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Differential Impacts on Bacterial Composition and Abundance in Rhizosphere Compartments between Al-Tolerant and Al-Sensitive Soybean Genotypes in Acidic Soil

  • Wen, Zhong-Ling (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Yang, Min-Kai (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Fazal, Aliya (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Liao, Yong-Hui (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Cheng, Lin-Run (Jinhua Academy of Agricultural Sciences) ;
  • Hua, Xiao-Mei (Research Center for Soil Pollution Prevention and Control, Nanjing Institute of Environmental Sciences, MEE) ;
  • Hu, Dong-Qing (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Shi, Ji-Sen (Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University) ;
  • Yang, Rong-Wu (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Lu, Gui-Hua (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Qi, Jin-Liang (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Hong, Zhi (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Qian, Qiu-Ping (Jinhua Academy of Agricultural Sciences) ;
  • Yang, Yong-Hua (Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University)
  • 투고 : 2020.03.11
  • 심사 : 2020.05.15
  • 발행 : 2020.08.28

초록

In this study, two soybean genotypes, i.e., aluminum-tolerant Baxi 10 (BX10) and aluminumsensitive Bendi 2 (BD2), were used as plant materials and acidic red soil was used as growth medium. The soil layers from the inside to the outside of the root are: rhizospheric soil after washing (WRH), rhizospheric soil after brushing (BRH) and rhizospheric soil at two sides (SRH), respectively. The rhizosphere bacterial communities were analyzed by high-throughput sequencing of V4 hypervariable regions of 16S rRNA gene amplicons via Illumina MiSeq. The results of alpha diversity analysis showed that the BRH and SRH of BX10 were significantly lower in community richness than that of BD2, while the WRH exhibited no significant difference between BX10 and BD2. Among the three sampling compartments of the same soybean genotype, WRH had the lowest community richness and diversity while showing the highest coverage. Beta diversity analysis results displayed no significant difference for any compartment between the two genotypes, or among the three different sampling compartments for any same soybean genotype. However, the relative abundance of major bacterial taxa, specifically nitrogen-fixing and/or aluminum-tolerant bacteria, was significantly different in the compartments of the BRH and/or SRH at phylum and genus levels, indicating genotype-dependent variations in rhizosphere bacterial communities. Strikingly, as compared with BRH and SRH, the WRH within the same genotype (BX10 or BD2) always had an enrichment effect on rhizosphere bacteria associated with nitrogen fixation.

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참고문헌

  1. Vonuexkull HR, Mutert E. 1995. Global extent, development and economic-impact of acid soils. Plant Soil 171: 1-15. https://doi.org/10.1007/BF00009558
  2. Ryan PR, Shaff JE, Kochian LV. 1992. Aluminum toxicity in roots - Correlation among ionic currents, ion fluxes, and root elongation in aluminum-sensitive and aluminum-tolerant wheat cultivars. Plant Physiol. 99: 1193-1200. https://doi.org/10.1104/pp.99.3.1193
  3. Koyama H, Toda T, Yokota S, Dawair Z, Hara T. 1995. Effects of aluminum and Ph on root-growth and cell viability in Arabidopsis-Thaliana strain landsberg in hydroponic culture. Plant Cell Physiol. 36: 201-205.
  4. Kochian LV. 1995. Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Phys. 46: 237-260. https://doi.org/10.1146/annurev.pp.46.060195.001321
  5. Ryan PR, Delhaize E, Jones DL. 2001. Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant Phys. 52: 527-560. https://doi.org/10.1146/annurev.arplant.52.1.527
  6. Wei LL, Chen CR, Xu ZH. 2010. Citric acid enhances the mobilization of organic phosphorus in subtropical and tropical forest soils. Biol. Fertil. Soils 46: 765-769. https://doi.org/10.1007/s00374-010-0464-x
  7. Ma JF, Ryan PR, Delhaize E. 2001. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6: 273-278. https://doi.org/10.1016/S1360-1385(01)01961-6
  8. Cheng FX, Cao GQ, Wang XR, Zhao J, Yan XL, Liao H. 2009. Isolation and application of effective nitrogen fixation rhizobial strains on low-phosphorus acid soils in South China. Chinese Sci. Bull. 54: 412-420.
  9. Dong DF, Peng XX, Yan XL. 2004. Organic acid exudation induced by phosphorus deficiency and/or aluminium toxicity in two contrasting soybean genotypes. Physiol. Plant. 122: 190-199. https://doi.org/10.1111/j.1399-3054.2004.00373.x
  10. Yang TY, Liu GL, Li YC, Zhu SM, Zou AL, Qi JL, et al. 2012. Rhizosphere microbial communities and organic acids secreted by aluminum-tolerant and aluminum-sensitive soybean in acid soil. Biol. Fertil. Soils 48: 97-108. https://doi.org/10.1007/s00374-011-0608-7
  11. Jaeger CH, Lindow SE, Miller S, Clark E, Firestone MK. 1999. Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and Tryptophan. Appl. Environ. Microbiol. 65: 2685-2690. https://doi.org/10.1128/AEM.65.6.2685-2690.1999
  12. Berg G, Eberl L, Hartmann A. 2005. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 7: 1673-1685. https://doi.org/10.1111/j.1462-2920.2005.00891.x
  13. Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P. 2013. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64: 807-838. https://doi.org/10.1146/annurev-arplant-050312-120106
  14. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM. 2006. The role of root exudates in rhizosphere interations with plants and other organisms. Annu. Rev. Plant Biol. 57: 233-266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
  15. Paterson E, Gebbing T, Abel C, Sim A, Telfer G. 2007. Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol. 173: 600-610. https://doi.org/10.1111/j.1469-8137.2006.01931.x
  16. Aira M, Gomez-Brandon M, Lazcano C, Baath E, Dominguez J. 2010. Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol. Biochem. 42: 2276-2281. https://doi.org/10.1016/j.soilbio.2010.08.029
  17. Kondorosi E, Mergaert P, Kereszt A. 2013. A Paradigm for endosymbiotic life: Cell differentiation of rhizobium bacteria provoked by host plant factors. Annu. Rev. Microbiol. 67: 611-628. https://doi.org/10.1146/annurev-micro-092412-155630
  18. Ofek M, Voronov-Goldman M, Hadar Y, Minz D. 2014. Host signature effect on plant root-associated microbiomes revealed through analyses of resident vs. active communities. Environ. Microbiol. 16: 2157-2167. https://doi.org/10.1111/1462-2920.12228
  19. Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63: 541-556. https://doi.org/10.1146/annurev.micro.62.081307.162918
  20. Berendsen RL, Pieterse CMJ, Bakker PAHM. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17: 478-486. https://doi.org/10.1016/j.tplants.2012.04.001
  21. Berg G, Grube M, Schloter M, Smalla K. 2014. Unraveling the plant nnicrobiome: looking back and future perspectives. Front. Microbiol. 5: 148. https://doi.org/10.3389/fmicb.2014.00148
  22. Li YC, Yang TY, Zhang PP, Zou AL, Peng X, Wang LL, et al. 2012. Differential responses of the diazotrophic community to aluminum-tolerant and aluminum-sensitive soybean genotypes in acidic soil. Eur. J. Soil Biol. 53: 76-85. https://doi.org/10.1016/j.ejsobi.2012.09.004
  23. Yang T, Ding Y, Zhu Y, Li Y, Wang X, Yang R, et al. 2012. Rhizosphere bacteria induced by aluminum-tolerant and aluminumsensitive soybeans in acid soil. Plant Soil Environ. 58: 262-267. https://doi.org/10.17221/652/2011-PSE
  24. Li YL, Fan XR, Shen QR. 2008. The relationship between rhizosphere nitrification and nitrogen-use efficiency in rice plants. Plant Cell Environ. 31: 73-85. https://doi.org/10.1111/j.1365-3040.2007.01737.x
  25. Inceoglu O, Salles JF, van Overbeek L, van Elsas JD. 2010. Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl. Environ. Microbiol. 76: 3675-3684. https://doi.org/10.1128/AEM.00040-10
  26. Lu GH, Tang CY, Hua XM, Cheng J, Wang GH, Zhu YL, et al. 2018. Effects of an EPSPS-transgenic soybean line ZUTS31 on rootassociated bacterial communities during field growth. PLoS One 13: e0192008. https://doi.org/10.1371/journal.pone.0192008
  27. Wen ZL, Yang MK, Du MH, Zhong ZZ, Lu YT, Wang GH, et al. 2019. Enrichments/Derichments of root-associated bacteria related to plant growth and nutrition caused by the growth of an EPSPS-Transgenic maize line in the field. Front. Microbiol. 10: 1335. . https://doi.org/10.3389/fmicb.2019.01335
  28. Lu GH, Zhu YL, Kong LR, Cheng J, Tang CY, Hua XM, et al. 2017. Impact of a glyphosate-tolerant soybean line on the rhizobacteria, revealed by Illumina MiSeq. J. Microbiol. Biotechnol. 27: 561-572. https://doi.org/10.4014/jmb.1609.09008
  29. Kennedy K, Hall MW, Lynch MDJ, Moreno-Hagelsieb G, Neufeld JD. 2014. Evaluating bias of illumina-based bacterial 16S rRNA gene profiles. Appl. Environ. Microbiol. 80: 5717-5722. https://doi.org/10.1128/AEM.01451-14
  30. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79: 5112-5120. https://doi.org/10.1128/AEM.01043-13
  31. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6: 1621-1624. https://doi.org/10.1038/ismej.2012.8
  32. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998. https://doi.org/10.1038/nmeth.2604
  33. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200. https://doi.org/10.1093/bioinformatics/btr381
  34. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. 2010. QIIME allows analysis of highthroughput community sequencing data. Nat. Methods 7: 335-336. https://doi.org/10.1038/nmeth.f.303
  35. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing mothur: open-source, platformindependent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541. https://doi.org/10.1128/AEM.01541-09
  36. Bulgarelli D, Garrido-Oter R, Munch PC, Weiman A, Droge J, Pan Y, et al. 2015. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17: 392-403. https://doi.org/10.1016/j.chom.2015.01.011
  37. Zhou JZ, Wu LY, Deng Y, Zhi XY, Jiang YH, Tu QC, et al. 2011. Reproducibility and quantitation of amplicon sequencing-based detection. ISME J. 5: 1303-1313. https://doi.org/10.1038/ismej.2011.11
  38. Edwards J, Johnson C, Santos-Medellin C, Lurie E, Podishetty NK, Bhatnagar S, et al. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. USA 112: E911-920. https://doi.org/10.1073/pnas.1414592112
  39. Minerdi D, Fani R, Gallo R, Boarino A, Bonfante P. 2001. Nitrogen fixation genes in an endosymbiotic Burkholderia strain. Appl. Environ. Microbiol. 67: 725-732. https://doi.org/10.1128/AEM.67.2.725-732.2001
  40. Griffith JC, Lee WG, Orlovich DA, Summerfield TC. 2017. Contrasting bacterial communities in two indigenous Chionochloa (Poaceae) grassland soils in New Zealand. PLoS One 12: e0179652. https://doi.org/10.1371/journal.pone.0179652
  41. Huang SC, Wang XD, Liu X, He GH, Wu JC. 2018. Isolation, identification, and characterization of an aluminum-tolerant bacterium Burkholderia sp. SB1 from an acidic red soil. Pedosphere 28: 905-912. https://doi.org/10.1016/S1002-0160(17)60390-4
  42. Ash C, Priest FG, Collins MD. 1993. Molecular-identification of ribosomal-Rna group 3 Bacilli (Ash, Farrow, Wallbanks And Collins) using a Pcr probe test - proposal for the creation of a new genus Paenibacillus. Anton. Van Leeuwenhoek 64: 253-260. https://doi.org/10.1007/BF00873085
  43. Gardener BBM. 2004. Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94: 1252-1258. https://doi.org/10.1094/PHYTO.2004.94.11.1252
  44. Montes MJ, Mercade E, Bozal N, Guinea J. 2004. Paenibacillus antarcticus sp nov., a novel psychrotolerant organism from the Antarctic environment. Int. J. Syst. Evol. Microbiol. 54: 1521-1526. https://doi.org/10.1099/ijs.0.63078-0
  45. Jie OY, Pei ZH, Lutwick L, Dalal S, Yang LY, Cassai N, et al. 2008. Paenibacillus thiaminolyticus: A new cause of human infection, inducing bacteremia in a patient on hemodialysis. Ann. Clin. Lab. Sci. 38: 393-400.
  46. Berge O, Guinebretiere MH, Achouak W, Normand P, Heulin T. 2002. Paenibacillus graminis sp nov and Paenibacillus odorifer sp. nov., isolated from plant roots, soil and food. Int. J. Syst. Evol. Microbiol. 52: 607-616. https://doi.org/10.1099/00207713-52-2-607
  47. Valverde A, Peix A, Rivas R, Velazquez E, Salazar S, Santa-Regina I, et al. 2008. Paenibacillus castaneae sp nov., isolated from the phyllosphere of Castanea sativa Miller. Int. J. Syst. Evol. Microbiol. 58: 2560-2564. https://doi.org/10.1099/ijs.0.65663-0
  48. Achouak W, Sutra L, Heulin T, Meyer JM, Fromin N, Degraeve S, et al. 2000. Pseudomonas brassicacearum sp nov and Pseudomonas thivervalensis sp. nov., two root-associated bacteria isolated from Brassica napus and Arabidopsis thaliana. Int. J. Syst. Evol. Microbiol. 50: 9-18. https://doi.org/10.1099/00207713-50-1-9
  49. Belimov AA, Dodd IC, Safronova VI, Hontzeas N, Davies WJ. 2007. Pseudomonas brassicacearum strain Am3 containing 1- aminocyclopropane-1-carboxylate deaminase can show both pathogenic and growth-promoting properties in its interaction with tomato. J. Exp. Bot. 58: 1485-1495. https://doi.org/10.1093/jxb/erm010
  50. Busse HJ. 2016. Review of the taxonomy of the genus Arthrobacter, emendation of the genus Arthrobacter sensu lato, proposal to reclassify selected species of the genus Arthrobacter in the novel genera Glutamicibacter gen. nov., Paeniglutamicibacter gen. nov., Pseudoglutamicibacter gen. nov., Paenarthrobacter gen. nov and Pseudarthrobacter gen. nov., and emended description of Arthrobacter roseus. Int. J. Syst. Evol. Microbiol. 66: 9-37. https://doi.org/10.1099/ijsem.0.000702
  51. Yan Y, Kuramae EE, de Hollander M, Klinkhamer PGL, van Veen JA. 2017. Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere. ISME J. 11: 56-66. https://doi.org/10.1038/ismej.2016.108
  52. Apprill A, McNally S, Parsons R, Weber L. 2015. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75: 129-137. https://doi.org/10.3354/ame01753
  53. Parada AE, Needham DM, Fuhrman JA. 2016. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18: 1403-1414. https://doi.org/10.1111/1462-2920.13023
  54. Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, et al.2016. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 22: e00009-15.
  55. Snijders AM, Langley SA, Kim YM, Brislawn CJ, Noecker C, Zink EM, et al. 2017. Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome. Nat. Microbiol. 2: 16221. https://doi.org/10.1038/nmicrobiol.2016.221