Skip to main content
SpringerLink
Log in

Genetic Diversity of Soybean Root Nodulating Bacteria

  • Chapter
  • First Online:
Bacterial Diversity in Sustainable Agriculture

Part of the book series: Sustainable Development and Biodiversity ((SDEB,volume 1))

Abstract

Soybean (Glycine max L. Merrill), is a summer annual herb grown extensively in China, Argentina, Brazil and USA. It was thought to be very selective for its symbiotic partner. Earlier, only Bradyrhizobium japonicum was reported to nodulate soybean. It now is reported to be nodulated by a number of rhizobial genera and species; Rhizobium, Bradyrhizobium, Mesorhizobium and Sinorhizobium. Sinorhizobial species (fredii) nodulating soybean shows broad host range, where as the slow growing Bradyrhizobium is more selective. Slow growing B. japonicum, B. elkanii, B. liaoningense and B. yuanmingense are more effective nodulaters of soybean. Fast growers Rhizobium tropici, Rhizobium sp., Rhizobium oryzae and Mesorhizobium tianshanense have also been reported to form nodules on soybean. A large genetic diversity exists within the slow growing Bradyrhizobium isolates nodulating soybean. Due to the ecological and economic importance, the Bradyrhizobia species and their diversity have been extensively investigated in the last few years. The diversity and the size of indigenous population in soil can vary with the presence of the host legume and the history of the land use pattern at the sampling site. This review focuses on the genetic diversity existing in the bacteria nodulating soybean with special reference to Indian work.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abe J, Xu D, Suzuki Y, Kanazawa A (2003) Soybean germplasm pools in Asia revealed by nuclear SSRs. Theor Appl Genet 106:445–453

    CAS  PubMed  Google Scholar 

  • Adhikari D, Kaneto M, Itoh K, Suyama K, Pokharel BB, Gaihre YK (2012) Genetic diversity of soybean-nodulating rhizobia in Nepal in relation to climate and soil properties. Plant Soil 357:131–145

    Article  CAS  Google Scholar 

  • Alberton O, Kaschuk G, Hungria M (2006) Sampling effects on the assessment of genetic diversity of rhizobia associated with soybean and common bean. Soil Biol Biochem 38:1298–1307

    Article  CAS  Google Scholar 

  • Amor BB, Shaw SL, Oldroyd GED, Maillet F, Penmetsa RV, Cook D, Long SR, Denarie J, Gough C (2003) The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J 34:495–506

    Article  PubMed  Google Scholar 

  • Anderson JW, Johnstone BM, Cook-Newell ME (1995) Meta-analysis of the effects of soy protein intake on serum lipids. New Eng J Med 333:276–282

    Article  CAS  PubMed  Google Scholar 

  • Andriankaja A, Boisson-Demier A, Frances L, Sauviac L, Jauneau A, Barker DG, de Cavalho-Niebel F (2007) AP2-ERF transcription factors mediate Nod factor-dependent MtENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19:2866–2885

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Annapurna K, Balakrishnan N, Vital L (2007) Verification and rapid identification of soybean rhizobia in Indian soils. Curr Microbiol 54:287–291

    Article  CAS  PubMed  Google Scholar 

  • Appunu C, Angele N, Laguerre G (2008) Genetic diversity of native Bradyrhizobia isolated from soybeans (Glycine max L.) in different agricultural-ecological-climatic regions of India. Appl Environ Microbiol 74:5991–5996

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Appunu C, Sasirekha N, Prabavathy VR, Nair S (2009) A significant proportion of indigenous rhizobia from India associated with soybean (Glycine max L.) distinctly belong to Bradyrhizobium and Ensifer genera. Biol Fertil Soils 46:57–63

    Article  Google Scholar 

  • Balatti PA, Pueppke SG (1992) Identifiation of North American soybean lines that form nitrogen-fixing nodules with Rhizobium fredii USDA 257. Can J Plant Science 72:49–55

    Article  Google Scholar 

  • Carroll BJ, McNeil DL, Gresshoff PM (1985) Isolation and properties of soybean [Glycine max (L.) Merr.] mutants that nodulate in the presence of high nitrate concentrations. Proc Natl Acad Sci U S A 82:4162–4166

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen LS, Figueredo A, Pedrosa FO, Hungria M (2000) Genetic Characterization of Soybean Rhizobia in Paraguay. App Environ Microbiol 66:5099–5103

    Article  CAS  Google Scholar 

  • Chen W, Wang E, Wang S, Li Y, Chen X, Li Y (1995) Characteristics of Rhizobium tianshanense sp. nov., a moderately and slowly growing root nodule bacterium isolated from an arid saline environment in Xinjiang, People’s Republic of China. Int J Syst Bacteriol 45:153–159

    Article  CAS  PubMed  Google Scholar 

  • Chen WX, Yan GH, Li JL (1988) Numerical taxonomic study of fast-growing soybean rhizobia and proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int J Syst Bacteriol 38:392–397

    Article  Google Scholar 

  • Chueire LMO, Hungria M (1997) N2-fixation ability of Brazilian soybean cultivars with Sinorhizobium fredii and Sinorhizobium xinjiangensis. Plant Soil 196:1–5

    Article  Google Scholar 

  • Delamuta JRM, Ribeiro RA, Menna P, Bangel EV, Hungria M (2012) Multilocus sequence analysis (MLSA) of Bradyrhizobium strains: revealing high diversity of tropical diazotrophic symbiotic bacteria. Braz J Microbiol 43:698–710

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Delves AC, Mathews A, Day DA, Carter AS, Carroll BJ, Gressshoff PM (1986) Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiol 82:588–590

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Denarie J, Debelle F, Prome JC (1996) Rhizobium lipochitooligosaccharide nodulation factors: signalling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535

    Article  CAS  PubMed  Google Scholar 

  • Dowdle SF, Bohlool BB (1985) Predominance of fast-growing Rhizobium japonicum in a soybean field in the People’s Republic of China. Appl Environ Microbiol 50:1171–1176

    Google Scholar 

  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966

    Article  CAS  PubMed  Google Scholar 

  • Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid DE, Gresshoff PM (2010) Molecular Analysis of Legume Nodule Development and Autoregulation. J Integ Plant Biol 52:61–76

    Article  CAS  Google Scholar 

  • Fred EB, Baldwin IL, McCoy E (1932) Root nodule bacteria and leguminous plants. UW-Madison Libraries Parallel Press (5)

    Google Scholar 

  • Gai JY, Xu DH, Gao Z (2000) Studies on the evolutionary relationship among eco-types of G. max and G. soja in China. Acta Agron Sinica 26:513–520

    Google Scholar 

  • Giongo A, Ambrosini A, Vargas LK, Freire JRJ, Bodanese-Zanettini MH, Passaglia LMP (2008) Evaluation of genetic diversity of bradyrhizobia strains nodulating soybean [Glycine max (L.) Merrill] isolated from South Brazilian fields. Appl Soil Ecol 38:261–269

    Article  Google Scholar 

  • Guo HJ, Wang ET, Zhang XX, Li QQ, Zhang YM, Tian CF, Chen WX (2014) Replicon-dependent differentiation of symbiosis-related genes in Sinorhizobium  strains nodulating Glycine max . Appl Environ Microbiol 80:1245–1255. doi: 10.1128/AEM.03037-13. Epub 6 Dec 2013

    Google Scholar 

  • Han LL, Wang ET, Han TX, Liu J, Sui XH, Chen WF, Chen WX (2009) Unique community structure and biogeography of soybean rhizobia in the saline-alkaline soils of Xinjiang, China. Plant Soil 324:291–305

    Article  CAS  Google Scholar 

  • Hirsch S, Oldroyd G (2009) Integrated Nod factor signaling in plants. In: Frantisek B, Stefano M (eds) Signaling in plants. Springer, Berlin, pp 71–90

    Chapter  Google Scholar 

  • Holt S, Muntyan I, Likver L (1996) Soya-Based Diets for Diabetes Mellitus. Altern Complement Ther 2:79–82

    Article  Google Scholar 

  • Hungria M, Chueire LMO, Megias M, Lamrabet Y, Probanza A, Guttierrez-Manero FJ, Campo RJ (2006) Genetic diversity of indigenous tropical fast-growing rhizobia isolated from soybean nodules. Plant Soil 288:343–356

    Article  CAS  Google Scholar 

  • Indrasumunar A, Kereszt A, Searle I, Miyagi M, Li D, Nguyen CDT, Men A, Carroll BJ, Gresshoff PM (2010) Inactivation of duplicated Nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol 51:201–214

    Article  CAS  PubMed  Google Scholar 

  • Indrasumunar A, Searle I, Lin MH, Kereszt A, Men A, Carroll, B.J. Gresshoff PM (2011) Nodulation factor receptor kinase 1a controls nodule organ number in soybean (Glycine max L. Merr.). Plant J 65:39–50

    Article  CAS  PubMed  Google Scholar 

  • Jensen ES, Peoples MB, Boddey RM, Gresshoff PM, Hauggaard-Nielsen H, Alves BJR, Morrison MJ (2012) Legumes for mitigation of climate change and feedstock in a bio-based economy: a review. Agro Sustain Dev 32:329–364

    Article  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 

  • Kalo P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GED (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308:1786–1789

    Article  CAS  PubMed  Google Scholar 

  • Kamst E, Spaink H, Kafetzopoulos D (1998) Biosynthesis and secretion of rhizobial lipochitin-oligosaccharide signal molecules. Subcell Biochem 29:29–70

    Article  CAS  PubMed  Google Scholar 

  • Keyser HH, Bohlool BB, Hu TS, Weber DF (1982) Fast-growing rhizobia isolated from root nodules of soybean. Science 215:1631–1632

    Article  CAS  PubMed  Google Scholar 

  • Kosslak RM, Bookland R, Barkei J, Paaren HE, Appelbaum ER (1987) Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci U S A 84:7428–7432

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, Bruijn FD, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426

    Article  CAS  PubMed  Google Scholar 

  • Kuykendall LD, Saxena B, Devine TE, Udell SE (1992) Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can J Microbiol 38:501–505

    Article  CAS  Google Scholar 

  • Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle F (2004) A putative Ca2+ and calmodulindependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364

    Article  CAS  PubMed  Google Scholar 

  • Li QQ, Wang ET, Zhang YZ, Zhang YM, Tian CF, Sui XH, Chen WF, Chen WX (2011a) Diversity and biogeography of rhizobia isolated from root nodules of Glycine max grown in Hebei Province, China. Microb Ecol 61:917–931

    Article  Google Scholar 

  • Li QQ, Wang ET, Chang YL, Zhang YZ, Zhang YM, Sui XH, Chen WF, Chen WX (2011b) Ensifer sojae sp. nov., isolated from root nodules of Glycine max grown in saline-alkaline soils. Int J Syst Evol Microbiol 61:1981–1988

    Article  CAS  Google Scholar 

  • Lim CW, Lee YW, Hwang CH (2011) Soybean nodule-enhanced CLE peptides in roots act as signals in GmNARK-mediated nodulation suppression. Plant Cell Physiol 52:1613–1627

    Article  CAS  PubMed  Google Scholar 

  • Lin MH, Gresshoff PM, Ferguson BJ (2012) Systemic regulation of soybean nodulation by acidic growth conditions. Plant Physiol 160:2028–2039

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640

    Article  CAS  PubMed  Google Scholar 

  • Malik MFA, Qureshi AS, Ashraf M, Ghafoor A (2006) Genetic variability of the main yield related characters in soybean. Int J Agri Biol 8:815–819

    Google Scholar 

  • Man CX, Wang H, Chen WF, Sui XH, Wang ET, Chen WX (2008) Diverse rhizobia associated with soybean grown in the subtropical and tropical regions of China. Plant Soil 310:77–87

    Article  CAS  Google Scholar 

  • Marchetti M, Capela D, Glew M, Cruveiller S, Chane-Woon-Ming B, Gris C et al (2010). Experimental evolution of a plant pathogen into a legume symbiont. Plos Biol 8: e1000280

    Google Scholar 

  • Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GED (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martens M, Dawyndt P, Coopman R, Gillis M, De Vos P, Willems A (2008) Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol 58:200–214

    Article  CAS  PubMed  Google Scholar 

  • Menna P, Barcellos FG, Hungria M (2009) Phylogeny and taxonomy of a diverse collection of Bradyrhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and glnII, recA, atpD and dnaK genes. Int J Syst Evol Microbiol 59:2934–2950

    Article  CAS  PubMed  Google Scholar 

  • Minamisawa K, Nakatsuka Y, Isawa T (1999) Diversity and field site variation of indigenous populations of soybean bradyrhizobia in japan by fingerprints with repeated sequences RSα, RSβ. FEMS Microbiol Ecol 29:171–178

    CAS  Google Scholar 

  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GED, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci U S A 101:4701–4705

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miyahara A, Hirani TA, Oakes M, Kereszt A, Kobe B, Djordjevic MA, Gresshoff PM (2008) Soybean nodule autoregulation receptor kinase phosphorylates two kinase-associated protein phosphatases in vitro. J Biol Chem 283:25381–25391

    Article  CAS  PubMed  Google Scholar 

  • Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kaawaguchi M (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429

    Article  CAS  PubMed  Google Scholar 

  • Oka-Kira E, Tateno K, Miura K, Haga T, Hayashi M, Harada K, Sato S, Tabata S, Shikazono N, Tanaka A, Watanabe Y, Fukuhara I, Nagata T, Kawaguchi M (2005) klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction. Plant J 44:505–515

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The Rules of Engagement in the Legume-Rhizobial Symbiosis. Annu Rev Genet 45:119–144

    Article  CAS  PubMed  Google Scholar 

  • Ormeno-Orrillo E, Vinuesa P, Zuniga-Davila D, Martínez-Romero E (2006) Molecular diversity of native bradyrhizobia isolated from lima bean (Phaseolus lunatus L.) in Peru. Syst Appl Microbiol 29:253–262

    Article  CAS  PubMed  Google Scholar 

  • Peng G, Yuan Q, Li H, Zhang W, Tan Z (2008) Rhizobium oryzae sp. nov., isolated from the wild rice Oryza alta. Int J Syst Evol Microbiol 58:2158–2163

    Article  CAS  PubMed  Google Scholar 

  • Peng GX, Tan ZY, Wang ET, Reinhold-Hurek B, Chen WF, Chen WX (2002) Identification of isolates from soybean nodules in Xinjiang Region as Sinorhizobium xinjiangense and genetic differentiation of S. xinjiangense from Sinorhizobium fredii. Int J Syst Evol Microbiol 52:457–462

    CAS  PubMed  Google Scholar 

  • Peoples MB, Brockwell J, Herridge DF, Rochester IJ, Alves BJR, Urquiaga S, Boddey RM, Dakora FD, Bhattarai S, Maskey SL, Sampet C, Rerkasem B, Khans DF, Hauggaard-Nielsen H, Jensen BS (2009) The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48:1–17

    Article  CAS  Google Scholar 

  • Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592

    Article  CAS  PubMed  Google Scholar 

  • Reid DE, Ferguson BJ, Gresshoff PM (2011) Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant Microbe Interact 24:606–618

    Article  CAS  PubMed  Google Scholar 

  • Reid DE, Li D, Ferguson BJ, Gresshoff PM (2013) Structure-function analysis of the GmRIC1 signal peptide and CLE domain required for nodulation control in soybean. J Exp Bot 64:1575–1585

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Risal CP, Yokoyama T, Ohkama-Ohtsu N, Djedidi S, Sekimoto H (2010) Genetic diversity of native soybean bradyrhizobia from different topographical regions along the southern slopes of the Himalayan Mountains in Nepal. Syst Appl Microbiol 33:416–425

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Navarro DN, Ruiz-Sainz JE, BuendõÂa-ClaverõÂa A, Santamaria C, Balatti PA, Krishnan HB, Pueppke SG (1996) Characterization of fast-growing rhizobia from nodulated soybean [Glycine max (L.) Merr.] in Vietnam. Syst Appl Microbiol 9:240–248

    Article  Google Scholar 

  • Salvagiotti F, Cassman KG, Specht JE, Walters DT, Weiss A, Dobermann A (2008) Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crops Res 108:1–13

    Article  Google Scholar 

  • SatyaPrakash C, Annapurna K (2006) Diversity of soybean bradyrhizobial population adapted to an Indian soil. J Plant Biochem Biotechnol 15:27–32

    Article  Google Scholar 

  • Sawada Y, Miyashita K, Tanabe I, Kato K (1989) Hup phenotype and serogroup identity of soybean nodulating bacteria isolated from Japanese soils. Soil Sci Plant Nutr 35:281–288

    Google Scholar 

  • Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195

    Article  CAS  PubMed  Google Scholar 

  • Scholla MH, Elkan GH (1984) Rhizobium fredii sp. nov., a fast growing species that effectively nodulates soybeans. Int J Syst Bacteriol 34:484–486

    Article  Google Scholar 

  • Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carrol BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109–112

    Article  CAS  PubMed  Google Scholar 

  • Shiro S, Matsuura S, Saiki R, Sigua GC, Yamamoto A, Umehara Y, Hayashi M, Saeki Y (2013) Genetic Diversity and Geographical Distribution of Indigenous Soybean-Nodulating Bradyrhizobia in the United States. Appl Environ Microbiol 79:3610–3618

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smit G, Puvanesarajah V, Carlson RW, Barbour WM, Stacey G (1992) Bradyrhizobium japonicum nodD1 can be specifically induced by soybean flavonoids that do not induce the nodYABCSUIJ operon. J Biol Chem 267:310–318

    CAS  PubMed  Google Scholar 

  • Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod-factor-induced transcription. Science 308:1789–1791

    Article  CAS  PubMed  Google Scholar 

  • Stowers MD, Eaglesham AR (1984) Physiological and symbiotic characteristics of fast-growing Rhizobium japonicum. Plant Soil 77:3–14

    Article  Google Scholar 

  • Sugiyama A, Shitan N, Yazaki K (2008) Signaling from soybean roots to rhizobium: an ATP binding cassette-type transporter mediates genistein secretion. Plant Signal Behav 3:38–40

    Article  PubMed Central  PubMed  Google Scholar 

  • Tian CF, Zhoub YJ, Zhanga YM, Lia QQ, Zhanga YZ, Li DF, Wang S, Wang J, Gilbert LB, Li YR, Chen WX (2012) Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations. Proc Natl Acad Sci U S A 109:8629–8634

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen LH, Miwa H, Nakagawa T, Sandal N, Albrektsen AS, Kawaguchi M, Downie A, Sato S, Tabata S, Kouchi H, Parniske M, Kawasaki S, Stougaard J (2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441:1153–1156

    Article  CAS  PubMed  Google Scholar 

  • van Berkum P, Terefework Z, Paulin L, Suomalainen S, Lindstrom K, Eardly BD (2003) Discordant phylogenies within the rrn loci of rhizobia. J Bacteriol 185:2988–2998

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Hameren B, Hayashi S, Gresshoff PM, Ferguson BJ (2013) Advances in the identification of novel factors required in soybean nodulation, a process critical to sustainable agriculture and food security. J Plant Biol Soil Health 1:6

    Google Scholar 

  • Van Horn L, McCoin M, Kris-Etherton PM, Burke F, Carson JA, Champagne CM, Karmally W, Sikand G (2008) The evidence for dietary prevention and treatment of cardiovascular disease. J Am Diet Assoc 108:287–331

    Article  CAS  PubMed  Google Scholar 

  • Velasquez MT, Bhathena SJ (2007) Role of Dietary Soy Protein in. Obesity Int J Med Sci 4:72–82

    Article  CAS  Google Scholar 

  • Vernie T, Moreau S, de Billy F, Plet J, Combier JP, Rogers C, Oldroyd G, Frugier F, Niebel A, Gamas P (2008) EFD Is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. Plant Cell 20:2696–2713

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vinuesa P, Leon-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Perez-Galdona R, Werner D, Martínez-Romero E (2005b) Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae:Genisteae) growing in the Canary Islands, along with B. japonicum bv. genistearum, Bradyrhizobium genospecies and Bradyrhizobium genospecies. Int J Syst Evol Microbiol 55:569–575

    Article  CAS  Google Scholar 

  • Vinuesa P, Rojas-Jimenez K, Contreas-Moreira B, Mahna SK, Prasad BN, Moe H, Selvaraju SB, Theirfelder H, Werner D (2008) Multilocus sequence analysis for assessment of the biogeography and evolutionary genetics of four Bradyrhizobium species that nodulate soybeans in the Asiatic Continent. Appl Environ Microbiol 74:6987–6996

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vinuesa P, Silva C, Werner D, Martínez-Romero E (2005) Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Phylogenet E 34:29–54

    Article  CAS  Google Scholar 

  • Wang H, Man CX, Wang ET, Chen WX (2009) Diversity of rhizobia and interactions among the host legumes and rhizobial genotypes in an agricultural-forestry ecosystem. Plant Soil 314:169–182

    Article  CAS  Google Scholar 

  • Wang JY, Wang R, Zhang YM, Liu HC, Chen WF, Wang ET, Sui XH, Chen WX (2013) Bradyrhizobium daqingense sp. nov., isolated from soybean nodules. Int J Syst Evol Microbiol 63:616–624

    Article  CAS  PubMed  Google Scholar 

  • Xu D, Abe J, Gai J, Shimamoto Y (2002) Diversity of chloroplast DNA SSRs in wild and cultivated soybeans: evidence for multiple origins of cultivated soybean. Theor Appl Genet 105:645–653

    Article  CAS  PubMed  Google Scholar 

  • Xu LM, Ge C (1984) Physiological-biochemical characteristics and symbiotic responses of the fast-growing Rhizobium japonicum. Soybean Sci 3:102–109

    Google Scholar 

  • Xu ML, Ge C, Cui Z, Li J, Fan H (1995) Bradyhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 45:706–711

    Article  CAS  PubMed  Google Scholar 

  • Yang JK, Zhang WT, Yuan TY, Zhou JC (2006) Genotypic characteristics of the rrn operon and genome of indigenous soybean bradyrhizobia in cropping zones of China. Can J Microbiol 52:968–976

    Article  CAS  PubMed  Google Scholar 

  • Yano K, Yoshida S, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci U S A 105:20540–20545

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yao ZY, Kan FL, Wang ET, Wei GH, Chen WX (2002) Characterization of rhizobia that nodulate legume species of the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov. Int J Syst Evol Microbiol 52:2219–2230

    Article  CAS  PubMed  Google Scholar 

  • Young JM (2003) The genus name Ensifer Casida 1982 takes priority over Sinorhizobium Chen et al 1988, and Sinorhizobium morelense Wang et al. 2002 is a later synonym of Ensifer adhaerens Casida 1982. Is the combination ‘Sinorhizobium adhaerens’ (Casida 1982) Willems et al. 2003 legitimate? Request for an Opinion. Int J Syst Evol Microbiol 53:2107–2110

    Google Scholar 

  • Zhang YF, Wang ET, Tian CF, Wang FQ, Han LL, Chen WF, Chen WX (2008) Bradyrhizobium elkanii, Bradyrhizobium yuanmingense and Bradyrhizobium japonicum are the main rhizobia associated with Vigna unguiculata and Vigna radiata in the subtropical region of China. FEMS Microbiol Lett 285:146–154

    Article  CAS  PubMed  Google Scholar 

  • Zhang YM, Li Y, Chen WF, Wang ET, Tian CF, Li QQ, Zhang YZ, Sui XH, Chen WX (2011) Biodiversity and biogeography of rhizobia associated with soybean plants grown in the North China Plain. Appl Environ Microbiol 77:6331–6342

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang YM, Li Y, Chen WF, Wang ET, Sui XH, Li QQ, Zhang YZ, Zhou YG, Chen WX (2012) Bradyrhizobium huanghuaihaiense sp. nov., an effective symbiotic bacterium isolated from soybean (Glycine max L.) nodules. Int J Syst Evol Microbiol 62:1951–1957

    Article  CAS  PubMed  Google Scholar 

  • Zhao T, Gai J (2004) The origin and evolution of cultivated soybean [Glycine max (L.) Merr.]). Sci Agr Sinica 37:945–962

    Google Scholar 

Download references

Acknowledgment

The first author thanks DBT, Govt. of India for RA fellowship.

Author information

Authors and Affiliations

  1. Division of Microbiology, Indian Agricultural Research Institute, New Delhi, 110012, India

    David L. Biate, Lakkineni Vithal Kumar, D. Ramadoss, Annu Kumari, Satish Naik, Kiran K. Reddy & Kannepalli Annapurna

Authors
  1. David L. Biate
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lakkineni Vithal Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Ramadoss
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Annu Kumari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Satish Naik
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kiran K. Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kannepalli Annapurna
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kannepalli Annapurna .

Editor information

Editors and Affiliations

  1. Dept. of Botany and Microbiology, Gurukul Kangri University, Haridwar (Uttarakhand), India

    Dinesh K. Maheshwari

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Biate, D. et al. (2014). Genetic Diversity of Soybean Root Nodulating Bacteria. In: Maheshwari, D. (eds) Bacterial Diversity in Sustainable Agriculture. Sustainable Development and Biodiversity, vol 1. Springer, Cham. https://doi.org/10.1007/978-3-319-05936-5_5

Download citation

Publish with us

Policies and ethics

Search

Navigation