Polyphasic approach for the characterization of rhizobial symbionts effective in fixing N 2 with common bean (Phaseolus vulgaris L.)

Applied Microbiology and Biotechnology

Volumn 93, Issue 5, 2012, Pages 2035-2049

  Cardoso, Juscélio Donizete ^a,b,c   Hungria, Mariangela ^b   Andrade, Diva S ^c  

^a STATE UNIVERSITY OF LONDRINA   (Brazil)

^b EMBRAPA CERRADOS   (Brazil)

^c INSTITUTO AGRONÔMICO DO PARANÁ   (Brazil)

Author keywords

16S rRNA; Biological nitrogen fixation; BOX PCR; Phaseolus vulgaris; Principal component analysis (PCA); RFLP PCR

Indexed keywords

16S RRNA; BIOLOGICAL NITROGEN FIXATIONS; BOX-PCR; PHASEOLUS VULGARIS; PRINCIPAL COMPONENT ANALYSIS (PCA); RFLP-PCR;

DIAGNOSIS; POLYMERASE CHAIN REACTION; PRINCIPAL COMPONENT ANALYSIS; RNA;

NITROGEN FIXATION;

NITROGEN; RNA 16S;

BIOTECHNOLOGY; LEGUME; NITROGEN FIXATION; NODULATION; POLYMERASE CHAIN REACTION; POLYMORPHISM; PRINCIPAL COMPONENT ANALYSIS; RHIZOBACTERIUM; SYMBIONT;

AGROECOSYSTEM; ARTICLE; BACTERIAL STRAIN; BURKHOLDERIA; CONTROLLED STUDY; ENTEROBACTER; GENOTYPE; GREENHOUSE; HERBASPIRILLUM LUSITANUM; LEIFSONIA XYLI; MORPHOLOGY; NITROGEN FIXATION; NODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PEANUT; PHASEOLUS VULGARIS; PHENOTYPE; PHYLOGENY; PHYSIOLOGY; PLANT GROWTH; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RHIZOBIUM; RHIZOBIUM TROPICI; SEQUENCE ANALYSIS; SOIL; STENOTROPHOMONAS MALTOPHILIA; SYMBIOSIS; VELVET BEAN;

ACTINOMYCETALES; BRAZIL; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; MOLECULAR SEQUENCE DATA; NITROGEN FIXATION; PHASEOLUS; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

ARACHIS HYPOGAEA; BURKHOLDERIA; ENTEROBACTER; HERBASPIRILLUM LUSITANUM; LEIFSONIA XYLI; MUCUNA PRURIENS; PHASEOLUS VULGARIS; RHIZOBIUM TROPICI; STENOTROPHOMONAS MALTOPHILIA;

EID: 84857918998     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3708-2     Document Type: Article

References (53)

1. Aguilar OM, López MV, Riccillo PM, González RA, Pagano M, Grasso DH, Pühler A, Favelukes G (1998) Prevalence of the Rhizobium etli-like allele in genes coding for 16S rRNA among the indigenous rhizobial populations found associated with wild beans from the Southern Andes in Argentina. Appl Environ Microbiol 64:2524-3520
2. Andrade DS, Hamakawa PJ (1994) Estimativa do número de células viáveis de rizóbio no solo e em inoculantes por infecção em plantas. Manual de métodos empregados em estudos de microbiologia agricula EMBRAPA-SPI:63-94
3. Andrade DS, Murphy PJ, Giller KE (2002) The diversity of Phaseolus-nodulation rhizobial populations is altered by liming of acid soils planted with Plaseolus vulgaris L. in Brazil. Appl Environ Microbiol 68(8):4025-4034 (Pubitemid 34836716)
4. Baldani JI, Baldani VLD, Seldin L, Döbereiner J (1986) Characterization of Herbaspirillum seropedicae gen. nov.: a rootassociated nitrogen-fixing bacterium. Int J Syst Bacteriol 36:86-93 (Pubitemid 16181951)
5. Binde DR, Menna P, Bangel EV, Barcellos FG, Hungria M (2009) rep-PCR fingerprinting and taxonomy based on the sequencing of the 16S rRNA gene of 54 elite commercial rhizobial strains. Appl Microbiol Biotechnol 83:897-908
6. Bremner J, Keeney D (1966) Steam distillation methods for determination of ammonium, nitrate and nitrite. Anal Chem Acta 32:482-485
7. Brockwell J, Hely FW, Neal-Smith CA (1966) Some symbiotic characteristics of rhizobia responsible for spontaneous, effective field nodulation of Lotus hispidus. Austr J Exp Agric Anim Husband 6:365-370
8. Caballero-Mellado J, Martinez-Romero E (1999) Soil fertilization limits the genetic diversity of Rhizobium in bean nodules. Symbiosis 26:111-121 (Pubitemid 29103158)
9. Cubo T, Romero F, Vinardell JM, Ruiz-Sainz JE (1997) Expression of the Rhizobium leguminosarum biovar phaseoli melA gene in other rhizobia does not require the presence of the nifA gene. Aust J Plant Physiol 24:195-203
10. Denton M, Kerr KG (1998) Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev 11:57-80 (Pubitemid 28046016)
11. Dôbereiner J (1992) History and new perspectives of diazotrophs in association with non-leguminous plants. Symbiosis 13:1-13
12. Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186-194 (Pubitemid 28177230)
13. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175-185 (Pubitemid 28177229)
14. Fages J, Arsac JF (1991) Sunflower inoculation with Azospirillum and other plant growth promoting rhizobacteria. Plant Soil 137:87-90
15. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791
16. Gagliardi PR, Camargo LEA (2009) Resistência de variedades comerciais de cana-de-açúcar ao agente causal do raquitismoda-soqueira. Cienc Rural 39:1211-1214
17. Geng J, Yuan P, Shao C, Yu S-B, Zhou BZ, Chen X-D (2010) Bacterial melanin interacts with double-stranded DNA with high affinity and may inhibit cell metabolism in vivo. Arch Microbiol 192:321-329
18. Giongo A, Passaglia LMP, Freire JRJ, de Sá ELS (2007) Genetic diversity and symbiotic efficiency of population of rhizobia of Phaseolus vulgaris L. in Brazil. Biol Fert Soils 43:593-598 (Pubitemid 47164054)
19. Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195-202 (Pubitemid 28177231)
20. Graham PH (1981) Some problems of nodulation and symbiotic nitrogen fixation in Phaseolus vulgaris: a review. Field Crops Res 4:93-112
21. Grange L, Hungria M (2004) Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biol Biochem 36:1389-1398 (Pubitemid 38965024)
22. Grange L, Hungria M, Graham PH, Martínez-Romero E (2007) New insights into the origins and evolution of rhizobia that nodulate common bean (Phaseolus vulgaris) in Brazil. Soil Biol Biochem 39(4):867-876 (Pubitemid 46178415)
23. Hauben L, Vauterin L, Moore ERB, Hoste B, Swings J (1999) Genomic diversity of the genus Stenotrophomonas. Int J Syst Bacteriol 49:1749-1760 (Pubitemid 29519107)
24. Hedges SB (1992) The number of replications needed for accurate estimation of the bootstrap p-value in phylogenetic studies. Mol Biol Evol 9:366-369
25. Herridge DF, Peoples MB (1990) Ureide assay for measuring nitrogen fixation by nodulated soybean calibrated by N methods. Plant Physiol 93:495-503 (Pubitemid 120015510)
26. Herridge DF, Bergersen FJ, Peoples MB (1990) Measurement of nitrogen fixation by soybean in the field using the ureide and natural N abundance methods. Plant Physiol 93:708-716 (Pubitemid 120015544)
27. 2fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res 65:151-164
28. Hungria M, Andrade DS, Chueire LMDO, Probanza A, Guttierrez-Mañero FJ, Megías M (2000) Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Soil Biol Biochem 32(11-12):1515-1528
29. Hungria M, Campo RJ, Mendes IC (2003) Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biol Fert Soils 39(2):88-93 (Pubitemid 38047108)
30. James EK (2000) Nitrogen fixation in endophytic and associative symbiosis. Field Crop Res 65(2-3):197-209
31. Jordan DC (1984) Family III. Rhizobiaceae Conn 1938. In: Krieg NR, Holt JG (eds) Bergey's manual of systematic bacteriology. Williams and Wilkins, Baltimore-London, pp 235-244
32. Kaschuk G, Hungria M, Andrade DS, Campo RJ (2006) Genetic diversity of rhizobia associated with common bean (Phaseolus vulgaris L.) grown under no-tillage and conventional systems in Southern Brazil. Appl Soil Ecol 32(2):210-220
33. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150-163
34. Laguerre G, Allard MR, Revoy F, Amarger N (1994) Rapid identification of rhizobia by restriction fragment length polymorphism analysis of PCR-amplified 16S rRNA genes. Appl Environ Microbiol 60:56-63 (Pubitemid 24019918)
35. Martinez-Romero E, Segovia E, Mercante FM, Franco AA, Graham PH, Pardo MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Bacterial 41:417-426
36. Mehnaz S, Kowalik T, Reynolds B, Lazarovits G (2010) Growth promoting effects of corn (Zea mays) bacterial isolates under greenhouse and field conditions. Soil Biol Biochem 42 (10):1848-1856
37. Menna P, Hungria M, Barcellos FG, Bangel EV, Hess PN, Martínez-Romero E (2006) Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Syst Appl Microbiol 29(4):315-332
38. 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 (Pubitemid 28319953)
39. Miyazawa M, Pavan MA, Block MF (1985) Spectrophotometry determination of nitrate in soil extracts without chemical reduction. Pesq Agropec Bras 20:129-133
40. Moawad H, El-Din B, Abdel-Aziz RA (1998) Improvement of biological nitrogen fixation in Egyptian winter legumes through better management of Rhizobium. Plant Soil 204:95-106
41. Mostasso L, Mostasso FL, Dias BG, Vargas MAT, Hungria M (2002) Selection of bean (Phaseolus vulgaris L.) rhizobial strains for the Brazilian cerrados. Field Crop Res 73:121-132 (Pubitemid 34119533)
42. Pavan MA, Bloch MFD, Zempulski HCD, Miyazawa M, Zocoler DC (1992) Manual de análise quimica de solo e controle de qualidade. Instituto Agronomico do Paraná, Londrina
43. Reinhardt ÉL, Ramos PL, Manfio GP, Barbosa HR, Pavan C, Moreira-Filho CA (2008) Molecular characterization of nitrogen-fixing bacteria isolated from Brazilian agricultural plants at São Paulo state. Braz J Microbiol 39:414-422
44. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
45. SAS I (1999) SAS/STAT user's guide. SAS Institute Inc 12: Cary
46. Sneath PHA, Sokal RR (1973) Numerical taxonomy. W H Freeman, San Francisco
47. Stocco P, Santos JCPd, Vargas VP, Hungria M (2008) Avaliação da biodiversidade de rizóbios simbiontes do feijoeiro (Phaseolus vulgaris L.) em Santa Catarina. Rev Bras Cienc Solo (32):1107-1120
48. Teixeira MA, Melo ISd, Vieira RF, Costa FEC, Harakava R (2007) Microrganismos endofíticos de mandioca de áreas comerciais e etnovariedades em três estados brasileiros. Pesq Agropec Bras 42:42-49
49. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-7882
50. Valverde A, Velázquez E, Gutiérrez C, Cervantes E, Ventosa A, Igual JM (2003) Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 53:1979-1983 (Pubitemid 37483861)
51. Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Method Mol Cell Biol 5:25-40 (Pubitemid 24312867)
52. Vincent JM (1970) A manual for the practical study of root-nodule bacteria. Blackwell Scientific, Oxford, IBP handbook, 15
53. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697-703