Skip to main content
Log in

Genetic diversity of rhizobia nodulating common bean (Phaseolus vulgaris L.) in the Central Black Sea Region of Turkey

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

We have analyzed 30 rhizobial isolates obtained from common bean (Phaseolus vulgaris L.) root nodules grown in the Middle Blacksea Region of Turkey, using ARDRA and nucleotide sequence data. ARDRA analysis with enzymes CfoI, HinfI, NdeII, MspI and PstI revealed three patterns. Based on sequence data from 16S rDNA, the patterns were identified as, Rhizobium leguminosarum bv. phaseoli (n = 16), R. etli bv. phaseoli (n = 8) and R. phaseoli (n = 6). On the other hand, nucleotide sequence phylogenies of housekeeping genes (recA, atpD and glnII) selected to confirm the 16S rDNA phylogeny revealed different evolutionary relationships. These results suggested the possibility of lateral transfers of these genes amongst different rhizobial species (including R. leguminosarum, R. etli and R. phaseoli) sharing the same ecological niche (nodulating P. vulgaris) which also indicates that there may be no true genetic barier among these species. Phylogenetic analysis based on DNA sequence data from the nodA and nifH genes showed that all rhizobial species obtained in this study were carrying nodA and nifH haplotypes which were the same or similar to those of CFN42 (R. etli type strain), suggesting a further support for the lateral transfer of CFN42 Sym plasmid, p42, amongst Turkish common bean nodulating rhizobial isolates.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abril A, Zurdo-Pineiro J-L, Peix A, Rivas R, Velazquez E (2007) Solubilization of phosphate by a strain of Rhizobium leguminosarum bv. trifolii isolated from Phaseolus vulgaris in El Chaco Arido soil (Argentina). First International Meeting on Microbial Phosphate Solubilization. Dev Plant Soil Sci 102:135–138. doi:10.1007/978-1-4020-5765-6_19

    Article  Google Scholar 

  • Aguilar OM, Riva O, Peltzer E (2004) Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc Natl Acad Sci USA 101(37):13548–13553. doi:10.1073/pnas.0405321101

    Article  PubMed  CAS  Google Scholar 

  • Akaike H (1974) A new look at statistical model identification. IEEE T Automat Contr 19:716–723. doi:10.1109/TAC.1974.1100705

    Article  Google Scholar 

  • Amarger N, Macheret V, Laguerre G (1997) Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int J Syst Bacteriol 47:996–1006. doi:10.1099/00207713-47-4-996

    Article  PubMed  CAS  Google Scholar 

  • Anyango B, Wilson KJ, Beynon JL, Giller KE (1995) Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. Appl Environ Microbiol 61(11):4016–4021

    PubMed  CAS  Google Scholar 

  • Aserse AA, Rasanen LA, Assefa F, Hailemariam A, Lindstrom K (2012) Phylogeny and genetic diversity of native rhizobia nodulating common bean (Phaseolus vulgaris L.) in Ethiopia. Syst Appl Microbiol 35(2):120–131. doi:10.1016/j.syapm.2011.11.005

    Article  PubMed  Google Scholar 

  • Beebe SE, Skroch PW, Tohme J, Duque MC, Pedraza F, Nienhuis J (2000) Structure of genetic diversity among common bean landraces of Middle American origin based on correspondence analysis of RAPD. Crop Sci 40:264–273. doi:10.2135/cropsci2000.401264x

    Article  Google Scholar 

  • Beebe S, Rengifo J, Gaitan E, Duque MC, Tohme J (2001) Diversity and origin of Andean landraces of common bean. Crop Sci 41:854–862. doi:10.2135/cropsci2001.413854x

    Article  Google Scholar 

  • Beyene D, Kassa S, Ampy F, Asseffa A, Gebremedhin T, Van Berkum P (2004) Ethiopian soils harbor natural populations of rhizobia that form symbioses with common bean (Phaseolus vulgaris L.). Arch Microbiol 181:129–136. doi:10.1007/s00203-003-0636-2

    Article  PubMed  CAS  Google Scholar 

  • Buttery BR, Park S, Van Berkum P (1997) Effects of common bean (Phaseolus vulgaris L.) cultivar and Rhizobium strain on plant growth, seed yield and nitrogen content. Can J Plant Sci 77:347–351

    Article  Google Scholar 

  • Chacon MI, Pickersgill B, Debouck DG (2005) Domectication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Masoamerican and Andean cultivated races. Theor Appl Genet 110:432–444. doi:10.1007/s00122-004-1842-2

    Article  CAS  Google Scholar 

  • Chen WX, Tan ZY, Gao JL, Li Y, Wang ET (1997) Rhizobium hainanense sp. nov., isolated from tropical legumes. Int J Syst Bacteriol 47(3):870–873. doi:10.1099/00207713-47-3-870

    Article  PubMed  CAS  Google Scholar 

  • Debelle F, Plazanet C, Roche P, Pujol C, Savagnac A, Rosenberg C, Prome JC, Denarie J (1996) The NodA proteins of Rhizobium meliloti and Rhizobium tropici specify the N-acylation of Nod factors by different fatty acids. Mol Microbiol 22(2):303–314. doi:10.1046/j.1365-2958.1996.00069.x

    Article  PubMed  CAS  Google Scholar 

  • Diouf A, de Lajudie P, Neyra M, Kersters K, Gillis M, Martinez-Romero E, Gueye M (2000) Polyphasic characterization of rhizobia that nodulate Phaseolus vulgaris in West Africa (Senegal and Gambia). Int J Syst Evol Micr 50:159–170

    Article  CAS  Google Scholar 

  • Ditta G, Virts E, Palomares A, Kim CH (1987) The nifA gene of Rhizobium meliloti is oxygen regulated. J Bacteriol 169(7):3217–3223

    PubMed  CAS  Google Scholar 

  • Dobert RC, Breil BT, Triplett EW (1994) DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationship to those of other nodulating bacteria. Mol Plant Microbe Interact 7:564–572

    Article  PubMed  CAS  Google Scholar 

  • Eardly BD, Young JP, Selander RK (1992) Phylogenetic position of Rhizobium sp. strain Or 191, a symbiont of both Medicago sativa and Phaseolus vulgaris, based on partial sequences of the 16S rRNA and nifH genes. Appl Environ Microbiol 58(6):1809–1815

    PubMed  CAS  Google Scholar 

  • Eck RV, Dayhoff MO (1966) In: Dayhoff MO (ed) Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver Spring

    Google Scholar 

  • Efron B (1982) The Jackknife, the bootstrap and other resampling plans. CBMS-NSF Regional Conference Series in applied mathematics, monograph 38. SIAM, Philadelphia

    Book  Google Scholar 

  • Eisen JA (1995) The RecA protein as a model molecule for molecular systematic studies of bacteria: comparison of trees of RecAs and 16S rRNAs from the same species. J Mol Evol 41:1105–1123. doi:10.1007/BF00173192

    Article  PubMed  CAS  Google Scholar 

  • Elliott GN, Chou JH, Chen WM, Bloemberg GV, Bontemps C, Martinez-Romero E, Velazquez E, Young JP, Sprent JI, James EK (2009) Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol 11(4):762–778. doi:10.1111/j.1462-2920.2008.01799.x

    Article  PubMed  Google Scholar 

  • Farris JS, Kallersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319. doi:10.1111/j.1096-0031.1994.tb00181.x

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fitch W (1977) On the problem of discovering the most parsimonious tree. Am Nat 111:223–257

    Article  Google Scholar 

  • Fred EB, Baldwin IL, McCoy E (1932) Root nodule bacteria and leguminous plants. University of Wisconsin, Madison

    Google Scholar 

  • Fuhrmann M, Hennecke H (1984) Rhizobium japonicum nitrogenase Fe protein gene (nifH). J Bacteriol 158(3):1005–1011

    PubMed  CAS  Google Scholar 

  • Gaunt MW, Turner SL, Rigotier-Gois L, Lloyd-Macgilp SA, Young JPW (2001) Phylogenies of atpD and recA support the small subunit rRNA-based classification of Rhizobia. Int J Syst Evol Micr 51:2037–2048

    Article  CAS  Google Scholar 

  • Gepts P (1990) Biochemical evidence bearing on the domestication of Phaseolus (Fabaceace) beans. Econ Bot 44(3):28–38. doi:10.1007/BF02860473

    Article  Google Scholar 

  • Gepts P, Bliss FA (1988) Dissemination pathways of common bean (Phaseolus vulgaris) deduced from phaseolin electrophoretic variability. 2. Europe and Africa. Econ Bot 42:86–104. doi:10.1007/BF02859038

    Article  Google Scholar 

  • Gepts P, Osborn TC, Rashka K, Bliss FA (1986) Phaseolin-protein variability in wild forms and landraces of the common bean (Phaseolus vulgaris): evidence for multiple centers of domestication. Econ Bot 40(4):451–468. doi:10.1007/BF02859659

    Article  CAS  Google Scholar 

  • Gepts P, Osborn TC, Rashka K, Bliss FA (1990) Phaseolin-protein variability in wild forms and landraces of the common bean (Phaseolus vulgaris): evidence for multiple centers of domestication. Econ Bot 40(4):451–468. doi:10.1007/BF02859659

    Article  Google Scholar 

  • Gonzalez V, Bustos P, Ramirez-Romero MA, Medrano-Soto A, Salgado H, Hernandez-Gonzalez I, Hernandez-Celis JC, Quintero V, Moreno-Hagelsieb G, Girard L, Rodriguez O, Flores M, Cevallos MA, Collado-Vides J, Romero D, Davila G (2003) The mosaic structure of the symbiotic plasmid of Rhizobium etli CFN42 and its relation to other symbiotic genome compartments. Genome Biol 4(6):R36. doi:10.1186/gb-2003-4-6-r36

    Article  PubMed  Google Scholar 

  • Gonzalez V, Santamaria RI, Bustos P, Hernandez-Gonzalez I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ramirez MA, Jimenez-Jacinto V, Collado-Vides J, Davila G (2006) The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci USA 103(10):3834–3839. doi:10.1073/pnas.0508502103

    Article  PubMed  Google Scholar 

  • Grange L, Hungria M (2004) Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biol Biochem 36:1389–1398. doi:10.1016/j.soilbio.2004.03.005

    Article  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum-likelihood. Syst Biol 52(5):696–704. doi:10.1080/10635150390235520

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Haukka K, Lindstrom K, Young JPW (1998) Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. Appl Environ Microb 64(2):419–426

    CAS  Google Scholar 

  • Hennecke H, Kaluza K, Thöny B, Fuhrmann M, Ludwig W, Stackebrandt (1985) Concurrent evolution of nitrogenase genes and 16S rRNA in Rhizobium species and other nitrogen fixing bacteria. Arch Microbiol 142:342–348. doi:10.1007/BF00491901

    Article  CAS  Google Scholar 

  • Herrera-Cervera JA, Caballero-Mellado J, Laguerre G, Tichy HV, Requena N, Amarger N, Martinez-Romero E, Olivares J, Sanjuan J (1999) At least five Rhizobial species nodulate Phaseolus vulgaris in a Spanish soil. FEMS Microbiol Ecol 30:87–97. doi:10.1111/j.1574-6941.1999.tb00638.x

    Article  CAS  Google Scholar 

  • Jordan DC (1984) Family III. Rhizobiaceae. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol. I. Williams & Wilkins, Baltimore

    Google Scholar 

  • Küçük Ç, Kıvanç M, Kınacı E (2006) Characterization of Rhizobium sp. isolated from Bean. Turk J Biol 30:127–132

    Google Scholar 

  • Kuykendall LD, Young JM, Martinez-Romero E, Kerr A, Sawada H (2005) Genus I. Rhizobium. In: Garrity GM (ed) Bergey’s manual of systematic bacteriology, part C the alpha-, beta-, delta-, and epsilon proteobacteria. Springer, New York

    Google Scholar 

  • Laguerre G, Fernandez MP, Edel V, Normand P, Amarger N (1993) Genomic heterogenecity among French Rhizobium strains ısolates from Phaseolus vulgaris L. Int J Syst Bacteriol 43(4):761–767. doi:10.1099/00207713-43-4-761

    Article  PubMed  CAS  Google Scholar 

  • Laguerre G, Allard M, Revoy F, Amarger N (1994) Rapid ıdentification of rhizobia by restriction fragment lenght polymorphism analysis of PCR-amplified 16S rRNA genes. Appl Environ Microb 60(1):56–63

    CAS  Google Scholar 

  • Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147:981–993

    PubMed  CAS  Google Scholar 

  • Laranjo M, Alexandre A, Rivas R, Velazquez E, Young JP, Liveira S (2008) Chickpea rhizobia symbiosis genes are highly conserved across multiple Mesorhizobium species. FEMS Microbiol Ecol 66:391–400. doi:10.1111/j.1574-6941.2008.00584.x

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Lopez A, Rogel MA, Ormeno-Orrillo E, Martinez-Romero J, Martinez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. Nov Syst Appl Microbiol 33(6):322–327. doi::10.1016/j.soilbio.2003.10.025

    Article  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(1):200–214. doi:10.1099/ijs.0.65392-0

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Romero E (2003) Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 252:11–23. doi:10.1023/A:1024199013926

    Article  CAS  Google Scholar 

  • Martinez-Romero E, Segovia L, Mercante FM, Franco AA, Graham P, Pardo MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Bacteriol 41:417–426. doi:10.1099/00207713-41-3-417

    Article  PubMed  CAS  Google Scholar 

  • Mhamdi R, Jebara M, Aouani ME, Ghrir R, Mars M (1999) Genotypic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in Tunusian soils. Biol Fert Soils 28:313–320. doi:10.1007/s003740050499

    Article  Google Scholar 

  • Mhamdi R, Laguerre G, Aouani ME, Mars M, Amarger N (2002) Different species and symbiotic genotypes of field rhizobia can nodulate Phaseolus vulgaris in Tunisian soils. FEMS Microbiol Ecol 41:77–84. doi:10.1111/j.1574-6941.2002.tb00968.x

    Article  PubMed  CAS  Google Scholar 

  • Michiels J, Dombrecht B, Vermeiren N, Xi C, Luyten E, Vanderleyden J (1998) Phaseolus vulgaris is a non-selective host for nodulation. FEMS Microbiol Ecol 26:193–205. doi:10.1111/j.1574-6941.2002.tb00968.x

    Article  CAS  Google Scholar 

  • Mnasri B, Badri Y, Saidi S, de Lajudie P, Mhamdi R (2009) Symbiotic diversity of Ensifer meliloti strains recovered from various legume species in Tunisia. Syst Appl Microbiol 32(8):583–592. doi:10.1016/j.syapm.2009.07.007

    Article  PubMed  CAS  Google Scholar 

  • Perez-Ramirez NO, Rogel MO, Wang E, Castellanos JZ, Martinez-Romero E (1998) Seed of Phaseolus vulgris bean carry Rhizobium etli. FEMS Microbiol Ecol 26:289–296. doi:10.1111/j.1574-6941.1998.tb00513.x

    Article  CAS  Google Scholar 

  • Pollack RA, Findlay L, Mondschein W, Modesto RR (2002) Laboratory exercises in microbiology. Wiley, New York,

    Google Scholar 

  • Posada D (2008) jModel test: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. doi:10.1093/molbev/msn083

    Article  PubMed  CAS  Google Scholar 

  • Ramirez-Bahena MH, Garcia-Fraile P, Peix A, Valverde A, Rivas R, Igual JM, Mateos PF, Martinez-Molina E, Velazquez E (2008) Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889AL, Rhizobium phaseoli Dangeard 1926AL and Rhizobium trifolii Dangeard 1926AL. R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 (=NCIMB 11478) as Rhizobium pisi sp. nov. Int J Syst Evol Micr 58:2484–2490. doi:10.1099/ijs.0.65621-0

    Article  CAS  Google Scholar 

  • Ramirez-Romero MA, Bustos P, Girard L, Rodriguez O, Cevallos MA, Davila G (1997) Sequence, localization and characteristics of the replicator region of the symbiotic plasmid of Rhizobium etli. Microbiology 143:2825–2831. doi:10.1099/00221287-143-8-2825

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro RA, Barcellos FG, Thompson FL, Hungria M (2009) Multilocus sequence analysis of Brazilian Rhizobium microsymbionts of common bean (Phaseolus vulgaris L.) reveals unexpected taxonomic diversity. Res Microbiol 160(4):297–306. doi:10.1016/j.resmic.2009.03.009

    Article  PubMed  CAS  Google Scholar 

  • Robledo M, Velazquez E, Ramirez-Bahena MH, Garcia-Fraile P, Perez-Alonso A, Rivas R, Martinez-Molina E, Mateos PF (2011) The celC gene, a new phylogenetic marker useful for taxonomic studies in Rhizobium. Syst Appl Microbiol 34:393–399. doi:10.1016/j.syapm.2011.01.010

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    PubMed  CAS  Google Scholar 

  • Santillana N, Ramirez-Bahena MH, Garcia-Fraile P, Velazquez E, Zuniga D (2008) Phylogenetic diversity based on rrs, atpD, recA genes and 16S-23S intergenic sequence analyses of rhizobial strains isolated from Vicia faba and Pisum sativum in Peru. Arch Microbiol 189(3):239–247. doi:10.1007/s00203-007-0313-y

    Article  PubMed  CAS  Google Scholar 

  • Sawada H, Ieki H, Oyaizu H, Matsumoto S (1993) Proposal for rejection of Agrobacterium tumefaciens and revised descriptions for the genus Agrobacterium and for Agrobacterium radiobacter and Agrobacterium rhizogenes. Int J Syst Bacteriol 43(4):694–702. doi:10.1099/00207713-43-4-694

    Article  PubMed  CAS  Google Scholar 

  • Scott KF, Rolfe BG, Shine J (1983) Biological nitrogen fixation: primary structure of the Rhizobium trifolii iron protein gene. DNA 2(2):149–155. doi:10.1089/dna.1983.2.149

    Article  PubMed  CAS  Google Scholar 

  • Segovia L, Young JPW, Martinez-Romero E (1993) Reclassification of American Rhizobium leguminosarum Bivar Phaseoli type I strains as R. etli sp. nov. Int J Syst Evol Micr 43(2):374–377. doi:10.1099/00207713-43-2-374

    CAS  Google Scholar 

  • Şehirali S (1988) Yemeklik Dane Baklagiller. Ankara Üniversitesi Ziraat Fakültesi Yayınları, Ankara, Türkiye

    Google Scholar 

  • Sessitsch A, Hardarson G, Akkermans ADL, De Vos WM (1997) Characterization of Rhizobium etli and other Rhizobium spp. that nodulate Phaseolus vulgaris L. in an Austrian soil. Mol Ecol 6:601–608. doi:10.1046/j.1365-294X.1997.00223.x

    Article  CAS  Google Scholar 

  • Shamseldin A, Werner D (2007) Presence of Rhizobium etli bv. phaseoli and Rhizobium gallicum bv. gallicum in Egyptian soils. World J Microb Biot 23:285–289. doi:10.1007/s11274-006-9204-7

    Article  Google Scholar 

  • Silva C, Vinuesa P, Eguiarte LE, Martinez-Romero E, Souza V (2003) Rhizobium etli and Rhizobium gallicum nodulate common bean (Phaseolus vulgaris) in a traditionally managed Milpa Plot in Mexico: population genetics and biogeographic ımplications. Appl Environ Microb 69(2):884–893. doi:10.1128/AEM.69.2.884-893.2003

    Article  CAS  Google Scholar 

  • Silva C, Vinuesa P, Eguiarte LE, Souza V, Martinez-Romero E (2005) Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. Mol Ecol 14(13):4033–4050. doi:10.1111/j.1365-294X.2005.02721.x

    Article  PubMed  CAS  Google Scholar 

  • Singh SP, Gepts P, Debouck DG (1991a) Races of common bean (Phaseolus vulgaris, Fabaceae). Econ Bot 45(3):379–396. doi:10.1007/BF02887079

    Article  Google Scholar 

  • Singh SP, Gutierrez JA, Molina A, Urrea C, Gepts P (1991b) Genetic diversity in cultivated common bean. II. Marker-based analysis of morphological and agronomic traits. Crop Sci 31:23–29

    Article  CAS  Google Scholar 

  • Singh SP, Nodari R, Gepts P (1991c) Genetic diversity in cultivated common bean: I. Allozymes. Crop Sci 31:19–23

    Article  CAS  Google Scholar 

  • Singh RK, Mishra RP, Jaiswal HK, Kumar V, Pandey SP, Rao SB, Annapurna K (2006) Isolation and identification of natural endophytic rhizobia from rice (Oryza sativa L.) through rDNA PCR-RFLP and sequence analysis. Curr Microbiol 52(2):117–122. doi:10.1007/s00284-005-0138-3

    Article  PubMed  CAS  Google Scholar 

  • Somasegaran P, Hoben HJ (1985) Methods in legume-rhizobium technology. USAID, USA

    Google Scholar 

  • Squartini A, Struffi P, Doring H, Selenska-Pobell S, Tola E, Giacomini A, Vendramin E, Velazquez E, Mateos PF, Martinez-Molina E, Dazzo FB, Casella S, Nuti MP (2002) Rhizobium sullae sp. nov. (formerly ‘Rhizobium hedysari’), the root-nodule microsymbiont of Hedysarum coronarium L. Int J Syst Evol Microbiol 52:1267–1276. doi:10.1099/ijs.0.01821-0 IJSEM IJSEM

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JT, Eardy BD, Van Berkum P, Ronson CW (1996) Four unnamed species of nonsymbiotic rhizobia isolated from the rhizosphere of Lotus corniculatus. Appl Environ Microb 62:2818–2825

    CAS  Google Scholar 

  • Swofford DL (1998) PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4 beta 10. Sinauer, Sunderland

    Google Scholar 

  • Tamimi SM, Young JPW (2004) Rhizobium etli is the dominant common bean nodulating rhizobia in cultivated soils from different locations in Jordan. Appl Soil Ecol 26:193–200. doi:10.1016/j.apsoil.2004.01.003

    Article  Google Scholar 

  • Tan ZY, Kan FL, Peng GX, Wang ET, Reinhold-Hurek B, Chen WX (2001) Rhizobium yanglingense sp. nov., isolated from arid and semi aridregions in China. Int J Syst Evol Microbiol 51(PT 3):909–914

    Article  PubMed  CAS  Google Scholar 

  • Temizkan G, Arda N (2004) Moleküler Biyolojide Kullanılan Yöntemler. Nobel Tıp Kitabevleri, İstanbul

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX-Windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:10.1093/nar/25.24.4876

    Article  PubMed  CAS  Google Scholar 

  • Tian CF, Wang ET, Han TX, Sui XH, Chen WX (2007) Genetic diversity of rhizobia associated with Vicia faba in three ecological regions of China. Arch Microbiol 188:273–282. doi:10.1007/s00203-007-0245-6

    Article  PubMed  CAS  Google Scholar 

  • Tian CF, Wang ET, Wu LJ, Han TX, Chen WF, Gu CT, Gu JG, Chen WX (2008) Rhizobium fabae sp. nov., a bacterium that nodulates Vicia faba. Int J Syst Evol Microbiol 58(PT 12):2871–2875. doi:10.1099/ijs.0.2008/000703-0

    Article  PubMed  CAS  Google Scholar 

  • Tian CF, Young JPW, Wang ET, Tamimi SM, Chen WX (2010) Population mixing of Rhizobium leguminosarum bv. viciae nodulating Vicia faba: the role of recombination and lateral transfer. FEMS Microbiol Ecol 1–14. doi:10.1111/j.1574-6941.2010.00909.x

  • Turner SL, Young JP (2000) The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17(2):309–319

    Article  PubMed  CAS  Google Scholar 

  • Valverde A, Igual JM, Peix A, Cervantes E, Velazquez E (2006) Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int J Syst Evol Micr 56:2631–2637. doi:10.1099/ijs.0.64402-0

    Article  CAS  Google Scholar 

  • Valverde A, Velázquez E, Cervantes E, Igual JM, van Berkum P (2011) Evidence for an American origin of the genes for symbiosis in Rhizobium lusitanum. Appl Environ Microbiol 77(16):5665–5679. doi:10.1128/AEM.02017-10

    Article  PubMed  CAS  Google Scholar 

  • Van Berkum P, Beyene D, Eardly BD (1996) Phylogenetic relationships among Rhizobium species nodulating the common bean (Phaseolus vulgaris L.). Int J Syst Bacteriol 46(1):240–244. doi:10.1099/00207713-46-1-240

    Article  PubMed  Google Scholar 

  • Van Berkum P, Beyene D, Bao G, Campbell TA, Eardly BD (1998) Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica [(L.) Ledebour]. Int J Syst Bacteriol 48(Pt 1):13–22. doi:10.1099/00207713-48-1-13

    Article  PubMed  Google Scholar 

  • Vazquez M, Davalos A, De Las Penas A, Sanchez F, Quinto C (1991) Novel organization of the common nodulation genes in Rhizobium leguminosarum bv. phaseoli strains. J Bacteriol 173(3):1250–1258

    PubMed  CAS  Google Scholar 

  • Vincent JM (1970) A manuel for the practical study of the root-nodule bacteria. Blackwell, Oxford

    Google Scholar 

  • Vinuesa P, Silva C, Werner D, Martinez-Romero E (2005a) Population genetics and phylogenetic ınference in bacterial molecular systematics: the roles of migration and recombination in bradyrhizobium species cohesion and delineation. Mol Phyl Evol 34:29–54. doi:10.1016/j.ympev.2004.08.020

    Article  CAS  Google Scholar 

  • Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral ML, Bedmar EJ, Martinez-Romero E (2005b) Molecular systematics of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs, atpD, recA and nifH sequences, and their use in the classification of Sesbania microsymbionts from Venezuelan wetlands. Syst Appl Microbiol 28(8):702–716. doi:10.1016/j.syapm.2005.05.007

    Article  PubMed  CAS  Google Scholar 

  • Wang ET, Van Berkum P, Beyene D, Sui XH, Dorado O, Chen WX, Martinez-Romero E (1998) Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae. Int J Syst Bacteriol 48(Pt 3):687–699. doi:10.1099/00207713-48-3-687

    Article  PubMed  CAS  Google Scholar 

  • Wang ET, Rogel MA, Garcia-delos Santos A, Martinez-Romero J, Cevallos MA, Martinez-Romero E (1999) Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int J Syst Bacteriol 49(Pt 4):1479–1491. doi:10.1099/00207713-49-4-1479

    Article  PubMed  CAS  Google Scholar 

  • Wei GH, Wang ET, Tan ZY, Zhu ME, Chen WX (2002) Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int J Syst Evol Microbiol 52(PT 6):2231–2239. doi:10.1099/ijs.0.02030-0

    Article  PubMed  CAS  Google Scholar 

  • Wei GH, Tan ZY, Zhu ME, Wang ET, Han SZ, Chen WX (2003) Characterization of rhizobia isolated from legume species within the genera Astragalus and Lespedeza grown in the Loess Plateau of China and description of Rhizobium loessense sp. nov. Int J Syst Evol Microbiol 53:1575–1583. doi:10.1099/ijs.0.02031-0

    Article  PubMed  CAS  Google Scholar 

  • Weir B (2006) Systematics, specificity, and ecology of New Zealand Rhizobia. PhD thesis, The University of of Auckland, New Zealand

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S Ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed  CAS  Google Scholar 

  • Willems A, Collins MD (1993) Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequences. Int J Syst Bacteriol 43(2):305–313. doi:10.1099/00207713-43-2-305

    Article  PubMed  CAS  Google Scholar 

  • Young JP, Crossman LC, Johnston AW, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson AR, Todd JD, Poole PS, Mauchline TH, East AK, Quail MA, Churcher C, Arrowsmith C, Cherevach I, Chillingworth T, Clarke K, Cronin A, Davis P, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Sanders M, Simmonds M, Whitehead S, Parkhill J (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7(4):R34. doi:10.1186/gb-2006-7-4-r34

    Article  PubMed  CAS  Google Scholar 

  • Zhang XX, Guo XW, Terefework Z, Paulin L, Cao YZ, Hu FR, Lindstrom K, Li FD (1999) Genetic diversity among rhizobial isolates from field-grown Astragalus sinicus of Southern China. Syst Appl Microbiol 22:312–320

    Article  Google Scholar 

  • Zhang XX, Turner SL, Guo XW, Yang HJ, Debelle F, Yang GP, De Narie J, Young JPW, Li FD (2000) The common nodulation genes of Astragalus sinicus Rhizobia are conserved despite chromosomal diversity. Appl Environ Microb 66(7):2988–2995

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are gratefully acknowledge J.P.W. Young from University of York for critical reading of the manuscript. We would also like to thank Dr. Erkut PEKŞEN from Ondokuz Mayis University for his valuable advice. This study was supported by a grant from the Ondokuz Mayis University Research Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cem Tolga Gurkanli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gurkanli, C.T., Ozkoc, I. & Gunduz, I. Genetic diversity of rhizobia nodulating common bean (Phaseolus vulgaris L.) in the Central Black Sea Region of Turkey. Ann Microbiol 63, 971–987 (2013). https://doi.org/10.1007/s13213-012-0551-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-012-0551-3

Keywords

Navigation