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Biology and Fertility of Soils

, Volume 48, Issue 4, pp 453–461 | Cite as

Two-year field study shows little evidence that PPO-transgenic rice affects the structure of soil microbial communities

  • Young Jin Chun
  • Hyo-Jeong Kim
  • Kee Woong Park
  • Soon-Chun Jeong
  • Bumkyu Lee
  • Kyoungwhan Back
  • Hwan Mook KimEmail author
  • Chang-Gi KimEmail author
Short Communication

Abstract

There is global concern about the environmental consequences associated with transgenic crops. Their effects on the soil ecosystem are of special interest when assessing ecological safety and integrity. Although many efforts have been made to develop crops genetically modified to have resistance to protoporphyrin oxidase (PPO)-inhibiting herbicides, little is known about their influence on soil microbial communities. We conducted a 2-year field study and an analysis via terminal restriction fragment length polymorphism (T-RFLP) to assess the impacts of PPO-transgenic rice on bacterial and fungal communities. In the first year we sampled the rhizosphere and surrounding bulk soil, while in the second year we sampled rhizosphere soil only. No differences were observed in the diversity indices and community composition of microbial communities between transgenic rice and its parental non-transgenic counterpart (cultivar Dongjin). Instead, community variation was strongly dependent on growth stage and year. Therefore, we observed no adverse effects by these crops of modified rice on the microbial community composition in paddy soils.

Keywords

Protoporphyrin oxidase Rice Soil microbial community T-RFLP Transgenic crop 

Notes

Acknowledgments

This research was supported by grants from the KRIBB Research Initiative Program, the National Research Foundation of Korea (NRF) funded by MEST (No. 20110028162), and the Next-Generation BioGreen 21 Program (No. PJ008008012011), Rural Development Administration, Republic of Korea.

References

  1. Abdo Z, Schuette UME, Bent SJ, Williams CJ, Forney LJ, Joyce P (2006) Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8:929–938. doi: 10.1111/j.1462-2920.2005.00959.x PubMedCrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi: 10.1111/j.1442-9993.2001.01070.pp.x Google Scholar
  3. Anderson MJ (2005) PerMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand http://www.stat.auckland.ac.nz/~mja/prog/
  4. Beale SI, Weinstein JD (1990) Tetrapyrrole metabolism in photosynthetic organisms. In: Dailey HA (ed) Biosynthesis of hemes and chlorophylls. McGraw-Hill, New York, pp 287–391Google Scholar
  5. Beare MH, Coleman DC, Crossley DA, Hendrix PF, Odum EP (1995) A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling. Plant Soil 170:5–22. doi: 10.1007/BF02183051 CrossRefGoogle Scholar
  6. Blackwood CB, Buyer JS (2004) Soil microbial communities associated with Bt and non-Bt corn in three soils. J Environ Qual 33:832–836. doi: 10.2134/jeq2004.0832 PubMedCrossRefGoogle Scholar
  7. Bradley KL, Hancock JE, Giardina CP, Pregitzer KS (2007) Soil microbial community responses to altered lignin biosynthesis in Populus tremuloides vary among three distinct soils. Plant Soil 294:185–201. doi: 10.1007/s11104-007-9246-0 CrossRefGoogle Scholar
  8. Bray JR, Curtis JT (1957) An ordination of the upland forest communities in southern Wisconsin. Ecol Monogr 27:325–349. doi: 10.2307/1942268 CrossRefGoogle Scholar
  9. Choi KW, Han O, Lee HJ, Yun YC, Moon YH, Kim M, Kuk YI, Han SU, Guh JO (1998) Generation of resistance to the diphenyl ether herbicide, oxyfluorfen, via expression of the Bacillus subtilis protoporphyrinogen oxidase gene in transgenic tobacco plants. Biosci Biotechnol Biochem 62:558–560. doi: 10.1271/bbb.62.558 CrossRefGoogle Scholar
  10. Cowgill SE, Bardgett RD, Kiezebrink DT, Atkinson HJ (2002) The effect of transgenic nematode resistance on non-target organisms in the potato rhizosphere. J Appl Ecol 39:915–923. doi: 10.1046/j.1365-2664.2002.00774.x CrossRefGoogle Scholar
  11. Dailey HA, Dailey TA (1996) Protoporphyrinogen oxidase of Myxococcus xanthus: expression, purification, and characterization of the cloned enzyme. J Biol Chem 271:8714–8718. doi: 10.1074/jbc.271.15.8714 PubMedCrossRefGoogle Scholar
  12. Daugrois JH, Hoy JW, Griffin JL (2005) Protoporphyrinogen oxidase inhibitor herbicide effects on Pythium root rot of sugarcane, Pythium species, and the soil microbial community. Phytopathology 95:220–226. doi: 10.1094/PHYTO-95-0220 PubMedCrossRefGoogle Scholar
  13. Dayan FE, Duke SO (1997) Phytotoxicity of protoporphyrinogen oxidase inhibitors: phenomenology, mode of action and mechanisms of resistance. In: Roe RM, Burton JD, Kuhr RJ (eds) Herbicide activity: toxicology, biochemistry and molecular biology. IOS, Washington, DC, pp 11–35Google Scholar
  14. de Vries J, Wackernagel W (2004) Microbial horizontal gene transfer and the DNA release from transgenic crop plants. Plant Soil 266:91–104. doi: 10.1007/s11104-005-4783-x CrossRefGoogle Scholar
  15. Devare MH, Jones CM, Thies JE (2004) Effect of Cry3Bb transgenic corn and tefluthrin on the soil microbial community: biomass, activity, and diversity. J Environ Qual 33:837–843. doi: 10.2134/jeq2004.0837 PubMedCrossRefGoogle Scholar
  16. Devare M, Londoño-R LM, Thies JE (2007) Neither transgenic Bt maize (MON863) nor tefluthrin insecticide adversely affect soil microbial activity or biomass: a 3-year field analysis. Soil Biol Biochem 39:2038–2047. doi: 10.1016/j.soilbio.2007.03.004 CrossRefGoogle Scholar
  17. Donegan KK, Seidler RJ, Doyle JD, Porteous LA, Di Giovanni G, Widmers F (1999) A field study with genetically engineered alfalfa inoculated with recombinant Sinorhizobium meliloti: effects on the soil ecosystem. J Appl Ecol 36:920–936. doi: 10.1046/j.1365-2664.1999.00448.x CrossRefGoogle Scholar
  18. Duke SO, Lydon J, Becerril JM, Sherman TD, Lehnen LP, Matsumoto H (1991) Protoporphyrinogen oxidase-inhibiting herbicides. Weed Sci 39:465–473, JSTOR / ChemPortGoogle Scholar
  19. Dunfield KE, Germida JJ (2001) Diversity of bacterial communities in the rhizosphere and root interior of field-grown genetically modified Brassica napus. FEMS Microbiol Ecol 38:1–9. doi: 10.1016/S0168-6496(01)00167-2 CrossRefGoogle Scholar
  20. 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. doi: 10.1128/AEM.69.12.7310-7318.2003 PubMedCrossRefGoogle Scholar
  21. Dunfield KE, Germida JJ (2004) Impact of genetically modified crops on soil- and plant-associated microbial communities. J Environ Qual 33:806–815. doi: 10.2134/jeq2004.0806 PubMedCrossRefGoogle Scholar
  22. Gebhard F, Smalla K (1999) Monitoring field releases of genetically modified sugar beets for persistence of transgenic plant DNA and horizontal gene transfer. FEMS Microbiol Ecol 28:261–272. doi: 10.1016/S0168-6496(98)00115-9 CrossRefGoogle Scholar
  23. Griffiths BS, Caul S, Thompson J, Birch ANE, Scrimgeour C, Cortet J, Foggo A, Hackett CA, Krogh PH (2006) Soil microbial and faunal community responses to Bt maize and insecticide in two soils. J Environ Qual 35:734–741. doi: 10.2134/jeq2005.0344 PubMedCrossRefGoogle Scholar
  24. Griffiths BS, Heckmann L-H, Caul S, Thompson J, Scrimgeour C, Krogh PH (2007) Varietal effects of eight paired lines of transgenic Bt maize and near-isogenic non-Bt maize on soil microbial and nematode community structure. Plant Biotechnol J 5:60–68. doi: 10.1111/j.1467-7652.2006.00215.x PubMedCrossRefGoogle Scholar
  25. Gschwendtner S, Reichmann M, Müller M, Radl V, Munch JC, Schloter M (2010) Effects of genetically modified amylopectin-accumulating potato plants on the abundance of beneficial and pathogenic microorganisms in the rhizosphere. Plant Soil 335:413–422. doi: 10.1007/s11104-010-0430-2 CrossRefGoogle Scholar
  26. Gyamfi S, Pfeifer U, Stierschneider M, Sessitsch A (2002) Effects of transgenic glufosinate-tolerant oilseed rape (Brassica napus) and the associated herbicide application on eubacterial and Pseudomonas communities in the rhizosphere. FEMS Microbiol Ecol 41:181–190. doi: 10.1016/S0168-6496(02)00290-8 PubMedCrossRefGoogle Scholar
  27. Ha SB, Lee SB, Lee DE, Guh JO, Back K (2003) Transgenic rice plants expressing Bacillus subtilis protoporphyrinogen oxidase gene show low herbicide oxyfluorfen resistance. Biol Plantarum 47:277–280. doi: 10.1023/B:BIOP.0000022265.66891.73 CrossRefGoogle Scholar
  28. Ha SB, Lee SB, Lee Y, Yang K, Lee N, Jang SM, Chung JS, Jung S, Kim YS, Wi SG, Back K (2004) The plastidic Arabidopsis protoporphyrinogen IX oxidase gene, with or without the transit sequence, confers resistance to the diphenyl ether herbicide in rice. Plant Cell Environ 27:79–88. doi: 10.1046/j.0016-8025.2003.01127.x CrossRefGoogle Scholar
  29. Hannula SE, de Boer W, van Veen JA (2010) In situ dynamics of soil fungal communities under different genotypes of potato, including a genetically modified cultivar. Soil Biol Biochem 42:2211–2223. doi: 10.1016/j.soilbio.2010.08.020 CrossRefGoogle Scholar
  30. Jacobs JM, Jacobs NJ, Sherman TD, Duke SO (1991) Effect of diphenyl ether herbicides on oxidation of protoporphyrinogen to protoporphyrin in organellar and plasma membrane enriched fractions of barley. Plant Physiol 97:197–203. doi: 10.1104/pp.97.1.197 PubMedCrossRefGoogle Scholar
  31. James C (2010) Global status of commercialized biotech/GM crops: ISAAA Briefs No. 42, ISAAA, Ithaca, NY. http://www.isaaa.org/resources/publications/briefs/42/
  32. Jung S, Back K (2005) Herbicidal and antioxidant responses of transgenic rice overexpressing Myxococcus xanthus protoporphyrinogen oxidase. Plant Physiol Biochem 43:423–430. doi: 10.1016/j.plaphy.2005.03.008 PubMedCrossRefGoogle Scholar
  33. Jung HI, Kuk YI (2007) Resistance mechanisms in protoporphyrinogen oxidase (PROTOX) inhibitor-resistant transgenic rice. J Plant Biol 50:586–594. doi: 10.1007/BF03030713 CrossRefGoogle Scholar
  34. Jung S, Lee Y, Yang K, Lee SB, Jang SM, Ha SB, Back K (2004) Dual targeting of Myxococcus xanthus protoporphyrinogen oxidase into chloroplasts and mitochondria and high level oxyfluorfen resistance. Plant Cell Environ 27:1436–1446. doi: 10.1111/j.1365-3040.2004.01247.x CrossRefGoogle Scholar
  35. Jung HI, Kuk YI, Back K, Burgos NR (2008) Resistance pattern and antioxidant enzyme profiles of protoporphyrinogen oxidase (PROTOX) inhibitor-resistant transgenic rice. Pestic Biochem Physiol 91:53–65. doi: 10.1016/j.pestbp.2008.01.005 CrossRefGoogle Scholar
  36. Jung HI, Kuk YI, Kim HY, Back K, Lee DJ, Lee S, Burgos NR (2010) Resistance levels and fitness of protoporphyrinogen oxidase (PROTOX) inhibitor-resistant transgenic rice in paddy fields. Field Crop Res 115:125–131. doi: 10.1016/j.fcr.2009.10.010 CrossRefGoogle Scholar
  37. Kikuchi H, Watanabe T, Jia Z, Kimura M, Asakawa S (2007) Molecular analyses reveal stability of bacterial communities in bulk soil of a Japanese paddy field: estimation by denaturing gradient gel electrophoresis of 16S rRNA genes amplified from DNA accompanied with RNA. Soil Sci Plant Nutr 53:448–458. doi: 10.1111/j.1747-0765.2007.00177.x CrossRefGoogle Scholar
  38. Kim M-S, Ahn J-H, Jung M-K, Yu J-H, Joo D, Kim M-C, Shin H-C, Kim T, Ryu T-H, Kweon S-J, Kim T, Kim D-H, Ka J-O (2005) Molecular and cultivation-based characterization of bacterial community structure in rice field soil. J Microbiol Biotechnol 15:1087, JMB / ScopusGoogle Scholar
  39. Kim M-C, Ahn J-H, Shin H-C, Kim T, Ryu T-H, Kim D-H, Song HG, Lee GH, Ka JO (2008) Molecular analysis of bacterial community structures in paddy soils for environmental risk assessment with two varieties of genetically modified rice, Iksan 483 and Milyang 204. J Microbiol Biotechnol 18:207–218, JMB / ScopusPubMedGoogle Scholar
  40. Kim C-G, Park KW, Lee B, Kim DI, Park J-Y, Kim H-J, Park JE, An JH, Cho K-H, Jeong S-C, Choi KH, Harn CH, Kim HM (2009) Gene flow from genetically modified to conventional chili pepper (Capsicum annuum L.). Plant Sci 176:406–412. doi: 10.1016/j.plantsci.2008.12.012 CrossRefGoogle Scholar
  41. Kruskal JB (1964) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115–129. doi: 10.1007/BF02289694 CrossRefGoogle Scholar
  42. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–147Google Scholar
  43. Lee HJ, Duke MV, Duke SO (1993) Cellular localization of protoporphyrinogen-oxidizing activities of etiolated barley (Hordeum vulgare L.) leaves. Plant Physiol 102:881–889. doi: 10.1104/pp.102.3.881/PlantPhysiol/Scopus PubMedGoogle Scholar
  44. Lee HJ, Lee SB, Chung JS, Han SU, Han O, Guh JO, Jeon JS, An G, Back K (2000) Transgenic rice plants expressing a Bacillus subtilis protoporphyrinogen oxidase gene are resistant to diphenyl ether herbicide oxyfluorfen. Plant Cell Physiol 41:743–749. doi: 10.1093/pcp/41.6.743/PCP/Scopus PubMedCrossRefGoogle Scholar
  45. Lee K, Yang K, Kang K, Kang S, Lee N, Back K (2007) Use of Myxococcus xanthus protoporphyrinogen oxidase as a selectable marker for transformation of rice. Pestic Biochem Physiol 88:31–35. doi: 10.1016/j.pestbp.2006.08.011 CrossRefGoogle Scholar
  46. Lermontova I, Grimm B (2000) Overexpression of plastidic protoporphyrinogen IX oxidase leads to resistance to the diphenyl-ether herbicide acifluorfen. Plant Physiol 122:75–84. doi: 10.1104/pp.122.1.75 PubMedCrossRefGoogle Scholar
  47. Lermontova I, Kruse E, Mock HP, Grimm B (1997) Cloning and characterization of a plastidal and a mitochondrial isoform of tobacco protoporphyrinogen IX oxidase. Proc Natl Acad Sci USA 94:8895–8900. doi: 10.1073/pnas.94.16.8895 PubMedCrossRefGoogle Scholar
  48. Li X, Nicholl D (2005) Development of PPO inhibitor-resistant cultures and crops. Pest Manag Sci 61:277–285. doi: 10.1002/ps.1011 PubMedCrossRefGoogle Scholar
  49. Li X, Volrath SL, Nicholl DBG, Chilcott CE, Johnson MA, Ward ER, Law MD (2003) Development of protoporphyrinogen oxidase as an efficient selection marker for Agrobacterium tumefaciens-mediated transformation of maize. Plant Physiol 133:736–747. doi: 10.1104/pp.103.026245 PubMedCrossRefGoogle Scholar
  50. Lilley AK, Bailey MJ, Cartwright C, Turner SL, Hirsch PR (2006) Life in earth: the impact of GM plants on soil ecology? Trends Biotechnol 24:9–14. doi: 10.1016/j.tibtech.2005.11.005 PubMedCrossRefGoogle Scholar
  51. Liphadzi KB, Al-Khatib K, Bensch CN, Stahlman PW, Dille JA, Todd T, Rice CW, Horak MJ, Head MJ (2005) Soil microbial and nematode communities as affected by glyphosate and tillage practices in a glyphosate-resistant cropping system. Weed Sci 53:536–545. doi: 10.1614/WS-04-129R1 CrossRefGoogle Scholar
  52. Liu W, Lu HH, Wu W, Wei QK, Chen YX, Thies JE (2008) Transgenic Bt rice does not affect enzyme activities and microbial composition in the rhizosphere during crop development. Soil Biol Biochem 40:475–486. doi: 10.1016/j.soilbio.2007.09.017 CrossRefGoogle Scholar
  53. Ma K, Lu Y (2011) Regulation of microbial methane production and oxidation by intermittent drainage in rice field soil. FEMS Microbiol Ecol 75:446–456. doi: 10.1111/j.1574-6941.2010.01018.x PubMedCrossRefGoogle Scholar
  54. Motavalli PP, Kremer RJ, Fang M, Means NE (2004) Impact of genetically modified crops and their management on soil microbially mediated plant nutrient transformations. J Environ Qual 33:816–824. doi: 10.2134/jeq2004.0816 PubMedCrossRefGoogle Scholar
  55. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G, Valori F (2007) Microbial diversity and microbial activity in the rhizosphere. Cienc Suelo 25:89–97Google Scholar
  56. Nannipieri P, Ascher J, Ceccherini MT, Guerri G, Renella G, Pietramellara G (2008a) Recent advances in functional genomics and proteomics of plant associated microbes. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Heideleberg, pp 215–241CrossRefGoogle Scholar
  57. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G, Valori F (2008b) Effects of root exudates on microbial diversity and activity in rhizosphere soils. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Heideleberg, pp 339–365CrossRefGoogle Scholar
  58. Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2011) Vegan: community ecology package, R package version 1.17-8, 2011 http://CRAN.R-project.org/package=vegan
  59. Oliveira AP, Pampulha ME, Bennett JP (2008) A two-year field study with transgenic Bacillus thuringiensis maize: effects on soil microorganisms. Sci Total Environ 405:351–357. doi: 10.1016/j.scitotenv.2008.05.046 PubMedCrossRefGoogle Scholar
  60. Powell JR, Dunfield KE (2007) Non-target impacts of genetically modified, herbicide-resistant crops on soil microbial and faunal communities. In: Gulden RH, Swanton CJ (eds) The first decade of herbicide resistant crops in Canada. Canadian Weed Science Society, Sainte Annede Bellevue, pp 127–137Google Scholar
  61. Powell JR, Levy-Booth DJ, Gulden RH, Asbil WL, Campbell RG, Dunfield KE, Hamill AS, Hart MM, Lerat S, Nurse RE, Peter Pauls K, Sikkema PH, Swanton CJ, Trevors JT, Klironomos JN (2009) Effects of genetically modified, herbicide-tolerant crops and their management on soil food web properties and crop litter decomposition. J Appl Ecol 46:388–396. doi: 10.1111/j.1365-2664.2009.01617.x CrossRefGoogle Scholar
  62. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, ISBN 3-900051-07-0, URL http://www.R-project.org/
  63. Rasche F, Hödl V, Poll C, Kandeler E, Gerzabek MH, van Elsas JD, Sessitsch A (2006) Rhizosphere bacteria affected by transgenic potatoes with antibacterial activities compared with the effects of soil, wild-type potatoes, vegetation stage and pathogen exposure. FEMS Microbiol Ecol 56:219–235. doi: 10.1111/j.1574-6941.2005.00027.x PubMedCrossRefGoogle Scholar
  64. Roger PA, Zimmerman WJ, Lumpkin TA (1993) Microbiological management of wetland rice fields. In: Metting FB Jr (ed) Soil microbial ecology. Dekker, New York, pp 417–455Google Scholar
  65. Santos JB, Jakelaitis A, Silva AA, Costa MD, Manabe A, Silva MCS (2006) Action of two herbicides on the microbial activity of soil cultivated with common bean (Phaseolus vulgaris) in conventional-till and no-till systems. Weed Res 46:284–289. doi: 10.1111/j.1365-3180.2006.00510.x CrossRefGoogle Scholar
  66. Sanyal D, Shrestha A (2008) Direct effect of herbicides on plant pathogens and disease development in various cropping systems. Weed Sci 56:155–160. doi: 10.1614/WS-07-081.1 CrossRefGoogle Scholar
  67. Savka MA, Farrand SK (1997) Modification of rhizobacterial populations by engineering bacterium utilization of a novel plant-produced resource. Nat Biotechnol 15:363–368. doi: 10.1038/nbt0497-363 PubMedCrossRefGoogle Scholar
  68. 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. doi: 10.1016/S0168-6496(02)00196-4 PubMedCrossRefGoogle Scholar
  69. Sethunathan N, Rao VR, Adhya TK, Raghu K (1983) Microbiology of rice soils. CRC Crit Rev Microbiol 10:125–172. doi: 10.3109/10408418209113561 CrossRefGoogle Scholar
  70. Siciliano SD, Germida JJ (1999) Taxonomic diversity of bacteria associated with the roots of field-grown transgenic Brassica napus cv. Quest, compared to the non-transgenic B. napus cv. Excel and B. rapa cv. Parkland. FEMS Microbiol Ecol 29:263–272. doi: 10.1016/S0168-6496(99)00019-7 CrossRefGoogle Scholar
  71. Siciliano SD, Theoret CM, De Freitas JR, Hucl PJ, Germida JJ (1998) Differences in the microbial communities associated with the roots of different cultivars of canola and wheat. Can J Microbiol 44:844–851. doi: 10.1139/cjm-44-9-844 CrossRefGoogle Scholar
  72. Smit E, Leeflang P, Glandorf B, van Elsas JD, Wernars K (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18s rRNA and temperature gradient gel electrophoresis. Appl Environ Microbiol 65:2614–2621, AEM / ScopusPubMedGoogle Scholar
  73. Trevors JT, Kuikman P, Watson B (1994) Transgenic plants and biogeochemical cycles. Mol Ecol 3:57–64. doi: 10.1111/j.1365-294X.1994.tb00045.x CrossRefGoogle Scholar
  74. van Overbeek L, 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. doi: 10.1111/j.1574-6941.2008.00469.x PubMedCrossRefGoogle Scholar
  75. Weinert N, Meincke R, Gottwald C, Heuer H, Gomes NCM, Schloter M, Berg G, Smalla K (2009) Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl Environ Microbiol 75:3859–3865. doi: 10.1128/AEM.00414-09 PubMedCrossRefGoogle Scholar
  76. White TJ, Bruns TD, Lee S, Taylor J (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322Google Scholar
  77. Wolfenbarger LL, Phifer PR (2000) The ecological risks and benefits of genetically engineered plants. Science 290:2088–2093. doi: 10.1126/science.290.5499.2088 PubMedCrossRefGoogle Scholar
  78. Wu W-X, Ye Q-F, Min H (2004) Effect of straws from Bt-transgenic rice on selected biological activities in water-flooded soil. Eur J Soil Biol 40:15–22. doi: 10.1016/j.ejsobi.2004.01.001 CrossRefGoogle Scholar
  79. Yang K, Jung S, Lee Y, Back K (2006) Modifying Myxococcus xanthus protoporphyrinogen oxidase to plant codon usage and high level of oxyfluorfen resistance in transgenic rice. Pestic Biochem Physiol 86:186–194. doi: 10.1016/j.pestbp.2006.04.003 CrossRefGoogle Scholar
  80. Zak DR, Blackwood CB, Waldrop MP (2006) A molecular dawn for biogeochemistry. Trends Ecol Evol 21:288–295. doi: 10.1016/j.tree.2006.04.003 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Young Jin Chun
    • 1
  • Hyo-Jeong Kim
    • 2
  • Kee Woong Park
    • 2
  • Soon-Chun Jeong
    • 2
  • Bumkyu Lee
    • 3
  • Kyoungwhan Back
    • 4
  • Hwan Mook Kim
    • 5
    Email author
  • Chang-Gi Kim
    • 2
    Email author
  1. 1.Environmental Appraisal CenterKorea Environment InstituteSeoulRepublic of Korea
  2. 2.Bio-Evaluation CenterKRIBBCheongwonRepublic of Korea
  3. 3.National Academy of Agricultural ScienceRural Development AdministrationSuwonRepublic of Korea
  4. 4.Division of Applied Bioscience and BiotechnologyChonnam National UniversityGwangjuRepublic of Korea
  5. 5.Department of PharmacyGachon University of Medicine and ScienceIncheonRepublic of Korea

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