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Diversity and functional characterization of bacterial endophytes dwelling in various rice (Oryza sativa L.) tissues, and their seed-borne dissemination into rhizosphere under gnotobiotic P-stress

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Abstract

Aim

Endophytic bacterial diversity in four rice cultivars grown in two soil-types, their plant-probiotic features and rhizospheric deployment under P-stress were investigated.

Methods

Oryza sativa cvs. TCN1, TCS10, TK8, and TN71 were cultivated in greenhouse using non-sterile acidic and near-neutral paddy soils for 60 days. Root, stem and leaf tissues were screened for culturable bacterial endophytes using nutrient agar. Endophytes were identified and profiled for plant-probiotic features. The richness, Shannon-Weiner diversity, evenness and Venn’s distribution in terms of endophytic strains were evaluated. Seed-borne endophytes were characterized through DGGE. The deployment of endophytes into the rhizosphere in TCN1 and TK8 under gnotobiotic P-stress was assessed.

Results

A total of 52 distinct endophytic bacterial strains affiliated to 5 classes and 20 discrete genera exhibiting differential plant-probiotic features were isolated from various tissues of four different rice cultivars. The diversity and distribution of endophytes fluctuated with soil-type, tissue-type and rice genotype. Gnotobiotic insoluble P treatment revealed significantly enhanced deployment of P-solubilizing rhizobacteria in TCN1 as compared to soluble P and P-lacking control.

Conclusions

Rice endophytic bacteria are diverse, and their distribution within the plant and deployment as rhizobacteria were found to be influenced by host genotype, edaphic factors and nutrient stress.

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References

  • Barraquio WL, Revilla L, Ladha JK (1997) Isolation of endophytic diazotrophic bacteria from wetland rice. Plant Soil 194:15–24

    Article  CAS  Google Scholar 

  • Boddey RM, de Oliveira OC, Urquiaga S, Reis VM, de Olivares FL, Baldani VLD, Döbereiner I (1995) Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement. Plant Soil 174:195–209

    Article  CAS  Google Scholar 

  • Botta AL, Santacecilia A, Ercole C, Cacchio P, Del Gallo M (2013) In vitro and in vivo inoculation of four endophytic bacteria on Lycopersicon esculentum. New Biotechnol 30:666–674

    Article  CAS  Google Scholar 

  • Bremner JM, Mulvaney CS (1982) Nitrogen‑total. In: Page AL, Miller RH, Kenney DR (Ed.) Methods of soil analysis. Part 2 – microbiological and biochemical properties. New York: Soil Science Society of America pp 595–624 (SSA book series, 5)

  • Chaudhary HJ, Peng G, Hu M, He Y, Yang L, Luo Y, Tan Z (2012) Genetic diversity of endophytic diazotrophs of the wild rice, Oryza alta and identification of the new diazotroph, Acinetobacter oryzae sp. nov. Microb Ecol 63:813–821

    Article  CAS  PubMed  Google Scholar 

  • Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41

    Article  Google Scholar 

  • Cheng YH, Cheng AH, Chen SS, Tu CC (1989) The outbreaks of pod rot of peanut and its control. J Agri Res China 38:353–364

    Google Scholar 

  • Clark LL, Dajcs JJ, McLean CH, Bartell JG, Stroman DW (2006) Pseudomonas otitidis sp. nov., isolated from patients with otic infections. Int J Syst Evol Microbiol 56:709–714

    Article  CAS  PubMed  Google Scholar 

  • Compant S, Clement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678

    Article  CAS  Google Scholar 

  • Cottyn B, Debode J, Regalado E, Mew TW, Swings J (2009) Phenotypic and genetic diversity of rice seed-associated bacteria and their role in pathogenicity and biological control. J Appl Microbiol 107:885–897

    Article  CAS  PubMed  Google Scholar 

  • Cuong ND, Nicolaisen MH, Sørensen J, Olsson S (2011) Hyphae-colonizing Burkholderia sp.- a new source of biological control agents against sheath blight disease (Rhizoctonia solani AG1-IA) in rice. Microb Ecol 62:425–434

    Article  PubMed  Google Scholar 

  • Dan M, Marien GJ, Goldsand G (1984) Endocarditis caused by Staphylococcus warneri on a normal aortic valve following vasectomy. Can Med Assoc J 131:211–213

    PubMed Central  CAS  PubMed  Google Scholar 

  • Edwards U, Rogall T, Blocker H, Emde M, Bottger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato Y, Morisaki H, Mitsui H, Minamisawa K (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant Nutr 46:617–629

    Article  Google Scholar 

  • Engelhard M, Hurek T, Reinhold-Hurek B (2000) Preferential occurrence of diazotrophic endophytes, Azoarcus spp., in wild rice species and land races of Oryza sativa in comparison with modern races. Environ Microbiol 2:131–141

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Shen D, Song W (2006) Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates. J Appl Microbiol 100:938–945

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Huang YD, Higashitani A, Nishimura Y, Iyama S, Hirota Y, Yoneyama Y, Dixon RA (1987) Effect of inoculation with Klebsiella oxytoca and Enterobacter cloacea on dinitrogen fixation by rice-bacteria associations. Plant Soil 103:221–226

    Article  CAS  Google Scholar 

  • Grimont PAD, Grimont F, Farmer JJ III, Asbury MA (1981) Cedecea davisae gen. nov., sp. nov. and Cedecea lapagei sp. nov., new Enterobacteriaceae from clinical specimens. Int J Syst Bacteriol 31:317–326

    Article  Google Scholar 

  • Hallmann J, Berg G (2006) Spectrum and population dynamics of bacterial root endophytes. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes, vol 6. Springer, Berlin, pp 15–31

    Chapter  Google Scholar 

  • Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914

    Article  CAS  Google Scholar 

  • Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    Article  CAS  PubMed  Google Scholar 

  • Hardoim PR, Andreote FD, Reinhold-Hurek B, Sessitsch A, van Overbeek LS, van Elsas JD (2011a) Rice root-associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol Ecol 77:154–164

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hardoim PR, Sessitsch A, Reinhold-Hurek B, van Overbeek LS, Van E (2011b) Assessment of rice root endophytes and their potential for plant growth promotion. In: Hardoim PR (ed) Bacterial endophytes of rice – their diversity, characteristics and perspectives. Groningen University, Groningen, pp 77–100

    Google Scholar 

  • Hardoim PR, Hardoim CC, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7:e30438

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hardoim PR, Nazir R, Sessitsch A, Elhottova D, Korenblum E, van Overbeek LS, van Elsas JD (2013) The new species Enterobacter oryziphilus sp. nov. and Enterobacter oryzendophyticus sp. nov. are key inhabitants of the endosphere of rice. BMC Microbiol 13:164–176

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hartmann A, Schmid M, Van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  CAS  Google Scholar 

  • Hayward AC, Fegan N, Fegan M, Stirling GR (2010) Stenotrophomonas and Lysobacter: ubiquitous plant-associated gamma-proteobacteria of developing significance in applied microbiology. J Appl Microbiol 108:756–770

    Article  CAS  PubMed  Google Scholar 

  • Heiner CR, Hunkapiller KL, Chen SM, Glass JI, Chen EY (1998) Sequencing multimegabase-template DNA with BigDye terminator chemistry. Genome Res 8:557–561

    PubMed Central  CAS  PubMed  Google Scholar 

  • Higgins DG, Bleasby AJ, Fuchs R (1992) Clustal V: improved software for multiple sequence alignment. CABIOS 8:189–191

    CAS  PubMed  Google Scholar 

  • Hirota Y, Fujii T, Sano T, Iyama S (1978) Nitrogen fixation in the rhizosphere of rice. Nature 276:416–417

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. Univ. of Calif. Agr. Exp. Sta. Berkeley, Circular 347

  • Holt KE, Baker S, Weill FX, Holmes EC, Kitchen A, Yu J, Sangal V, Brown DJ, Coia JE, Kim DW, Choi SY, Kim SH, da Silveira WD, Pickard DJ, Farrar JJ, Parkhill J, Dougan G, Thomson NR (2012) Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet 44:1056–1059

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hurek T, Reinholdhurek B, Vanmontagu M, Kellenberger E (1994) Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J Bacteriol 176:1913–1923

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jeong H, Jeong DE, Kim SH, Song GC, Park SY, Ryu CM, Park SH, Choi SK (2012) Draft genome sequence of the plant growth-promoting bacterium Bacillus siamensis KCTC 13613T. J Bacteriol 194:4148–4149

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ji X, Lu G, Gai Y, Gao H, Lu B, Kong L, Mu Z (2010) Colonization of Morus alba L. by the plant growth-promoting and antagonistic bacterium Burkholderia cepacia strain Lu10-1. BMC Microbiol 10:243–254

    Article  PubMed Central  PubMed  Google Scholar 

  • Ji SH, Gururani MA, Chun SC (2014) Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiol Res 169:83–98

    Article  CAS  PubMed  Google Scholar 

  • Jones Junior JB (2001) Laboratory guide for conducting soil tests and plant analysis. CRC, Boca Raton, p 363

    Book  Google Scholar 

  • Kaga H, Mano H, Tanaka F, Watanabe A, Kaneko S, Morisaki H (2009) Rice seeds as sources of endophytic bacteria. Microbes Environ 24:154–162

    Article  PubMed  Google Scholar 

  • Kämpfer P, Denner EB, Meyer S, Moore ER, Busse HJ (1997) Classification of “Pseudomonas azotocolligans” Anderson 1955, 132, in the genus Sphingomonas as Sphingomonas trueperi sp. nov. Int J Syst Bacteriol 47:577–583

    Article  PubMed  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  CAS  PubMed  Google Scholar 

  • Knauth S, Hurek T, Brar D, Reinhold-Hurek B (2005) Influence of different Oryza cultivars on expression of nifH gene pools in roots of rice. Environ Microbiol 7:1725–1733

    Article  CAS  PubMed  Google Scholar 

  • Kumar G, Kanaujia N, Bafana A (2012) Functional and phylogenetic diversity of root-associated bacteria of Ajuga bracteosa in Kangra valley. Microbiol Res 167:220–225

    Article  PubMed  Google Scholar 

  • La Scola B, Birtles RJ, Mallet MN, Raoult D (1998) Massilia timonae gen. nov., sp. nov., isolated from blood of an immunocompromised patient with cerebellar lesions. J Clin Microbiol 36:2847–2852

    PubMed Central  PubMed  Google Scholar 

  • Lee S, Ka JO, Song HG (2012) Growth promotion of Xanthium italicum by application of rhizobacterial isolates of Bacillus aryabhattai in microcosm soil. J Microbiol 50:45–49

    Article  CAS  PubMed  Google Scholar 

  • Lin SY, Shen FT, Young CC (2011) Rapid detection and identification of the free-living nitrogen fixing genus Azospirillum by 16S rRNA-gene-targeted genus-specific primers. Antonie Van Leeuwenhoek 99:837–844

    Article  CAS  PubMed  Google Scholar 

  • Liu JR, Lin YD, Chang ST, Zeng YF, Wang SL (2010) Molecular cloning and characterization of an insecticidal toxin from Pseudomonas taiwanensis. J Agric Food Chem 58:12343–12349

    Article  CAS  PubMed  Google Scholar 

  • Loaces I, Ferrando L, Scavino AF (2011) Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microb Ecol 61:606–618

    Article  PubMed  Google Scholar 

  • Louden BC, Haarmann D, Lynne AM (2011) Use of blue agar CAS assay for siderophore detection. J Microbiol Bio Edu 12:51–53

    Article  Google Scholar 

  • Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Environ 23:109–117

    Article  PubMed  Google Scholar 

  • Mano H, Tanaka F, Watanabe A, Kaga H, Okunishi S, Morisaki H (2006) Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 21:86–100

    Article  Google Scholar 

  • Mano H, Tanaka F, Nakamura C, Kaga H, Morisaki H (2007) Culturable endophytic bacterial flora of the maturing leaves and roots of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 22:175–185

    Article  Google Scholar 

  • Muthukumarasamy R, Kang UG, Park KD, Jeon WT, Park CY, Cho YS, Kwon SW, Song J, Roh DH, Revathi G (2007) Enumeration, isolation and identification of diazotrophs from Korean wetland rice varieties grown with long-term application of N and compost and their short-term inoculation effect on rice plants. J Appl Microbiol 102:981–991

    CAS  PubMed  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL, Miller RH, Kenney DR (Ed.) Methods of soil analysis. Part 2 – microbiological and biochemical properties. New York: Soil Science Society of America pp 539–579. (SSA book series, 5)

  • Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY, Jin H, Guo J (2011) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways). Mol Plant Microbe Interact 24:533–542

    Article  CAS  PubMed  Google Scholar 

  • Okunishi S, Sako K, Mano H, Imamura A, Morisaki H (2005) Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa). Microbes Environ 20:168–177

    Article  Google Scholar 

  • Olivares FL, Balandi VLD, Reis VM, Baldani JI, Dobereiner J (1996) Occurrence of the endophytic diazotrophic Herbaspirillum spp. in roots, stem, and leaves, predominantly of Gramineae. Biol Fertil Soils 21:197–200

    Article  Google Scholar 

  • Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125

    Article  CAS  PubMed  Google Scholar 

  • Panhwar QA, Radziah O, Zaharah AR, Sariah M, Razi IM (2011) Role of phosphate solubilizing bacteria on rock phosphate solubility and growth of aerobic rice. J Environ Biol 32:607–612

    CAS  PubMed  Google Scholar 

  • Panhwar QA, Naher UA, Jusop S, Othman R, Latif MA, Ismail MR (2014) Biochemical and molecular characterization of potential phosphate-solubilizing bacteria in acid sulfate soils and their beneficial effects on rice growth. PLoS One 9:e97241

    Article  PubMed Central  PubMed  Google Scholar 

  • Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220

    Article  CAS  PubMed  Google Scholar 

  • Ruiza D, Agaras B, de Werra P, Wall LG, Valverde C (2011) Characterization and screening of plant probiotic traits of bacteria isolated from rice seeds cultivated in Argentina. J Microbiol 49:902–912

    Article  CAS  PubMed  Google Scholar 

  • Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, Van Overbeek L, Brar D, Van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe 25:28–36

  • Shivaji S, Chaturvedi P, Suresh K, Reddy GS, Dutt CB, Wainwright M, Narlikar JV, Bhargava PM (2006) Bacillus aerius sp. nov., Bacillus aerophilus sp. nov., Bacillus stratosphericus sp. nov. and Bacillus altitudinis sp. nov., isolated from cryogenic tubes used for collecting air samples from high altitudes. Int J Syst Evol Microbiol 56:1465–1473

    Article  CAS  PubMed  Google Scholar 

  • Stoltzfus JR, So R, Malarvithi PP, Ladha JK, de Bruijn FJ (1997) Isolation of endophytic bacteria from rice and assessment of their potential for supplying rice with biologically fixed nitrogen. Plant Soil 194:25–36

    Article  CAS  Google Scholar 

  • Sun L, Qiu F, Zhang X, Dai X, Dong X, Song W (2008) Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microb Ecol 55:415–424

    Article  CAS  PubMed  Google Scholar 

  • Suresh K, Prabagaran SR, Sengupta S, Shivaji S (2004) Bacillus indicus sp. nov., an arsenic-resistant bacterium isolated from an aquifer in West Bengal, India. Int J Syst Evol Microbiol 54:1369–1375

    Article  CAS  PubMed  Google Scholar 

  • Swings J, Van Den Mooter M, Vauterin L, Hoste B, Gillis M, Mew W, Kersters K (1990) Reclassification of the Causal Agents of Bacterial Blight (Xanthomonas campestris pv. oryzae) and Bacterial Leaf Streak (Xanthomonas campestris pv. oryzicola) of Rice as Pathovars of Xanthomonas oryzae (ex Ishiyama 1922) sp. nov., nom. rev. Int J Syst Bacteriol 40:309–311

    Article  Google Scholar 

  • Taghavi S, van der Lelie D, Hoffman A, Zhang YB, Walla MD, Vangronsveld J, Newman L, Monchy S (2010) Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet 6:e1000943

    Article  PubMed Central  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tian X, Cao L, Tan H, Han W, Chen M, Liu Y, Zhou S (2007) Diversity of cultivated and uncultivated actinobacterial endophytes in the stems and roots of rice. Microb Ecol 53:700–707

    Article  PubMed  Google Scholar 

  • Van Overbeek LS, Van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296

    Article  PubMed  Google Scholar 

  • Vandamme P, Moore ER, Cnockaert M, De Brandt E, Svensson-Stadler L, Houf K, Spilker T, Lipuma JJ (2013) Achromobacter animicus sp. nov., Achromobacter mucicolens sp. nov., Achromobacter pulmonis sp. nov. and Achromobacter spiritinus sp. nov., from human clinical samples. Syst Appl Microbiol 36:1–10

    Article  CAS  PubMed  Google Scholar 

  • Vanlaere E, Lipuma JJ, Baldwin A, Henry D, De Brandt E, Mahenthiralingam E, Speert D, Dowson C, Vandamme P (2008) Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. Int J Syst Evol Microbiol 58:1580–1590

    Article  CAS  PubMed  Google Scholar 

  • Veitch J, Kansara A, Bailey D, Kustos I (2014) Severe systemic Bacillus anthracis infection in an intravenous drug user. BMJ Case Rep 2014

  • Vincent JM (1970) A manual for the practical study of root-nodule bacteria. Blackwell Scientific Publications Ltd., Oxford, UK, ISBN: 0632064102

  • Wang LT, Tai CJ, Wu YC, Chen YB, Lee FL, Wang SL (2010) Pseudomonas taiwanensis sp. nov., isolated from soil. Int J Syst Evol Microbiol 60:2094–2098

    Article  PubMed  Google Scholar 

  • Watts D, MacBeath JR (2001) Automated fluorescent DNA sequencing on the ABI PRISM 310 genetic analyzer. Methods Mol Biol 167:153–170

    CAS  PubMed  Google Scholar 

  • Yang JH, Liu HX, Zhu GM, Pan YL, Xu LP, Guo JH (2008) Diversity analysis of antagonists from rice-associated bacteria and their application in biocontrol of rice diseases. J Appl Microbiol 104:91–104

    CAS  PubMed  Google Scholar 

  • You C, Zhou F (1989) Non-nodular endorhizospheric nitrogen fixation in wetland rice. Can J Microbiol 35:403–408

    Article  CAS  Google Scholar 

  • Young LS, Hameed A, Peng SY, Shan YH, Wu SP (2013) Endophytic establishment of the soil isolate Burkholderia sp. CC-Al74 enhances growth and P-utilization rate in maize (Zea mays L.). Appl Soil Ecol 66:40–47

    Article  Google Scholar 

  • Zhang X, Sun L, Qiu F, McLean RJ, Jiang R, Song W (2008) Rheinheimera tangshanensis sp. nov., a rice root-associated bacterium. Int J Syst Evol Microbiol 58:2420–2424

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Authors would like to thank the editor and anonymous reviewers for their constructive comments on this manuscript. Authors acknowledge Dr. Wei-An Lai for technical support. This research was funded by grants (Grant No. 100-2313-B-150-001-MY3 and 102-2321-B-150-001) from Ministry of Science and Technology, Taiwan.

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The authors declare that they have no conflict of interest.

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  1. Department of Soil and Environmental Sciences, College of Agriculture and Natural Resources, National Chung Hsing University, No.250, Kuo Kuang Road, Taichung, 40227, Taiwan

    Asif Hameed & Yu-Ting Hsieh

  2. Department of Biotechnology, College of Applied Arts and Sciences, National Formosa University, No.64, Wunhua Rd., Huwei Township, Yunlin, 632, Taiwan

    Meng-Wei Yeh, Wei-Ching Chung, Chaur-Tsuen Lo & Li-Sen Young

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  1. Asif Hameed
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Hameed, A., Yeh, MW., Hsieh, YT. et al. Diversity and functional characterization of bacterial endophytes dwelling in various rice (Oryza sativa L.) tissues, and their seed-borne dissemination into rhizosphere under gnotobiotic P-stress. Plant Soil 394, 177–197 (2015). https://doi.org/10.1007/s11104-015-2506-5

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