Plant and Soil

, Volume 366, Issue 1–2, pp 585–603 | Cite as

The effect of plant growth-promoting rhizobacteria on the growth of rice (Oryza sativa L.) cropped in southern Brazilian fields

  • Rocheli de Souza
  • Anelise Beneduzi
  • Adriana Ambrosini
  • Pedro Beschoren da Costa
  • Jacqueline Meyer
  • Luciano K. Vargas
  • Rodrigo Schoenfeld
  • Luciane M. P. Passaglia
Regular Article
First Online:
Received:
Accepted:

Abstract

Background and Aims

Several strains of rhizobacteria may be found in the rhizospheric soil, on the root surface or in association with rice plants. These bacteria are able to colonize plant root systems and promote plant growth and crop yield through a variety of mechanisms. The objectives of this study were to isolate, identify, and characterize putative plant growth-promoting rhizobacteria (PGPR) associated with rice cropped in different areas of southern Brazil.

Methods

Bacterial strains were selectively isolated based on their growth on three selective semi-solid nitrogen-free media. Bacteria were identified at the genus level by PCR-RFLP 16S rRNA gene analysis and partial sequencing methodologies. Bacterial isolates were evaluated for their ability to produce indolic compounds and siderophores and to solubilize phosphate. In vitro biological nitrogen fixation and the ability to produce 1-aminocyclopropane-1-carboxylate deaminase were evaluated for each bacterial isolate used in the inoculation experiments.

Results

In total, 336 bacterial strains were isolated representing 31 different bacterial genera. Strains belonging to the genera Agrobacterium, Burkholderia, Enterobacter, and Pseudomonas were the most prominent isolates. Siderophore and indolic compounds producers were widely found among isolates, but 101 isolates were able to solubilize phosphate. Under gnotobiotic conditions, eight isolates were able to stimulate the growth of rice plants. Five of these eight isolates were also field tested in rice plants subjected to different nitrogen fertilization rates.

Conclusions

The results showed that the condition of half-fertilization plus separate inoculation with the isolates AC32 (Herbaspirillum sp.), AG15 (Burkholderia sp.), CA21 (Pseudacidovorax sp.), and UR51 (Azospirillum sp.) achieved rice growth similar to those achieved by full-fertilization without inoculation, thus highlighting the potential of these strains for formulating new bioinoculants for rice crops.

Keywords

PGPR Plant growth promoting rhizobacteria Plant yield Nutrient uptake Rice 
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Notes

Acknowledgments

This work was financed by a grant and fellowships from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brasil) and INCT da Fixação Biológica do Nitrogênio (Brasil).

Supplementary material

11104_2012_1430_MOESM1_ESM.doc (44 kb)
Table SM-1 The effect of native PGPR on the growth of rice under different nitrogen fertilizer treatments with or without inoculation in the field assay (DOC 44 kb)
11104_2012_1430_MOESM2_ESM.doc (44 kb)
Table SM-2 Number of panicles and rice yield under different nitrogen fertilizer treatments with or without inoculation of native PGPR in the field assay. (DOC 44 kb)
11104_2012_1430_MOESM3_ESM.doc (46 kb)
Table SM-3 Effect on N, P and K uptake per gram of rice shoot under different nitrogen fertilizer treatments with or without inoculation of native PGPR in the field assay. (DOC 45 kb)

References

  1. Adesmoye AO, Kloepper JW (2009) Plant-microbes interactions in enhanced fertilizer use efficiency. Appl Microbiol Biotechnol 85:1–12. doi: 10.1007/s00253-009-2196 CrossRefGoogle Scholar
  2. Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929. doi: 10.1007/s00248-009-9531-y PubMedCrossRefGoogle Scholar
  3. Ahmad F, Ahmad I, Khan MS (2006) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181. doi: 10.1016/j.micres.2006.04.001 PubMedCrossRefGoogle Scholar
  4. 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 PubMedCrossRefGoogle Scholar
  5. Ambrosini A, Beneduzi A, Stefanski T, Pinheiro FG, Vargas LK, Passaglia LMP (2012) Screening of plant growth promoting Rhizobacteria isolated from sunflower (Helianthus annuus L.). Plant Soil 356:245–264. doi: 10.1007/s11104-011-1079-1 CrossRefGoogle Scholar
  6. Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57–67. doi: 10.1023/A:1004326910584 CrossRefGoogle Scholar
  7. Araujo WL, Maccheroni W Jr, Aguilar-Vildoso CI, Barroso PAV, Saridakis HO, Azevedo JL (2001) Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can J Microbiol 47:229–236. doi: 10.1139/cjm-47-3-229 PubMedCrossRefGoogle Scholar
  8. Beneduzi A, Peres D, Vargas LK, Bodanese-Zanettini MH, Passaglia LMP (2008) Evaluation of genetic diversity and plant growth promoting activities of nitrogen-fixing bacilli isolated from rice fields in South Brazil. Appl Soil Ecol 39:311–320. doi: 10.1016/j.apsoil.2008.01.006 CrossRefGoogle Scholar
  9. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13. doi: 10.1111/j.1574-6941.2009.00654.x PubMedCrossRefGoogle Scholar
  10. Bhromsiri C, Bhromsiri A (2010) Isolation, screening of growth-promoting activities and diversity of Rhizobacteria from Vetiver Grass and Rice plants. Thail J Agric Sci 43:217–230Google Scholar
  11. Biswas JC, Ladha JK, Dazzo FB, Irbg R, Irbg B (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650CrossRefGoogle Scholar
  12. Boddey RM (1987) Methods for quantification of nitrogen fixation associated with gramineae. Crit Rev Plant Sci 6:209–266CrossRefGoogle Scholar
  13. Borges LGA, Dalla Vechia V, Corçao G (2003) Characterization and genetic diversity via REP-PCR of Escherichia coli isolates from polluted waters in southern Brazil. FEMS Microbiol Ecol 45:173–180. doi: 10.1016/S0168-6496(03)00147-8 CrossRefGoogle Scholar
  14. Brämer CO, Vandamme P, Silva LF, Gomez JGC, Steinbüchel A (2001) Burkholderia sacchari sp. nov., a polyhydroxyalkanoate-accumulating bacterium isolated from soil of a sugar-cane plantation in Brazil. Int J Syst Evol Microbiol 51:1709–1713PubMedCrossRefGoogle Scholar
  15. Briones AM, Okabe S, Umemiya Y, Ramsing N, Reichardt W, Okuyama H (2002) Influence of different cultivars on populations of ammonia-oxidizing bacteria in the root environment of rice. Appl Environ Microbiol 68:3067–3075. doi: 10.1128/AEM.68.6.3067-3075.2002 PubMedCrossRefGoogle Scholar
  16. Brosius J, Palmer ML, Kennedy PJ, Noller HF (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A 75(10):4801–4805. doi: 10.1073/pnas.75.10.4801 PubMedCrossRefGoogle Scholar
  17. Caballero-Mellado J, Onofre-Lemus J, Estrada SP, Martínez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319. doi: 10.1128/AEM.00324-07 PubMedCrossRefGoogle Scholar
  18. Çakmakçi R, Dönmez F, Aydın A, Şahin F (2006) Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol Biochem 38(6):1482–1487. doi: 10.1016/j.soilbio.2005.09.019 CrossRefGoogle Scholar
  19. Çakmakçi R, Erat M, Erdogan U, Donmez MF (2007) The influence of plant growth-promoting rhizobacteria on growth and enzyme activities in wheat and spinach plant. J Plant Nutr Soil Sci 170:288–295. doi: 10.1002/jpln.200625105 CrossRefGoogle Scholar
  20. Chabot R, Antoun H, Cescas MP (1996) Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Plant Soil 184:311–321CrossRefGoogle Scholar
  21. Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261. doi: 10.1099/ijs.0.64915-0 PubMedCrossRefGoogle Scholar
  22. Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729. doi: 10.1046/j.1462-2920.2003.00471.x PubMedCrossRefGoogle Scholar
  23. De Freitas JR, Germida JJ (1990) Plant growth promoting rhizobacteria for winter wheat. Can J Microbiol 36:265–272CrossRefGoogle Scholar
  24. Di Cello F, Bevivino L, Chiarini R, Fani R, Paffetti D, Tabacchioni S, Dalmastri C (1997) Biodiversity of a Burkholderia cepacia population isolated from the maize. Appl Environ Microbiol 63:4485–4493PubMedGoogle Scholar
  25. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149CrossRefGoogle Scholar
  26. Döbereiner J, Baldani VLD, Baldani JI (1995) Como isolar e identificar bactérias diazotróficas de plantas não-leguminosas. Embrapa-SPI, BrasíliaGoogle Scholar
  27. Duarah I, Deka M, Saikia N, Deka Boruah HP (2011) Phosphate solubilizers enhance NPK fertilizer use efficiency in rice and legume cultivation. Biotechnol 1:227–238. doi: 10.1007/s13205-011-0028-2 Google Scholar
  28. Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189. doi: 10.1016/j.apsoil.2007.02.005 CrossRefGoogle Scholar
  29. Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 67:5285–5293. doi: 10.1128/AEM.67.11.5285-5293.2001 PubMedCrossRefGoogle Scholar
  30. Estrada P, Mavingui P, Cournoyer B, Fontaine F, Balandreau J, Caballero-Mellado J (2002) A N2-fixing endophytic Burkholderia sp. associated with maize plants cultivated in Mexico. Can J Microbiol 48:285–294. doi: 10.1139/W02-023 PubMedCrossRefGoogle Scholar
  31. Farina R, Beneduzi A, Ambrosini A, Campos SB, Lisboa BB, Wendisch V, Vargas LK, Passaglia LMP (2012) Diversity of plant growth-promoting rhizobacteria communities associated with the stages of canola growth. Appl Soil Ecol 55:44–52. doi: 10.1016/j.apsoil.2011.12.011 CrossRefGoogle Scholar
  32. Felske A, Rheims H, Wokerink A, Stackebrandt E, Akkermans DL (1997) Ribosome analysis reveals prominent activity of an uncultured member of the class Actinobacteria in grasslands soils. Microbiol 143:2983–2989. doi: 10.1099/00221287-143-9-2983 CrossRefGoogle Scholar
  33. Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol 76:1145–1152. doi: 10.1007/s00253-007-1077-7 PubMedCrossRefGoogle Scholar
  34. García-Fraile P, Rivas R, Willems A, Peix A, Martens M, Martínez-Molina E, Mateos PF, Velazquez E (2007) Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. Int J Syst Evol Microbiol 57:844–848. doi: 10.1099/ijs.0.64680-0 PubMedCrossRefGoogle Scholar
  35. Gillis M, Van Van T, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fernande MP (1995) Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Bacteriol 45:274–289. doi: 10.1099/00207713-45-2-274 CrossRefGoogle Scholar
  36. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117CrossRefGoogle Scholar
  37. Glick BR, Patten CL, Holguin G, Penrose DM (1999) Biochemical and genetics mechanisms used by plant growth promoting bacteria. Imperial College Press, LondonCrossRefGoogle Scholar
  38. Glick BR, Pasternak JJ (2003) Plant growth promoting bacteria. In: Glick BR, Pasternak JJ (eds) Molecular biotechnology principles and applications of recombinant DNA, 3rd. ASM Press, Washington, pp 436–454Google Scholar
  39. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7. doi: 10.1016/j.femsle.2005.07.030 PubMedCrossRefGoogle Scholar
  40. Govindarajan M, Kwon SW, Weon HY (2007) Isolation, molecular characterization and growth-promoting activities of endophytic sugarcane diazotroph Klebsiella sp. GR9. World J Microbiol Biotechnol 23:997–1006. doi: 10.1007/s11274-006-9326-y CrossRefGoogle Scholar
  41. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395–412. doi: 10.1016/j.soilbio.2004.08.030 CrossRefGoogle Scholar
  42. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  43. Hameed S, Yasmin S, Malik KA, Zafar Y, Hafeez FY (2004) Rhizobium, Bradyrhizobium and Agrobacterium strains isolated from cultivated legumes. Biol Fertil Soils 39:179–185. doi: 10.1007/s00374-003-0697-z CrossRefGoogle Scholar
  44. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis version 2.09. Palaeontol Electron 4(1):9Google Scholar
  45. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598. doi: 10.1007/s00248-007-9247-9 CrossRefGoogle Scholar
  46. Hinton DM, Bacon CW (1995) Enterobacter cloacae is an endophytic symbiont of corn. Mycopathologia 129:117–125. doi: 10.1007/BF01103471 PubMedCrossRefGoogle Scholar
  47. Jaillais Y, Chory J (2010) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17:642–645. doi: 10.1038/nsmb0610-642 PubMedCrossRefGoogle Scholar
  48. James EK (2000) Nitrogen fixation in endophytic and associative symbiosis. Field Crop Res 65:197–209. doi: 10.1016/S0378-4290(99)00087-8 CrossRefGoogle Scholar
  49. Joshi P, Bhatt AB (2011) Diversity and function of plant growth promoting Rhizobacteria associated with wheat Rhizosphere in North Himalayan Region. Int J Environ Sci 1:1135–1143Google Scholar
  50. Kämpfer P, Thummes K, Chu HI, Tan CC, Arun AB, Chen WM, Lai WA, Shen FT, Rekha PD, Young CC (2008) Pseudacidovorax intermedius gen. nov., sp. nov., a novel nitrogen-fixing betaproteobacterium isolated from soil. Int J Syst Evol Microbiol 58:491–495. doi: 10.1099/ijs.0.65175-0 PubMedCrossRefGoogle Scholar
  51. 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 32:210–220. doi: 10.1016/j.apsoil.2005.06.008 CrossRefGoogle Scholar
  52. Khorshidi YR, Ardakani MR, Ramezanpour MR, Khavazi K, Zargari K (2011) Response of yield and yield components of rice (Oryza sativa L.) to Pseudomonas flouresence and Azospirillum lipoferum under different nitrogen levels. American-Eurasian J Agric Environ Sci 10:387–395Google Scholar
  53. Khush G (2003) Productivity improvements in rice. Nutr Rev 61:114–116. doi: 10.1301/nr.2003.jun.S114-S116 CrossRefGoogle Scholar
  54. Kim KY, Jordan D, McDonald GA (1998) Effect of phosphate-solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol Fertil Soils 26:79–87. doi: 10.1007/s003740050347 CrossRefGoogle Scholar
  55. Kowalchuk GA, Buma DS, De Boer W, Klinkhamer PGL, Van Veen JA (2002) Effects of above-ground plant species com-position and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek 81:509–520. doi: 10.1023/A:1020565523615 PubMedCrossRefGoogle Scholar
  56. Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251PubMedCrossRefGoogle Scholar
  57. Ladha JK, Reddy PM (2003) Nitrogen fixation in rice systems: state of knowledge and future prospect. Plant Soil 252:151–167. doi: 10.1023/A:1024175307238 CrossRefGoogle Scholar
  58. Lim JH, Baek SH, Lee ST (2008) Burkholderia sediminicola sp. nov., isolated from freshwater sediment. Int J Syst Evol Microbiol 58:565–569. doi: 10.1099/ijs.0.65502-0 PubMedCrossRefGoogle Scholar
  59. Lugtenberg B, Chin-A-Woeng T, Bloemberg GV (2002) Microbe plant interactons: principles and mechanisms. Antonie Van Leeuwenhoek 81:373–383. doi: 10.1023/A:1020596903142 PubMedCrossRefGoogle Scholar
  60. Lynch JM (1990) The rhizosphere. Wiley-Interscience, Chichester, p 458Google Scholar
  61. Magnani GS, Didonet CM, Cruz LM, Picheth CF, Pedrosa FO, Souza EM (2010) Diversity of endophytic bacteria in Brazilian sugarcane. Genet Mol Res 9:250–258. doi: 10.4238/vol9-1gmr703 PubMedCrossRefGoogle Scholar
  62. Malik KA, Bilal R, Mezhnez S, Rasul G, Mirza MS, Ali S (1997) Association of nitrogen fixing, plant-growth-promoting rhizobacteria (PGPR) with kallar grass and rice. Plant Soil 194:37–44CrossRefGoogle Scholar
  63. Masalha J, Kosegarten H, Elmaci O, Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fertil Soils 30:433–439. doi: 10.1007/s003740050021 CrossRefGoogle Scholar
  64. Mitchell RJ, Hester AJ, Campbell CD, Chapman SJ, Cameron CM, Hewison RL, Potts JM (2010) Is vegetation composition or soil chemistry the best predictor of the soil microbial community? Plant Soil 333:417–430. doi: 10.1007/s11104-010-0357-7 CrossRefGoogle Scholar
  65. Neilands JK (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726. doi: 10.1074/jbc.270.45.26723 PubMedGoogle Scholar
  66. Nogueira MA, Albino UB, Brandão-Junior O, Braun G, Cruz MF, Dias BA, Duarte RTD, Gioppo NMR, Menna P, Orlandi JM, Raimam MP, Rampazzo LGL, Santos MA, Silva MEZ, Vieira FP, Torezan JMD, Hungria M, Andrade G (2006) Promising indicators for assessment of agroecosystems alteration among natural, reforested and agricultural land use in southern Brazil. Agric Ecosyst Environ 115:237–247. doi: 10.1016/j.agee.2006.01.008 CrossRefGoogle Scholar
  67. Okon Y, Labandrera-Gonzalez CA (1994) Agronomic applications of Azospirillum: an evaluation of 20 years of worldwide field inoculation. Soil Biol Biochem 26:1591–1601. doi: 10.1016/0038-0717(94)90311-5 CrossRefGoogle Scholar
  68. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15. doi: 10.1034/j.1399-3054.2003.00086.x PubMedCrossRefGoogle Scholar
  69. Reis VM, Estrada PS, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Mavingui P, Baldani VLD, Schmid M, Baldani JI, Balandreau J, Hartmann A, Caballero-Mellado J (2004) Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int J Syst Evol Microbiol 54:2155–2162. doi: 10.1099/ijs.0.02879-0 PubMedCrossRefGoogle Scholar
  70. Reiter B, Bürgmann H, Burg K, Sessitsch A (2003) Endophytic nifH gene diversity in African sweet potato. Can J Microbiol 49:549–555. doi: 10.1139/w03-070 PubMedCrossRefGoogle Scholar
  71. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906. doi: 10.1071/PP01093 Google Scholar
  72. Rico A, Ortiz-Barredo A, Ritter E, Murillo J (2004) Genetic characterization of Erwinia amylovora strains by amplified fragment length polymorphism. J Appl Microbiol 96:302–310. doi: 10.1046/j.1365-2672.2003.02156.x PubMedCrossRefGoogle Scholar
  73. Roesch LFW, Quadros PD, Camargo FAO, Triplett EW (2007) Screening of diazotrophic bacteria Azopirillum spp. for nitrogen fixation and auxin production in multiple field sites in southern Brazil. World J Microbiol Biotechnol 23:1377–1383. doi: 10.1007/s11274-007-9376-9 CrossRefGoogle Scholar
  74. Roesch LFW, Camargo FAO, Bento FM, Triplett EW (2008) Biodiversity of diazotrophic bacteria within the soil, root and stem of field-grown maize. Plant Soil 302:91–104. doi: 10.1007/s11104-007-9458-3 CrossRefGoogle Scholar
  75. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  76. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual. Ed. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  77. Santi Ferrara FI, Oliveira ZM, Gonzales HHS, Floh EIS, Barbosa HR (2011) Endophytic and rhizospheric enterobacteria isolated from sugar cane have different potentials for producing plant growth-promoting substances. Plant Soil 353:409–417. doi: 10.1007/s11104-011-1042-1 CrossRefGoogle Scholar
  78. Sasaki K, Ikeda S, Eda S, Mitsui H, Hanzawa E, Kisara C, Kazama Y, Kushida A, Shinano T, Minamisawa K, Sat T (2010) Impact of plant genotype and nitrogen level on rice growth response to inoculation with Azospirillum sp. strain B510 under paddy field conditions. Soil Sci Plant Nutr 56:636–644. doi: 0.1111/j.1747-0765.2010.00499.x CrossRefGoogle Scholar
  79. Schulten HR, Schnitzer M (1998) The chemistry of soil organic nitrogen: a review. Biol Fertil Soils 26:1–15CrossRefGoogle Scholar
  80. Schulz B, Boyle C (2006) What are endophytes? In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 1–13CrossRefGoogle Scholar
  81. Selosse MA, Baudoin E, Vandenkoornhuyse P (2004) Symbiotic microorganisms, a key for ecological success and protection of plants. C R Biol 327:639–648. doi: 10.1016/j.crvi.2003.12.008 PubMedCrossRefGoogle Scholar
  82. Shaharoona B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Appl Microbiol Biotechnol 79:147–155. doi: 10.1007/s00253-008-1419-0 PubMedCrossRefGoogle Scholar
  83. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, UrbanaGoogle Scholar
  84. Shoebitz M, Ribaudo CM, Pardo MA, Cantore ML, Ciampi L, Curá JA (2009) Plant growth promoting properties of a strain of Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Soil Biol Biochem 41:1768–1774. doi: 10.1016/j.soilbio.2007.12.031 CrossRefGoogle Scholar
  85. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot R, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751. doi: 10.1128/AEM.67.10.4742-4751.2001 PubMedCrossRefGoogle Scholar
  86. Sociedade Sul-Brasileira de Arroz Irrigado (2010) Arroz irrrigado: Recomendações técnicas para o Sul do Brasil. Bento Gonçalves, RS: Sosbai, p 188Google Scholar
  87. Su C, Lei L, Duan Y, Zhang KQ, Yang J (2012) Culture-independent methods for studying environmental microorganisms: methods, application, and perspective. Appl Microbiol Biotechnol 93:993–1003. doi: 10.1007/s00253-011-3800-7 PubMedCrossRefGoogle Scholar
  88. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolution genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  89. Tedesco JM, Gianelo C, Bissani CA, Bohnen H, Volkweiss SJ (1995) Análises de solo, plantas e outros materiais. Universidade Federal do Rio Grande do Sul, Porto AlegreGoogle Scholar
  90. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higging DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  91. Tian F, Ding Y, Zhu H, Yao L, Du B (2009) Genetic diversity of siderophore producing bacteria of tobacco Rhizosphere. Braz J Microbiol 40:276–284CrossRefGoogle Scholar
  92. Tuzun S, Kloepper JW (1994) In: Ryder MH (ed) Induced systemic resistance by plant growth-promoting rhizobacteria. CSIRO, Adelaide, pp 104–109Google Scholar
  93. Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254. doi: 10.1007/s10658-007-9165-1 CrossRefGoogle Scholar
  94. Vega NWO (2007) A review on beneficial effects of rhizosphere bacteria on soil nutrient availability and plant nutrient uptake. Rev Fac Nal Agr Medellín 60:3621–3643Google Scholar
  95. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586. doi: 10.1023/A:1026037216893 CrossRefGoogle Scholar
  96. Wartiainen I, Eriksson T, Zheng W, Rasmussen U (2008) Variation in the active diazotrophic community in rice paddy-nifH PCR-DGGE analysis of rhizosphere and bulk soil. Appl Soil Ecol 39:65–75. doi: 10.1016/j.apsoil.2007.11.008 CrossRefGoogle Scholar
  97. 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. doi: 10.1007/s11104-010-0454-7 CrossRefGoogle Scholar
  98. Zhang Y, Li D, Wang H, Xiao Q, Liu X (2006) Molecular diversity of nitrogen-fixing bacteria from the Tibetan plateau, China. FEMS Microbiol Lett 260:134–142. doi: 10.1111/j.1574-6968.2006.00317.x PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Rocheli de Souza
    • 1
  • Anelise Beneduzi
    • 2
  • Adriana Ambrosini
    • 1
  • Pedro Beschoren da Costa
    • 1
  • Jacqueline Meyer
    • 1
  • Luciano K. Vargas
    • 2
  • Rodrigo Schoenfeld
    • 3
  • Luciane M. P. Passaglia
    • 1
  1. 1.Departamento de Genética, Instituto de BiociênciasUniversidade Federal do Rio Grande do Sul (UFRGS)Porto AlegreBrasil
  2. 2.Fundação Estadual de Pesquisa Agropecuária (FEPAGRO)Porto AlegreBrasil
  3. 3.Instituto Riograndense do Arroz (IRGA)CachoeirinhaBrasil

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