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Impact of a Glyphosate-Tolerant Soybean Line on the Rhizobacteria, Revealed by Illumina MiSeq

  • Lu, Gui-Hua (NJU-NJFU Joint Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Zhu, Yin-Ling (NJU-NJFU Joint Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Kong, Ling-Ru (NJU-NJFU Joint Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Cheng, Jing (NJU-NJFU Joint Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Tang, Cheng-Yi (NJU-NJFU Joint Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Hua, Xiao-Mei (Nanjing Institute of Environmental Sciences, MEP) ;
  • Meng, Fan-Fan (Jilin Academy of Agricultural Sciences) ;
  • Pang, Yan-Jun (NJU-NJFU Joint Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Yang, Rong-Wu (NJU-NJFU Joint Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Qi, Jin-Liang (NJU-NJFU Joint Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University) ;
  • Yang, Yong-Hua (NJU-NJFU Joint Institute for Plant Molecular Biology, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University)
  • Received : 2016.09.07
  • Accepted : 2016.12.14
  • Published : 2017.03.28

Abstract

The global commercial cultivation of transgenic crops, including glyphosate-tolerant soybean, has increased widely in recent decades with potential impact on the environment. The bulk of previous studies showed different results on the effects of the release of transgenic plants on the soil microbial community, especially rhizosphere bacteria. In this study, comparative analyses of the bacterial communities in the rhizosphere soils and surrounding soils were performed between the glyphosate-tolerant soybean line NZL06-698 (or simply N698), containing a glyphosate-insensitive EPSPS gene, and its control cultivar Mengdou12 (or simply MD12), by a 16S ribosomal RNA gene (16S rDNA) amplicon sequencing-based Illumina MiSeq platform. No statistically significant difference was found in the overall alpha diversity of the rhizosphere bacterial communities, although the species richness and evenness of the bacteria increased in the rhizosphere of N698 compared with that of MD12. Some influence on phylogenetic diversity of the rhizosphere bacterial communities was found between N698 and MD12 by beta diversity analysis based on weighted UniFrac distance. Furthermore, the relative abundances of part rhizosphere bacterial phyla and genera, which included some nitrogen-fixing bacteria, were significantly different between N698 and MD12. Our present results indicate some impact of the glyphosate-tolerant soybean line N698 on the phylogenetic diversity of rhizosphere bacterial communities together with a significant difference in the relative abundances of part rhizosphere bacteria at different classification levels as compared with its control cultivar MD12, when a comparative analysis of surrounding soils between N698 and MD12 was used as a systematic contrast study.

Keywords

References

  1. James C. 2015. Global status of commercialized biotech/GM crops: 2014. China Biotechnol. 35: 1-14.
  2. Padgette SR, Kolacz KH, Delannay X, Re DB, Lavallee BJ, Tinius CN, et al. 1995. Development, identification, and characterization of a glyphosate-tolerant soybean line. Crop Sci. 35: 1451-1461. https://doi.org/10.2135/cropsci1995.0011183X003500050032x
  3. 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
  4. 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
  5. 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
  6. 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. https://doi.org/10.1111/j.1574-6941.2009.00654.x
  7. 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
  8. 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
  9. 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
  10. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, et al. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl. Acad. Sci. USA 110: 6548-6553. https://doi.org/10.1073/pnas.1302837110
  11. Liang JG, Sun S, Ji J, Wu HY, Meng F, Zhang MR, et al. 2014. Comparison of the rhizosphere bacterial communities of zigongdongdou soybean and a high-methionine transgenic line of this cultivar. PLoS One 9: e103343. https://doi.org/10.1371/journal.pone.0103343
  12. Dunfield KE, Germida JJ. 2004. Impact of genetically modified crops on soil-and plant-associated microbial communities. J. Environ. Qual. 33: 806-815. https://doi.org/10.2134/jeq2004.0806
  13. Liu B, Zeng Q, Yan FM, Xu HG, Xu CR. 2005. Effects of transgenic plants on soil microorganisms. Plant Soil 271: 1-13. https://doi.org/10.1007/s11104-004-1610-8
  14. Turrini A, Sbrana C, Giovannetti M. 2015. Belowground environmental effects of transgenic crops: a soil microbial perspective. Res. Microbiol. 166: 121-131. https://doi.org/10.1016/j.resmic.2015.02.006
  15. Gans J, Wolinsky M, Dunbar J. 2005. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309: 1387-1390. https://doi.org/10.1126/science.1112665
  16. Inceoglu O, Abu Al-Soud W, Salles JF, Semenov AV, van Elsas JD. 2011. Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLoS One 6: e23321. https://doi.org/10.1371/journal.pone.0023321
  17. Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, et al. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488: 91-95. https://doi.org/10.1038/nature11336
  18. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, et al. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86-90. https://doi.org/10.1038/nature11237
  19. Schlaeppi K, Dombrowski N, Oter RG, van Themaat EVL, Schulze-Lefert P. 2014. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc. Natl. Acad. Sci. USA 111: 585-592. https://doi.org/10.1073/pnas.1321597111
  20. 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
  21. Schmidt PA, Balint M, Greshake B, Bandow C, Rombke J, Schmitt I. 2013. Illumina metabarcoding of a soil fungal community. Soil Biol. Biochem. 65: 128-132. https://doi.org/10.1016/j.soilbio.2013.05.014
  22. Bakker MG, Chaparro JM, Manter DK, Vivanco JM. 2015. Impacts of bulk soil microbial community structure on rhizosphere microbiomes of Zea mays. Plant Soil 392: 115-126. https://doi.org/10.1007/s11104-015-2446-0
  23. Yang CY, Li Y, Zhou B, Zhou YY, Zheng W, Tian Y, et al. 2015. Illumina sequencing-based analysis of free-living bacterial community dynamics during an Akashiwo sanguine bloom in Xiamen sea, China. Sci. Rep. 5: 8476. https://doi.org/10.1038/srep08476
  24. 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-E920. https://doi.org/10.1073/pnas.1414592112
  25. 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
  26. Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J. 2014. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the illumina MiSeq platform. Microbiome 2: article 6.
  27. Magoc T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 2957-2963. https://doi.org/10.1093/bioinformatics/btr507
  28. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998. https://doi.org/10.1038/nmeth.2604
  29. Cole JR, Wang Q, Fish JA, Chai BL, McGarrell DM, Sun YN, et al. 2014. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42: D633-D642. https://doi.org/10.1093/nar/gkt1244
  30. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72: 5069-5072. https://doi.org/10.1128/AEM.03006-05
  31. Chen H, Boutros PC. 2011. VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics 12: 35. https://doi.org/10.1186/1471-2105-12-35
  32. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541. https://doi.org/10.1128/AEM.01541-09
  33. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7: 335-336. https://doi.org/10.1038/nmeth.f.303
  34. Zhou J, Wu L, Deng Y, Zhi X, Jiang YH, Tu Q, et al. 2011. Reproducibility and quantitation of amplicon sequencingbased detection. ISME J. 5: 1303-1313. https://doi.org/10.1038/ismej.2011.11
  35. White JR, Nagarajan N, Pop M. 2009. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput. Biol. 5: e1000352. https://doi.org/10.1371/journal.pcbi.1000352
  36. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57: 289-300.
  37. Weaver MA, Krutz LJ, Zablotowicz RM, Reddy KN. 2007. Effects of glyphosate on soil microbial communities and its mineralization in a Mississippi soil. Pest Manag. Sci. 63: 388-393. https://doi.org/10.1002/ps.1351
  38. Kremer RJ, Means NE. 2009. Glyphosate and glyphosateresistant crop interactions with rhizosphere microorganisms. Eur. J. Agron. 31: 153-161. https://doi.org/10.1016/j.eja.2009.06.004
  39. Wang Z, Liu ZH, Wang HY. 2012. Salinization resistance transgenic soybean reduced bacterial diversity in rhizosphere. Adv. Intel. Soft. Comput. 134: 377-384.
  40. Nakatani AS, Fernandes MF, de Souza RA, da Silva AP, dos Reis FB, Mendes IC, Hungria M. 2014. Effects of the glyphosate-resistance gene and of herbicides applied to the soybean crop on soil microbial biomass and enzymes. Field Crops Res. 162: 20-29. https://doi.org/10.1016/j.fcr.2014.03.010
  41. Arango L, Buddrus-Schiemann K, Opelt K, Lueders T, Haesler F, Schmid M, et al. 2014. Effects of glyphosate on the bacterial community associated with roots of transgenic Roundup Ready (R) soybean. Eur. J. Soil Biol. 63: 41-48. https://doi.org/10.1016/j.ejsobi.2014.05.005
  42. Newman MM, Hoilett N, Lorenz N, Dick RP, Liles MR, Ramsier C, Kloepper JW. 2016. Glyphosate effects on soil rhizosphere-associated bacterial communities. Sci. Total Environ. 543: 155-160. https://doi.org/10.1016/j.scitotenv.2015.11.008
  43. Siciliano SD, Germida JJ. 1999. Taxonomic diversity of bacteria associated with the roots of field-grown transgenic Brassica napus cv. Quest, com pared to the non-transgenic B. napus cv. Excel and B. rapa cv. Parkland. FEMS Microbiol. Ecol. 29: 263-272. https://doi.org/10.1111/j.1574-6941.1999.tb00617.x
  44. Dunfield KE, Germida JJ. 2001. Diversity of bacterial communities in the rhizosphere and root interior of fieldgrown genetically modified Brassica napus. FEMS Microbiol. Ecol. 38: 1-9. https://doi.org/10.1111/j.1574-6941.2001.tb00876.x
  45. Dunfield KE, Germida JJ. 2003. Seasonal changes in the rhizosphere microbial communities associated with fieldgrown genetically modified canola (Brassica napus). Appl. Environ. Microbiol. 69: 7310-7318. https://doi.org/10.1128/AEM.69.12.7310-7318.2003
  46. Jin J, Wang GH, Liu XB, Liu JD, Chen XL, Herbert SJ. 2009. Temporal and spatial dynamics of bacterial community in the rhizosphere of soybean genotypes grown in a black soil. Pedosphere 19: 808-816. https://doi.org/10.1016/S1002-0160(09)60176-4
  47. Xu YX, Wang GH, Jin J, Liu JJ, Zhang QY, Liu XB. 2009. Bacterial communities in soybean rhizosphere in response to soil type, soybean genotype, and their growth stage. Soil Biol. Biochem. 41: 919-925. https://doi.org/10.1016/j.soilbio.2008.10.027
  48. Li CG, Li XM, Kong WD, Wu Y, Wang JG. 2010. Effect of m onoculture s oybean o n soil m icrobial c omm unity in t he Northeast China. Plant Soil 330: 423-433. https://doi.org/10.1007/s11104-009-0216-6
  49. Yang T, Liu G, Li Y, Zhu S, Zou A, Qi J, Yang Y. 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
  50. 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
  51. Masson-Boivin C, Giraud E, Perret X, Batut J. 2009. Establishing nitrogen-fixing symbiosis with legumes: how many Rhizobium recipes? Trends Microbiol. 17: 458-466. https://doi.org/10.1016/j.tim.2009.07.004
  52. Berg G, Grube M, Schloter M, Smalla K. 2014. Unraveling the plant microbiome: looking back and future perspectives. Front. Microbiol. 5: article 148.
  53. Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB, et al. 2009. The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat. Rev. Microbiol. 7: 514-525. https://doi.org/10.1038/nrmicro2163
  54. Chen Y, Duan R, Li X, Li K, Liang J, Liu C, et al. 2015. Homology analysis and cross-immunogenicity of OmpA from pathogenic Yersinia enterocolitica, Yersinia pseudotuberculosis and Yersinia pestis. Mol. Immunol. 68: 290-299. https://doi.org/10.1016/j.molimm.2015.09.016
  55. Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, et al. 2009. Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl. Environ. Microbiol. 75: 748-757. https://doi.org/10.1128/AEM.02239-08
  56. Muller H, Furnkranz M, Grube M, Berg G. 2013. Genome sequence of Serratia plymuthica strain S13, an endophyte with germination-and plant-growth-promoting activity from the flower of Styrian oil pumpkin. Genome Announc. 1: e00594.
  57. Tang CY, Yang MK, Wu FY, Zhao H, Pang YJ, Yang RW, et al. 2015. Identification of miRNAs and their targets in transgenic Brassica napus and its acceptor (Westar) by highthroughput sequencing and degradome analysis. RSC Adv. 5: 85383-85394. https://doi.org/10.1039/C5RA14672K
  58. Lin WY, Huang TK, Chiou TJ. 2 013. Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell 25: 4061-4074. https://doi.org/10.1105/tpc.113.116012

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