Diversity and plant growth promoting evaluation abilities of bacteria isolated from sugarcane cultivated in the South of Brazil

Applied Soil Ecology

Volumn 63, Issue , 2013, Pages 94-104

  Beneduzi, Anelise ^a   Moreira, Fernanda ^b   Costa, Pedro B ^b   Vargas, Luciano K ^a   Lisboa, Bruno B ^a   Favreto, Rodrigo ^a   Baldani, José Ivo ^c   Passaglia, Luciane Maria P ^b  

^a Fundacao Estadual de Pesquisa Agropecuaria   (Brazil)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^c EMBRAPA AGROBIOLOGIA   (Brazil)

Author keywords

Nitrogen Fixation; PCR RFLP; Plant Growth Promoting Bacteria (PGPB); Sugarcane

Indexed keywords

ACHROMOBACTER; AGROBACTERIUM; BACTERIA (MICROORGANISMS); BURKHOLDERIA; GLUCONACETOBACTER; GLUCONACETOBACTER DIAZOTROPHICUS; RHIZOBIUM; STENOTROPHOMONAS;

EID: 84871098501     PISSN: 09291393     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.apsoil.2012.08.010     Document Type: Article

References (93)

1. Ali B., Sabri A.N., Jung L.K., Hasnain S. Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum L. Lett. Appl. Microbiol. 2009, 48:542-547.
2. Ait Barka E., Nowak J., Clement C. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl. Environ. Microbiol. 2006, 72:7246-7252.
3. Ambrosini A., Beneduzi A., Stefanski T., Pinheiro F.G., Vargas L.K., Passaglia L.M.P. Screening of plant growth promoting rhizobacteria isolated from sunflower (Helianthus annuus L.). Plant Soil 2011, 356:245-264.
4. Antoun H., Beauchamp C.J., Goussard N., Chabot R., Lalande R. Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L). Plant Soil 1998, 204:57-68.
5. Arshad M., Frankenberger W.T. Microbial production of plant growth regulators. Soil Microbial Ecology 1993, 307-347. Marcel and Dekker, Inc., New York. F. Blaine, Metting (Eds.).
6. Baldani J.I., Baldani V.L.D. History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An. Acad. Bras. Cienc. 2005, 77:549-579.
7. Baldani J.I., Caruso L., Baldani V.L.D., Goi S.R., Döbereiner J. Recent advances in BNF with non-legume plants. Soil Biol. Biochem. 1997, 29:911-922.
8. Barrett C.F., Parker M.A. Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl. Environ. Microbiol. 2006, 72:1198-1206.
9. Bashan Y., Puente M.E., Rodriguez-Mendoza M.N., Toledo G., Holguin G., Ferrera-Cerrato R., Pedrin S. Survival of Azospirillum brasilense in the bulk soil and rhizosphere of 23 soil types. Appl. Environ. Microbiol. 1995, 61:1938-1945.
10. Bashan Y., Holguin G., Lifshitz R. Isolation and characterization of plant growth-promoting rhizobacteria. Methods in Plant Molecular Biology and Biotechnology Isolation and Characterization of Plant Growth-Promoting Rhizobacteria 1993, 331-334. CRC Press Inc., Boca Raton, FL. C.M. Bourne (Ed.).
11. Beattie G.A. Plant-associated bacteria: survey, molecular phylogeny, genomics and recent advances. Plant-Associated Bacteria 2006, 1-56. Springer, the Netherlands. S.S. Gnanamanickam (Ed.).
12. Beneduzi A., Peres D., Vargas L.K., Bodanese-Zanettini M.H., Passaglia L.M.P. Evaluation of genetic diversity and plant growth promoting activities of nitrogen-fixing bacilli isolated from rice fields in South Brazil. Appl. Soil. Ecol. 2008, 39:311-320.
13. Beneduzi A., Costa P.B., Parma M., Melo I.S., Bodanese-Zanettini M.H., Passaglia L.M.P. Paenibacillus riograndensis sp. nov., a nitrogen-fixing species isolated from the rhizosphere of Triticum aestivum. Int. J. Syst. Evol. Microbiol. 2010, 60:128-133.
14. Berg G., Krechel A., Ditz M., Faupel A., Ulrich A., Hallmann J. Comparison of endophytic and ectophytic potato associated bacterial communities and their antagonistic activity against plant pathogenic fungi. FEMS Microbiol. Ecol. 2005, 51:215-229.
15. Bevivino A., Sarrocco S., Dalmastri C., Tabacchioni S., Cantale C., Chiarini L. Characterization of a free-living maize rhizosphere population of Burkholderia cepacia: effect of seed treatment on disease suppression and growth promotion of maize. FEMS Microbiol. Ecol. 1998, 27:225-237.
16. Blackburn F. Sugarcane 1984, Longman, New York.
17. Boddey R.M. Methods for quantification of nitrogen fixation associated with gramineae. Crit. Rev. Plant Sci. 1987, 6:209-266.
18. Boddey R.M. Biological nitrogen fixation in sugarcane: a key to energetically viable bio-fuel production. CRC Crit. Rev. Plant Sci. 1995, 14:263-279.
19. Boddey R.M., Urquiaga S., Alves B.J.R., Reis V. Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 2003, 252:139-149.
20. Borges L.G.D., Dalla Vechia V., Corção G. Characterization and genetic diversity via REP-PCR of Escherichia coli isolates from polluted waters in southern Brazil. FEMS Microbiol. Ecol. 2003, 45:173-180.
21. Brockwell J., Pilka A., Holliday R.A. Soil pH is a major determinant of the numbers of naturally occurring Rhizobium meliloti in non-cultivated soils of New South Wales. Aust. J. Exp. Agric 1991, 31:211-219.
22. Burris R.H. Nitrogen fixation assay methods and techniques. Methods Enzymol. 1972, 24:415-431.
23. Çakmakçi R., Dönmez F., Aydi{dotless}n A., şahin F. Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol. Biochem. 2006, 38:1482-1487.
24. Caballero-Mellado J., Onofre-Lemus J., Estrada-de los Santos P., Martinez-Aguilar L. The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl. Environ. Microbiol. 2007, 73:5308-5319.
25. Chowdhury S.P., Schmid M., Hartmann A., Tripathi A.K. Identification of diazotrophs in the culturable bacterial community associated with roots of Lasiarus sindicus, a perennial grass of Thar desert, India. Microb. Ecol. 2007, 54:82-90.
26. Coenye T., Vandamme P. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ. Microbiol. 2003, 5:719-729.
27. Compant S., Duffy B., Nowak J., Clement C., Ait Barka E. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action and future prospects. Appl. Environ. Microbiol. 2005, 71:4951-4959.
28. Copping L.G., Menn J.J. Biopesticides: a review of their action, applications and efficacy. Pest Manag. Sci. 2000, 56:651-676.
29. Costacurta A., Vanderleyden J. Synthesis of phytohormones by plant associated bacteria. Crit. Rev. Microbiol. 1995, 21:1-18.
30. Cruz L.M., Souza E.M., Weber O.B., Baldani J.I., Döbereiner J., Pedrosa F. 16S ribosomal DNA characterization of nitrogen-fixing bacteria isolated from banana (Musa spp.) and pineapple (Ananas comosus L. Merril). Appl. Environ. Microbiol. 2001, 67:2375-2379.
31. de Freitas J.R., Banerjee M.R., Germida J.J. Phosphate solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol. Fertil. Soils 1997, 24:358-364.
32. Dean D.R., Jacobson M.R. Biochemical genetics of nitrogenase. Biological Nitrogen Fixation 1992, 763-834. Chapman & Hall, New York. G. Stacey, R.H. Burris, H.J. Evans (Eds.).
33. Dias L.A.S. Análises multidimensionais. Eletroforese de Isoenzimas e Proteínas Afins: Fundamentos e Aplicações em Plantas e Microrganismos 1998, 405-473. UFV, Viçosa. A.C. Alfenas (Ed.).
34. Döbereiner J. Isolation and identification of root associated diazotrophs. Plant Soil 1988, 110(2):207-212.
35. Döbereiner J. History and new perspectives of diazotrophs in association with non-leguminous plants. Symbiosis 1992, 13:1-13.
36. Döbereiner J., Baldani V.L.D., Reis V.M. Endophytic occurrence of diazotrophic bacteria in non-leguminous crops. Azospirillum VI and Related Microorganisms. 1995, Springer-Verlag, Heidelberg, Berlin. I. Fendrik, M. del Gallo, J. Vanderleyden, M. de Zamaroczy (Eds.).
37. Elmerich C., Newton W.E. Associative and Endophytic Nitrogen-Fixing Bacteria and Cyanobacterial Associations 2007, Springer, Netherlands.
38. Elo S., Maunuksela L., Salkinoja-Salonen M., Smolander A., Haahtela K. Humus bacteria of Norway spruce stands: plant growth promoting properties and birch, red fescue and alder colonizing capacity. FEMS Microbiol. Ecol. 2000, 31:143-152.
39. Estrada de los Santos P., Bustillos-Cristales R., Caballero-Mellado J. Burkholderia, a genus rich in plant associated nitrogen fixers with wide environmental and geographic distribution. Appl. Environ. Microbiol. 2001, 67:2790-2798.
40. Fierer N., Jackson R.B. The diversity and biogeography of soil bacterial communities. PNAS 2006, 103:626-631.
41. Franco A.A., Dobereiner J. A biologia do solo e a sustentabilidade dos solos tropicais. Summa Phytopathologica 1994, 20:68-74.
42. Garcia de Salamone I.E., Hynes R.K., Nelson L.M. Role of cytokinins in plant growth promotion by rhizosphere bacteria. PGPR: Biocontrol and Biofertilization 2005, 173-195. Springer, Netherlands. A. Siddiqui (Ed.).
43. Giongo A., Ambrosini A., Vargas L.K., Freire J.R.J., Bodanese-Zanettini M.H., Passaglia L.M.P. Evaluation of genetic diversity of bradyrhizobia strains nodulating soybean [Glycine max (L.) Merrill] isolated from South Brazilian fields. Appl. Soil Ecol. 2008, 38:261-269.
44. Glick B.R. The enhancement of plant growth by free-living bacteria. Can. J. Microbiol. 1995, 41:109-117.
45. Glickmann E., Dessaux Y. A critical examination of the specificity of the Salkowski Reagent for indolic compounds produced by phytopathogenic bacteria. Appl. Environ. Microbiol. 1995, 61:793-796.
46. James E.K. Nitrogen fixation in endophytic and associative symbiosis. Field Crops Res. 2000, 65:197-209.
47. Janssen P.H. Identifying the dominant soil bacteria taxa in libraries of 16S rRNA and 16S rRNA genes. Appl. Environ. Microbiol. 2006, 72:1719-1728.
48. Kaschuk G., Hungria M., Andrade D.S., Campo R.J. Genetic diversity of rhizobia associated with common bean (Phaseolus vulgaris L.) grown under no-tillage and conventional systems in Southern Brazil. Appl. Soil Ecol. 2006, 32:210-220.
49. Kemmitt S.J., Wright D., Goulding K.W.T., Jones D.L. pH regulation of carbon and nitrogen dynamics in two agricultural soils. Soil Biol. Biochem. 2006, 38:898-911.
50. Khalid A., Tahir S., Arshad M., Zahir Z.A. Relative efficiency of rhizobacteria for auxin biosynthesis in rhizosphere vs. non-rhizosphere soil. Aust. J. Soil Res. 2004, 42:921-926.
51. Kuklinsky-Sobral J., Araújo W.L., Mendes R., Geraldi I.O., Pizzirani-Kleiner A.A., Azevedo J.L. Isolation and characterization of soybean-associated bacteria and their potencial for plant growth promotion. Environ. Microbiol. 2004, 6:1244-1251.
52. Lalande R., Bissonnette N., Coutlée D., Antoun H. Identification of rhizobacteria from maize and determination of their plant-growth promoting potential. Plant Soil 1989, 115:7-11.
53. Magnani G.S., Didonet C.M., Cruz L.M., Picheth C.F., Pedrosa F.O., Souza E.M. Diversity of endophytic bacteria in Brazilian sugarcane. Genet. Mol. Res. 2010, 9:250-258.
54. Masalha J., Kosegarten H., Elmaci ö., Mengel K. The central role of microbial activity for iron acquisition in maize and sunflower. Biol. Fertil. Soils 2000, 30:433-439.
55. Mirza M.S., Ahmad W., Latif F., Haurat J., Bally R., Normand P., Malik K.A. Isolation, partial characterization, and the effect of plant growth-promoting bacteria (PGPB) on micro-propagated sugarcane in vitro. Plant Soil 2001, 237:47-54.
56. Natheer S.E., Muthukkaruppan S. Assessing the in vitro zinc solubilization potential and improving sugarcane growth by inoculating Gluconacetobacter diazotrophicus. Ann. Microbiol 2011.
57. Nowak J., Shulaev V. Priming for transplant stress resistance in vitro propagation. In Vitro Cell Dev. Biol. Plant 2003, 39:107-124.
58. Oliveira A.L.O., Canuto E.L., Urquiaga S., Reis V.M., Baldani J.I. Yield of micropropagated sugarcane varieties in different soil types following inoculation with diazotrophic bacteria. Plant Soil 2006, 284:23-32.
59. Omarjee J., Van Antwerpen V., Balandreau J., Kuniata L., Rutherford S. Isolation and characterization of some endophytic bacteria from Papua New Guinea sugarcane. Proc. S. Afr. Sug. Technol. Ass. 2004, 78:189-194.
60. Palus J.A., Borneman J., Ludden P.W., Triplett E.W. A diazotrophic bacterial endophyte isolated from stems of Zea mays L. and Zea luxurians Iltis and Doebley. Plant Soil 1996, 186:135-142.
61. Patten C., Glick B. Bacterial biosynthesis of indole-3-acetic acid. Can. J. Microbiol. 1996, 42:207-220.
62. Perin L., Martínez-Aguilar L., Castro-González R., Estrada-de los Santos P., Cabellos-Avelar T., Guedes H.V., Reis V.M., Caballero-Mellado J. Diazotrophic Burkholderia species associated with field-grown maize and sugarcane. Appl. Environ. Microbiol. 2006, 72:3103-3110.
63. Perlova O., Ureta A., Meletzus D., Nordlund S. Sensing of N-status in Gluconacetobacter diazotrophicus: biochemistry and genetics of nitrogen fixation and assimilation. Symbiosis 2003, 35:73-84.
64. Poly F., Monrozier L.J., Bally R. Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res. Microbiol. 2001, 152:95-103.
65. Reinhold-Hurek B., Hurek T. Life in grasses, diazotrophic endophytes. Trends Microbiol. 1998, 6:139-144.
66. Reis Júnior F.B., Silva L.G., Reis V.M., Döbereiner J. Ocorrência de bactérias diazotróficas em diferentes genótipos de cana-de-açúcar. Pesq. Agropec. Bras 2000, 35:985-994.
67. Reis V.M., Estrada-de los Santos P., Tenorio-Salgado S., Vogel J., Stoffels M., Guyon S., Mavingui P., Baldani V.L.D., Schmid M., Baldani J.I., Balandreau J., Hartmann A., Caballero-Mellado J. Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant associated bacterium. Int. J. Syst. Evol. Microbiol. 2004, 54:2155-2162.
68. Reis V.M., Lee S., Kennedy C. Biological nitrogen fixation in sugarcane. Associative and Endophytic Nitrogen-Fixing Bacteria and Cyanobacterial Associations 2007, 213-232. Springer, Netherlands. C. Elmerich, W.E. Newton (Eds.).
69. Reiter B., Bürgmann H., Burg K., Sessitsch A. Endophytic nifH gene diversity in African sweet potato. Can. J. Microbiol. 2003, 49:549-555.
70. Rico A., Ortiz-Barredo A., Ritter E., Murillo J. Genetic characterization of Erwinia amylovora strains by amplified fragment length polymorphism. J. Appl. Microbiol. 2004, 96:302-310.
71. Rivas R., Mateos P.F., Martinez-Molina E., Velázquez E. Paenibacillus xylanilyticus sp. nov., an airborne xylanolytic bacterium. Int. J. Syst. Evol. Microbiol. 2005, 55:405-408.
72. Rohlf, F.J. 1990. NTSYS-pc numerical taxonomy and multivariate system. Version 2.01. Exeter Software. Setauket, New York.
73. 2-fixer) and Bacillus licheniformis (P-solubilizer), both from a semiarid mangrove rhizosphere. FEMS Microbiol. Ecol. 2001, 35:181-187.
74. 2-fixing and phosphate solubilizing bacteria. Plant Soil 2004, 265:123-129.
75. Sambrook J., Russel D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, New York.
76. Salles J.F., De Souza F.A., van Elsas J.D. Molecular method to assess the diversity of Burkholderia species in environmental samples. Appl. Environ. Microbiol. 2002, 68:1595-1603.
77. Salles J.F., van Veen J.A., van Elsas J.D. Multivariate analyses of Burkholderia species in soil: effect of crop and land use history. Appl. Environ. Microbiol. 2004, 70:4012-4020.
78. Sarwar M., Kremer R.J. Determination of bacterially derived auxins using a microplate method. Lett. Appl. Microbiol. 1992, 20:282-285.
79. Schwyn B., Neilands J.B. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 1987, 160:47-56.
80. Scott A.J., Knott M. A cluster analysis method for grouping means in the analysis of variance. Biometrics 1974, 30:507-512.
81. Shannon C.E., Weaver W. The Mathematical Theory of Communication 1949, University of Illinois Press, Urbana.
82. Soares R.A., Roesch L.F.W., Zanatta G., Camargo F.A.O., Passaglia L.M.P. Occurrence and distribution of nitrogen fixing bacterial community associated with oat (Avena sativa) assessed by molecular and microbiological techniques. Appl. Soil Ecol. 2006, 33:221-234.
83. Somers E., Vanderleyden J., Srinivasan M. Rhizosphere bacterial signalling: a love parade beneath our feet. Crit. Rev. Microbiol. 2004, 30:205-240.
84. Suman A., Shasany A.K., Singh M., Shahi H.N., Gaur A., Khanuja S.P.S. Molecular assessment of diversity among endophytic diazotrophs isolated from subtropical Indian sugarcane. World J. Microbiol. Biotechnol. 2001, 17:39-45.
85. Suman A., Gaur A., Shrivastava A.K., Yadav R.L. Improving sugarcane growth and nutrient uptake by inoculating Gluconacetobacter diazotrophicus. Plant Growth Regul 2005, 47:155-162.
86. Sylvester-Bradley R., Asakawa N., La Torraca S., Magalhães F.M.M., Oliveira L., Pereira R.M. Levantamento quantitativo de microrganismos solubilizadores de fosfatos na rizosfera de gramíneas e leguminosas forrageiras na Amazônia. Acta Amazônica 1982, 12:15-22.
87. Tripathi A.K., Nagarajan T., Verma S.C., Rudulier D.L. Inhibition of biosynthesis and activity of nitrogenase in Azospirillum brasilense Sp7 under salinity stress. Curr. Microbiol. 2002, 44:363-367.
88. Vandamme P., Giovan J., LiPuma J.J. Diversity and role of Burkholderia spp. Burkholderia: Molecular Biology and Genomics 2007, 1-27. Horizon Scientific Press, Norwich. P. Vandamme, T. Coenye (Eds.).
89. van Elsas J.D., Garbeva P., Salles J. Effects of agronomical measures on the microbial diversity of soils as related to the suppression of soil-borne plant pathogens. Biodegradation 2002, 13:29-40.
90. Wong-Villarreal A., Caballero-Mellado J. Rapid identification of nitrogen-fixing and legume-nodulating Burkholderia species based on PCR 16SrRNA species-specific oligonucleotides. Syst. Appl. Microbiol. 2010, 33:35-43.
91. Yim W.J., Poonguzhali S., Madhaiyan M., Palaniappan P., Siddikee M.A., Sa T. Characterization of plant-growth promoting diazotrophic bacteria isolated from field grown Chinese cabbage under different fertilization conditions. J. Microbiol. 2009, 47:147-155.
92. Zehr J.P., Jenkins B.D., Short S.M., Steward G.F. Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ. Microbiol. 2003, 5:539-554.
93. Zinniel D.K., Lambrecht P., Harris N.B., Feng Z., Kuczmarski D. Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl. Env. Microbiol. 2002, 68:2198-2208.