale of lost and found. Int J Syst Evol Microbiol 54:2285–2289

    Article  PubMed  Google Scholar 

  • Vargas LK, Volpiano CG, Lisboa BB, Giongo A, Beneduzi A, Passaglia LMP (2017) Potential of rhizobia as plant growth-promoting rhizobacteria. In: Zaidi A, Khan M, Musarrat J (eds) Microbes for legume improvement. Springer, Cham, pp 153–174

    Chapter  Google Scholar 

  • Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A (2016) Role of plant growth promoting Rhizobacteria in agricultural sustainability-a review. Molecules 21:piiE573

    Article  CAS  Google Scholar 

  • Velázquez E, Carro L, Flores-Félix JD, Martínez-Hidalgo P, Menéndez E, Ramírez-Bahena MH, Mulas R, González-Andrés F, Martínez-Molina E, Peix A (2017a) 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, Singapore, pp 41–70

    Chapter  Google Scholar 

  • Velázquez E, García-Fraile P, Ramírez-Bahena MH, Rivas R, Martínez-Molina E (2017b) Current status of the taxonomy of bacteria able to establish nitrogen-fixing legume symbiosis. In: Zaidi A, Khan M, Musarrat J (eds) Microbes for legume improvement. Springer, Cham, pp 1–43

    Google Scholar 

  • Venter AP, Twelker S, Oresnik IJ, Hynes MF (2001) Analysis of the genetic region encoding a novel rhizobiocin from Rhizobium leguminosarum bv. Viciae strain 306. Can J Microbiol 47:495–502

    Article  CAS  PubMed  Google Scholar 

  • Verma JP, Yadav J, Tiwari KN (2012) Enhancement of nodulation and yield of chickpea by co-inoculation of indigenous Mesorhizobium spp. and plant growth–promoting rhizobacteria in Eastern Uttar Pradesh. Comm Soil Sci Plant Anal 43:605–621

    Article  CAS  Google Scholar 

  • Verma JP, Yadav J, Tiwaric KN, Kumarb A (2013) Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286

    Article  Google Scholar 

  • Vicario JC, Primo ED, Dardanelli MS, Giordano W (2016) Promotion of peanut growth by co-inoculation with selected strains of Bradyrhizobium and Azospirillum. J Plant Growth Regul 35:413–419

    Article  CAS  Google Scholar 

  • Vieira JD, da Silva PRD, Stefenon VM (2017) In vitro growth and indoleacetic acid production by Mesorhizobium loti SEMIA806 and SEMIA816 under the influence of copper ions. Microbiol Res 8:57–58

    Article  CAS  Google Scholar 

  • Villar-Igea M, Velázquez E, Rivas R, Willems A, van Berkum P, Trujillo ME, Mateos PF, Gillis M, Martínez-Molina E (2007) Phosphate solubilizing rhizobia originating from Medicago, Melilotus and Trigonella grown in a Spanish soil. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate Solubilization. Springer, Heidelberg, pp 149–156

    Chapter  Google Scholar 

  • Vincent JM (1970) The cultivation, isolation and maintenance of rhizobia. In: Vincent JM (ed) A manual for the practical study of root-nodule. Blackwell Scientific Publications, Oxford, pp 1–13

    Google Scholar 

  • Wang Y, Zhang Z, Zhang P, Cao Y, Hu T, Yang P (2016) Rhizobium symbiosis contribution to short-term salt stress tolerance in alfalfa (Medicago sativa L.). Plant Soil 402:247–261

    Article  CAS  Google Scholar 

  • Wdowiak-Wróbel S, Małek W (2016) Properties of Astragalus sp. microsymbionts and their putative role in plant growth promotion. Arch Microbiol 198:793–801

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wolde-meskel E, Heerwaarden J, Abdulkadir B, Kassa S, Aliyi I, Degefu T, Wakwey K, Kanampiu F, Giller KE (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 

  • Wright W, Little J, Liu F, Chakraborty R (2013) Isolation and structural identification of the trihydroxamate siderophore vicibactin and its degradative products from Rhizobium leguminosarum ATCC 14479 bv. trifolii. Bio Metals 26:271–283

    CAS  Google Scholar 

  • Xu L, Shi J, Li C, Zhu S, Li B (2017) Rhizobium hedysari sp. nov., a novel species isolated from a root nodule of Hedysarum multijugum in China. Antonie Van Leeuwenhoek 110:479–488

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Zhang Y, Mohamad OA, Jiang C, Friman VP (2018) Mesorhizobium zhangyense sp. nov., isolated from wild Thermopsis lanceolate in northwestern China. Arch Microbiol 200:603–610

    Article  CAS  PubMed  Google Scholar 

  • Yadav J, Verma JP (2014) Effect of seed inoculation with indigenous Rhizobium and plant growth promoting rhizobacteria on nutrients uptake and yields of chickpea (Cicer arietinum L.). Eur J Soil Biol 63:70–77

    Article  CAS  Google Scholar 

  • Yan J, Li Y, Yan H, Chen WF, Zhang X, Wang ET, Han XZ, Xie ZH (2017a) Agrobacterium salinitolerans sp. nov., a saline-alkaline-tolerant bacterium isolated from root nodule of Sesbania cannabina. Int J Syst Evol Microbiol 67:1906–1911

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Yan H, Liu LX, Chen WF, Zhang XX, Verástegui-Valdés MM, Wang ET, Han XZ (2017b) Rhizobium hidalgonense sp. nov., a nodule endophytic bacterium of Phaseolus vulgaris in acid soil. Arch Microbiol 199:97–104

    Article  CAS  PubMed  Google Scholar 

  • Yanni YG, Dazzo FB (2010) Enhancement of rice production using endophytic strains of Rhizobium leguminosarum bv. trifolii in extensive field inoculation trials within the Egypt Nile delta. Plant Soil 336:129–142

    Article  CAS  Google Scholar 

  • Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, de Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. In: Ladha JK, de Bruijn FJ, Malik KA (eds) Opportunities for biological nitrogen fixation in rice and other non-legumes. Developments in plant and soil sciences, vol 75. Springer, Dordrecht, pp 99–114

    Chapter  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, Martínez-Molina E, Mateos P, Velázquez E, Wopereis J, Triplett E, Umali-García 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. Australian J Plant Physiol 28:845–870

    CAS  Google Scholar 

  • Yanni YG, Dazzo FB, Squartini A, Zanardo M, Zidan MI, Elsadany AEY (2016) Assessment of the natural endophytic association between Rhizobium and wheat and its ability to increase wheat production in the Nile delta. Plant Soil 407:367–383

    Article  CAS  Google Scholar 

  • Yanni Y, Zidan M, Dazzo F, Rizk R, Mehesen A, Abdelfattah F, Elsadany A (2018) Enhanced symbiotic performance and productivity of drought stressed common bean after inoculation with tolerant native rhizobia in extensive fields. Agric Ecosyst Environ 232:119–128

    Article  Google Scholar 

  • Yuhashi K, Ichikawa N, Ezura H, Akao S, Minakawa Y, Nukui N, Yasuta T, Minamisawa K (2000) Rhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum. Appl Environ Microbiol 66:2658–2663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuttavanichakul W, Lawongs P, Wongkaew S, Teaumroong N, Boonkerd N, Nomura N, Tittabutr P (2012) Improvement of peanut rhizobial inoculant by incorporation of plant growth promoting rhizobacteria (PGPR) as biocontrol against the seed borne fungus Aspergillus niger. Biol Control 63:87–97

    Article  Google Scholar 

  • Zhang J, Guo C, Chen W, de Lajudie P, Zhang Z, Shang Y, Wang ET (2018) Mesorhizobium wenxiniae sp. nov., isolated from chickpea (Cicer arietinum L.) in China. Int J Syst Evol Microbiol 68:1930–1936

    Article  CAS  PubMed  Google Scholar 

  • Zhu RF, Tang F, Liu J, Liu FQ, Deng XY, Chen JS (2016) Co-inoculation of arbuscular mycorrhizae and nitrogen fixing bacteria enhance alfalfa yield under saline conditions. Pak J Bot 48:763–769

    Article  CAS  Google Scholar 

  • Zurdo-Piñeiro JL, Rivas R, Trujillo ME, Vizcaíno N, Carrasco JA, Chamber M, Palomares A, Mateos PF, Martínez-Molina E, Velázquez E (2007) Ochrobactrum cytisi sp. nov., isolated from nodules of Cytisus scoparius in Spain. Int J Syst Evol Microbiol 57:784–788

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank their numerous collaborators and students involved in this research over the years. Funding was provided by “Ministerio de Economía, Ciencia, Industria y Competitividad (MINECO)” through the Projects AGL2010-17380 and AGL2013-48098-P, by “Junta de Castilla y León” through the project SA058U16 and by the “Diputación de Salamanca (local Government)” through the Projects V113/463AC06 and 18VB2I/463AC06.

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  1. Departamento de Microbiología y Genética, Universidad de Salamanca, Salamanca, Spain

    Encarna Velázquez, Lorena Carro, José David Flores-Félix, Esther Menéndez & Martha-Helena Ramírez-Bahena

  2. Unidad Asociada Universidad de Salamanca- CSIC ‘Interacción Planta-Microorganismo’, Salamanca, Spain

    Encarna Velázquez & Alvaro Peix

  3. IRNASA-CSIC, Salamanca, Spain

    Alvaro Peix

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  1. Encarna Velázquez
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Correspondence to Encarna Velázquez .

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  1. Himalayan School of Biosciences, Swami Rama Himalayan University, Dehradun, Uttarakhand, India

    Vivek Kumar

  2. School of Environmental Science & Engg, Sun Yat-sen University, Guangzhou, Guangdong, China

    Ram Prasad

  3. Centre for Life Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India

    Manoj Kumar

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

    Devendra K. Choudhary

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Velázquez, E., Carro, L., Flores-Félix, J.D., Menéndez, E., Ramírez-Bahena, MH., Peix, A. (2019). Bacteria-Inducing Legume Nodules Involved in the Improvement of Plant Growth, Health and Nutrition. In: Kumar, V., Prasad, R., Kumar, M., Choudhary, D. (eds) Microbiome in Plant Health and Disease. Springer, Singapore. https://doi.org/10.1007/978-981-13-8495-0_4

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