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Effect of genetically modified rice producing resveratrol on the soil microbial communities

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Abstract

Cultivation of genetically modified (GM) crops has rapidly increased in the global agricultural area. However, cultivation of GM crops in the field evoked the concern of the possibility of unintentional consequences from transgenic plant into environment. In our present study, we have assessed the effects of RS526, GM rice producing resveratrol on the surrounding soil microbial community. The effects of RS526 on the soil microbial community in its field of growth were assessed using a conventional culture technique and culture-independent molecular methods. Three replicate field plots were planted with single GM rice and a non-GM counterpart, Dongjin. The soil microbial communities around these plants were compared using colony counting, denaturing gradient gel electrophoresis (DGGE), pyrosequencing analysis, and community-level physiological profiling during the growing periods. The bacterial, fungal, and actinomycetes population densities of the RS526 soils were found to be within the range of those of the non-GM rice cultivar. The DGGE banding patterns of the GM and non-GM soils were also similar, suggesting that the bacterial community structures were stable within a given month and were unaffected by the presence of a GM plant. The data obtained from pyrosequencing analysis showed that the bacterial community distribution at the phylum level were highly similar to DGGE patterns between two tested groups. The substrate utilization pattern of RS526 and Dongjin rice soil was quite similar between each sampling time. These results indicate that soil microbial communities are not significantly affected by the cultivation of RS526 within the experimental time frame.

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References

  • Ahn JH, Kim MC, Shin HC, Choi MK, Yoon SS, Kim TS, Song HG, Lee GH, Ka JO (2006) Improvement of PCR amplification bias for community structure analysis of soil bacteria by denaturing gradient gel electrophoresis. J Microbiol Biotechnol 16(10):1561–1569

    CAS  Google Scholar 

  • Ahrenholtz I, Harms K, de Vries J, Wackernagel W (2000) Increased killing of Bacillus subtilis on the hair roots of transgenic T4 lysozyme-producing potatoes. Appl Environ Microbiol 66:1862–1865

    Article  CAS  Google Scholar 

  • Baek SH, Shin WC, Ryu HS, Lee DW, Moon E, Seo CS, Hwang E, Lee HS, Ahn MH, Jeon Y, Kang HJ, Lee SW, Kim SY, D’Souza R, Kim HJ, Hong ST, Jeon JS (2013) Creation of resveratrol-enriched rice for the treatment of metabolic syndrome and related diseases. PLoS One 8(3):e57930. doi:10.1371/journal.pone.0057930

    Article  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  Google Scholar 

  • Barriuso J, Valverde JR, Mellado RP (2012) Effect of Cry1Ab protein on rhizobacterial communities of Bt-maize over a four-year cultivation period. PLoS One 7(4):e35481

    Article  CAS  Google Scholar 

  • Baumgarte S, Tebbe CC (2005) Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810), and its effect on bacterial communities in the maize rhizosphere. Mol Ecol 14:2539–2551

    Article  CAS  Google Scholar 

  • Becker R, Ulrich A, Hedtke C, Hornermeier B (2001) Einfluss des Anbaus von transgenem herbizidresistentem Raps auf das Agrar-O¨ kosystem. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 44:159–167

    Article  Google Scholar 

  • Becker R, Behrendt U, Hommel B, Kropf S, Ulrich A (2008) Effects of transgenic fructan-producing potatoes on the community structure of rhizosphere and phyllosphere bacteria. FEMS Microbiol Ecol 66:411–425

    Article  CAS  Google Scholar 

  • Brusetti L, Francia P, Bertolini C, Pagliuca A, Borin S, Sorlini S, Abruzzese A, Sacchi G, Viti C, Giovannetti L, Giuntini E, Bazzicalupa M, Daffonchio D (2004) Bacterial communities associated with the rhizosphere of transgenic Bt 176 maize (Zea mays) and its non-transgenic counterpart. Plant Soil 266:11–21

    Article  CAS  Google Scholar 

  • Brussard L, Behan-Pelletier VM, Bignell DE, Brown VK, Didden WAM, Folgarait PJ, Fragoso C, Freckman DW, Gupta VVSR, Hattori T, Hawksworth DL, Klopatek C, Lavelle P, Malloch D, Rusek J, Soderstrom B, Tiedje JM, Virginia RA (1997) Biodiversity and ecosystem functioning in soil. Ambio 26:563–570

    Google Scholar 

  • Bujanda L, Hijona E, Larzabal M, Beraza M, Aldazabal P, García-Urkia N, Saraqueta C, Cosme A, Irastorza B, González A, Arenas JI (2008) Resveratrol inhibits nonalcoholic fatty liver disease in rats. BMC Gastroenterol 8:40–48

    Article  Google Scholar 

  • Clark MS, Smith MS, Doran JW (1998) Changes in soil chemical properties resulting from organic and low-input farming practices. Agron J 90:662–671

    Article  Google Scholar 

  • Creasy LL, Coffee M (1988) Phytoalexin production potential of grape berries. J Am Soc Hortic Sci 113:230–234

    CAS  Google Scholar 

  • Dunfield KE, Germida JJ (2003) Seasonal changes in the rhizosphere microbial communities associated with field-grown genetically modified canola (Brassica napus). Appl Environ Microbiol 69:7310–7318

    Article  CAS  Google Scholar 

  • Fang H, Dong B, Yan H, Tang F, Wang B, Yu Y (2012) Effect of vegetation of transgenic Bt rice lines and their straw amendment on soil enzymes, respiration, functional diversity and community structure of soil microorganisms under field conditions. J Environ Sci 24:1259–1270

    Article  CAS  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon source utilization. Appl Environ Microbiol 57:2351–2358

    CAS  Google Scholar 

  • Graner G, Persson P, Meijer J, Alström S (2003) A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett 224:269–276

    Article  CAS  Google Scholar 

  • Guarente L, Picard F (2005) Calorie restriction—the SIR2 connection. Cell 120:473–482

    Article  CAS  Google Scholar 

  • Gupta VVSR, Roberts G, Putcha S (2000) Soil health: the role of microbes in crop productivity. In: Proceedings of the 10th Australian cotton conference held during August 2000 at Brisbane, Australia, pp 639–643

  • Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

    Article  CAS  Google Scholar 

  • Hamedy M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27

    Article  Google Scholar 

  • Houlden A, Timms-Wilson TM, Day MJ, Bailey MJ (2008) Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiol Ecol 65:193–201

    Article  CAS  Google Scholar 

  • Hur MS, Kim YH, Song HR, Kim JM, Choi YI, Yi HN (2011) Effect of genetically modified poplars on soil microbial communities during the phytoremediation of waste mine tailings. Appl Environ Microbiol 77(21):7611–7619

    Article  CAS  Google Scholar 

  • Icoz I, Stotzky G (2008) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biol Biochem 40:559–586

    Article  CAS  Google Scholar 

  • Jeandel P, Bessis R, Gautheron B (1991) The production of resveratrol (3,5,4¢-trihydroxystilbene) by grape berries in different developmental stages. Am J Enol Vitic 42:41–46

    Google Scholar 

  • Khodakovskaya MV, Kim BS, Kim JN, Alimohammadi M, Dervishi E, Mustafa T, Cernigla CE (2013) Carbon nanotubes as plant growth regulators: effects on tomato growth, reproductive system, and soil microbial community. Small 9(1):115–123

    Article  CAS  Google Scholar 

  • Koskella J, Stotzky G (1997) Microbial utilization of free and clay bound insecticidal toxins from Bacillus thuringiensis and their retention of insecticidal activity after incubation with microbes. Appl Environ Microbiol 63:3561–3568

    CAS  Google Scholar 

  • Langcake P, Cornford CA, Pryce RJ (1979) Identification of pterostilbene as a phytoalexin from Vitis vinifera leaves. Phytochemistry 18:1025–1027

    Article  CAS  Google Scholar 

  • Lee JH, Yi H, Jeon YS, Won S, Chun J (2012) TBC: a clustering algorithm based on prokaryotic taxonomy. J Microbiol 50:181–185

    Article  Google Scholar 

  • Lockwood JL, Filonow AB (1981) Responses of fungi to nutrient-limiting conditions and to inhibitory substances in natural habitats. Adv Microb Ecol 5:1–62

    Article  CAS  Google Scholar 

  • Markus MA, Morris BJ (2008) Resveratrol in prevention and treatment of common clinical conditions of aging. Clin Interv Aging 3:331–339

    CAS  Google Scholar 

  • Meng Y, Ma Q-Y, Kou X-P, Xu J (2005) Effect of resveratrol on activation of nuclear factor kappa-B and inflammatory factors in rat model of acute pancreatitis. World J Gastroenterol 11(4):525–528

    Article  CAS  Google Scholar 

  • Mikstacka R, Rimando AM, Ignatowicz E (2010) Antioxidant effect of trans-resveratrol, pterostilbene, Quercetin and their combination in human erythrocytes in vitro. Plant Food Hum Nutr 65:57–63

    Article  CAS  Google Scholar 

  • Milling A, Smalla K, Maidl FX, Schloter M, Munch JC (2004) Effects of transgenic potatoes with an altered starch composition on the diversity of soil and rhizosphere bacteria and fungi. Plant Soil 266:23–39

    Article  CAS  Google Scholar 

  • Mulder C, Wouterse M, Raubuch M, Roelofs W, Rutgers M (2006) Can transgenic maize affect soil microbial communities? PLoS Comput Biol 2:1165–1172

    CAS  Google Scholar 

  • NIAST (2000) Methods of soil chemical analysis. National Institute of Agricultural Science and Technology, RDA, Suwon

    Google Scholar 

  • Oger P, Petit A, Dessaux Y (1997) Genetically engineered plants producing opines alter their biological environment. Nat Biotechnol 15:369–372

    Article  CAS  Google Scholar 

  • Oger P, Mansouri H, Dessaux Y (2000) Effect of crop rotation and soil cover on alteration of the soil microflora generated by the culture of transgenic plants producing opines. Mol Ecol 9:881–890

    Article  CAS  Google Scholar 

  • Qin Y, Kim SM, Ahn HI, Lee JH, Baek SO, Shin KS, Woo HJ, Cho HS, Kweon SJ, Lim MH (2013) Bioassay for the response of resveratrol transgenic rice lines to bacterial and fungal diseases. Plant Breed Biotechnol 1:253–261

    Article  Google Scholar 

  • Rui E, Moura PR, Gonçalves Kde A, Kobarg J (2005) Expression and spectroscopic analysis of a mutant hepatitis B virus onco-protein HBx without cysteine residues. J Virol Methods 126:65–74

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • Schmalenberger A, Tebbe CC (2002) Bacterial community composition in the rhizosphere of a transgenic, herbicide-resistant maize (Zea mays) and comparison to its non-transgenic cultivar Bosphore. FEMS Microbiol Ecol 40:29–37

    Article  CAS  Google Scholar 

  • Sessitsch A, Kan FY, Pfeifer U (2003) Diversity and community structure of culturable Bacillus spp. populations in the rhizospheres of transgenic potatoes expressing the lytic peptide cecropin B. Appl Soil Ecol 22:149–158

    Article  Google Scholar 

  • Sessitsch A, Coenye T, Sturz AV, Vandamme P, Ait Barka E, Salles JF, Van Elsas JD, Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signaling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240

    Article  Google Scholar 

  • Shen RF, Cai H, Gong WH (2006) Transgenic Bt cotton has no apparent effect on enzymatic activities or functional diversity of microbial communities in rhizosphere soil. Plant Soil 285:149–159

    Article  CAS  Google Scholar 

  • Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signaling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240

    Article  CAS  Google Scholar 

  • Spence C, Alff E, Hohnson C, Ramos C, Donofrio N, Sundaresan V, Bais H (2014) Natural rice rhizosphere microbes suppress rice blast infections. BMC Plant Biol 14:30

    Article  Google Scholar 

  • Stotzky G (2004) Persistence and biological activity in soil of the insecticidal proteins from Bacillus thuringiensis, especially from transgenic plants. Plant Soil 266:77–89

    Article  CAS  Google Scholar 

  • Tesfayeam M, Dufault NS, Dornbusch MR, Allan DL, Vance CP, Samac DA (2003) Influence of enhanced malate dehydrogenase expression by alfalfa on diversity of rhizobacteria and soil nutrient availability. Soil Biol Biochem 35:1103–1113

    Article  Google Scholar 

  • Wei M, Tan F, Zhu H, Cheng K, Wu X, Wang J, Zhao K, Tang X (2012) Impact of Bt-transgenic rice (SHK601) on soil ecosystems in the rhizosphere during crop development. Plant Soil Environ 58(5):217–223

    CAS  Google Scholar 

Download references

Acknowledgments

This study was carried out with the support of “Research Program for Agricultural Science & Technology Development (Project No. PJ009609032015)”, National Academy of Agricultural Science, Rural Development Administration, Republic of Korea.

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Authors and Affiliations

  1. Department of Biosafety, National Academy of Agricultural Science, 370 Nongsaengmyeong-ro, Wansan-gu, Jeonju-si, Jeollabuk-do, 560-500, Republic of Korea

    Soo-In Sohn, Soon-Jong Kweon, Hyun-Suk Cho & Tae-Hoon Ryu

  2. Institute for Future Environmental Ecology Co., Ltd., 5 Palbok 1-gil, Deokjin-gu, Jeonju-si, Jeollabuk-do, 561-842, Republic of Korea

    Young-Ju Oh

  3. ChunLab, Inc., Seoul National University, 1 Gwanak-ro, Gwank-gu, Seoul, 151-742, Republic of Korea

    Byung-Yong Kim

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  1. Soo-In Sohn
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  2. Young-Ju Oh
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  3. Byung-Yong Kim
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  4. Soon-Jong Kweon
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  5. Hyun-Suk Cho
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Correspondence to Soo-In Sohn.

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Sohn, SI., Oh, YJ., Kim, BY. et al. Effect of genetically modified rice producing resveratrol on the soil microbial communities. J Korean Soc Appl Biol Chem 58, 795–805 (2015). https://doi.org/10.1007/s13765-015-0106-y

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