Do genetic modifications in crops affect soil fungi? a review

Biology and Fertility of Soils

Volumn 50, Issue 3, 2014, Pages 433-446

  Hannula, S E ^a   de Boer, W ^a,b   van Veen, J A ^a,c  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c LEIDEN UNIVERSITY   (Netherlands)

Author keywords

'Normal operating range'; Genetically modified (GM) plants; Risk assessment; Soil fungi

Indexed keywords

AGRICULTURAL ECOSYSTEM; COMMUNITY STRUCTURE; CULTIVAR; ECOLOGICAL IMPACT; ECOSYSTEM FUNCTION; ENVIRONMENTAL RISK; FUNGUS; SOIL MICROORGANISM; SOIL ORGANIC MATTER; TRANSGENIC PLANT;

FUNGI;

EID: 84897573198     PISSN: 01782762     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00374-014-0895-x     Document Type: Review

References (115)

1. Berg B, McClaugherty C (2008) Plant litter: decomposition, humus formation, carbon sequestration (second ed.). Springer, Berlin, New York.
2. 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): 1-13.
3. Birch ANE, Griffiths BS, Caul S, Thompson J, Heckmann LH, Krogh PH, Cortet J (2007) The role of laboratory, glasshouse and field scale experiments in understanding the interactions between genetically modified crops and soil ecosystems: a review of the ECOGEN project. Pedobiologia 51(3): 251-260.
4. Blackwood CB, Buyer JS (2004) Soil microbial communities associated with Bt and non-Bt corn in three soils. J Environ Qual 33: 832-836.
5. Bruinsma M, Kowalchuk GA, van Veen JA (2003) Effects of genetically modified plants on microbial communities and processes in soil. Biol Fertility Soils 37(6): 329-337.
6. Burgess MS, Mehuys GR, Madramootoo CA (2002) Decomposition of grain-corn residues (Zea mays L.): a litterbag study under three tillage systems. Can J Soil Sci 82(2): 127-138.
7. Carlile MJ, Watkinson SC, Gooday GW (2001) The fungi, 2nd edn. Academic Press, San Diego, CA, USA.
8. Castaldini M, Turrini A, Sbrana C, Benedetti A, Marchionni M, Mocali S, Fabiani A, Landi S, Santomassimo F, Pietrangeli B, Nuti MP, Miclaus N, Giovannetti M (2005) Impact of Bt corn on rhizospheric and soil eubacterial communities on beneficial mycorrhizal symbiosis in experimental microcosms. Appl Environ Microbiol 71(11): 6719-6729. doi: 10. 1128/aem. 71. 11. 6719-6729. 2005.
9. Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertility Soils 48(5): 489-499. doi: 10. 1007/s00374-012-0691-4.
10. Cheeke TE, Pace BA, Rosenstiel TN, Cruzan MB (2011) The influence of fertilizer level and spore density on arbuscular mycorrhizal colonization of transgenic Bt 11 maize (Zea mays) in experimental microcosms. FEMS Microbiol Ecol 75(2): 304-312. doi: 10. 1111/j. 1574-6941. 2010. 01013. x.
11. Cheeke TE, Rosenstiel TN, Cruzan MB (2012) Evidence of reduced arbuscular mycorrhizal fungal colonization in multiple lines of Bt maize. Am J Bot 99(4): 700-707. doi: 10. 3732/ajb. 1100529.
12. Cheeke TE, Cruzan MB, Rosenstiel TN (2013) Field evaluation of arbuscular mycorrhizal fungal colonization in Bacillus thuringiensis toxin-expressing (Bt) and non-Bt maize. Appl Environ Microbiol 79(13): 4078-4086. doi: 10. 1128/aem. 00702-13.
13. Chun Y, Kim H-J, Park K, Jeong S-C, Lee B, Back K, Kim H, Kim C-G (2012) Two-year field study shows little evidence that PPO-transgenic rice affects the structure of soil microbial communities. Biol Fertility Soils 48(4): 453-461. doi: 10. 1007/s00374-011-0626-5.
14. Cortet J, Andersen MN, Caul S, Griffiths B, Joffre R, Lacroix B, Sausse C, Thompson J, Krogh PH (2006) Decomposition processes under Bt (Bacillus thuringiensis) maize: results of a multi-site experiment. Soil Biol Biochem 38(1): 195-199.
15. Costa R, Gotz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56(2): 236-249.
16. 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(6): 915-923.
17. Daudu CK, Muchaonyerwa P, Mnkeni PNS (2009) Litterbag decomposition of genetically modified maize residues and their constituent Bacillus thuringiensis protein (Cry1Ab) under field conditions in the central region of the Eastern Cape, South Africa. Agric Ecosyst Environ 134(3-4): 153-158. doi: 10. 1016/j. agee. 2009. 06. 012.
18. de Vaufleury A, Kramarz PE, Binet P, Cortet J, Caul S, Andersen MN, Plumey E, Coeurdassier M, Krogh PH (2007) Exposure and effects assessments of Bt-maize on non-target organisms (gastropods, microarthropods, mycorrhizal fungi) in microcosms. Pedobiologia 51(3): 185-194. doi: 10. 1016/j. pedobi. 2007. 04. 005.
19. de Vries FT, van Groenigen JW, Hoffland E, Bloem J (2011) Nitrogen losses from two grassland soils with different fungal biomass. Soil Biol Biochem 43(5): 997-1005. doi: 10. 1016/j. soilbio. 2011. 01. 016.
20. de Vries FT, Thébault E, Liiri M, Birkhofer K, Tsiafouli MA, Bjørnlund L, Bracht Jørgensen H, Brady MV, Christensen S, de Ruiter PC, d'Hertefeldt T, Frouz J, Hedlund K, Hemerik L, Hol WHG, Hotes S, Mortimer SR, Setälä H, Sgardelis SP, Uteseny K, van der Putten WH, Wolters V, Bardgett RD (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci USA 110(35): 14296-14301. doi: 10. 1073/pnas. 1305198110.
21. Deacon LJ, Pryce-Miller EJ, Frankland JC, Bainbridge BW, Moore PD, Robinson CH (2006) Diversity and function of decomposer fungi from a grassland soil. Soil Biol Biochem 38(1): 7-20.
22. Donegan KK, Palm CJ, Fieland VJ, Porteous LA, Ganio LM, Schaller DL, Bucao LQ, Seidler RJ (1995) Changes in levels, species and DNA fingerprints of soil-microorganisms associated with cotton expressing the Bacillus-Thuringiensis var Kurstaki endotoxin. Appl Soil Ecol 2(2): 111-124.
23. Donegan KK, Schaller DL, Stone JK, Ganio LM, Reed G, Hamm PB, Seidler RJ (1996) Microbial populations, fungal species diversity and plant pathogen levels in field plots of potato plants expressing the Bacillus thuringiensis var tenebrionis endotoxin. Transgenic Res 5(1): 25-35.
24. Donegan KK, Seidler RJ, Doyle JD, Porteous LA, Digiovanni G, Widmer F, Watrud LS (1999) A field study with genetically engineered alfalfa inoculated with recombinant Sinorhizobium meliloti: effects on the soil ecosystem. J Appl Ecol 36(6): 920-936.
25. 2. Proc Natl Acad Sci USA 107(24): 10938-10942. doi: 10. 1073/pnas. 0912421107.
26. 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): 1-9.
27. 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(12): 7310-7318. doi: 10. 1128/aem. 69. 12. 7310-7318. 2003.
28. Fang M, Motavalli PP, Kremer RJ, Nelson KA (2007) Assessing changes in soil microbial communities and carbon mineralization in Bt and non-Bt corn residue-amended soils. Appl Soil Ecol 37(1-2): 150-160. doi: 10. 1016/j. apsoil. 2007. 06. 001.
29. Fließbach A, Messmer M, Nietlispach B, Infante V, Mader P (2012) Effects of conventionally bred and Bacillus thuringiensis (Bt) maize varieties on soil microbial biomass and activity. Biol Fertility Soils 48(3): 315-324. doi: 10. 1007/s00374-011-0625-6.
30. Flores S, Saxena D, Stotzky G (2005) Transgenic Bt plants decompose less in soil than non-Bt plants. Soil Biol Biochem 37(6): 1073-1082.
31. Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42: 243-270. doi: 10. 1146/annurev. phyto. 42. 012604. 135455.
32. Girlanda M, Bianciotto V, Cappellazzo GA, Casieri L, Bergero R, Martino E, Luppi AM, Perotto S (2008) Interactions between engineered tomato plants expressing antifungal enzymes and nontarget fungi in the rhizosphere and phyllosphere. FEMS Microbiol Lett 288(1): 9-18. doi: 10. 1111/j. 1574-6968. 2008. 01306. x.
33. Götz M, Nirenberg H, Krause S, Wolters H, Draeger S, Buchner A, Lottmann J, Berg G, Smalla K (2006) Fungal endophytes in potato roots studied by traditional isolation and cultivation-independent DNA-based methods. FEMS Microbiol Ecol 58(3): 404-413.
34. Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37(2): 112-129. doi: 10. 1111/j. 1574-6976. 2012. 00343. x.
35. Griffiths BS, Geoghegan IE, Robertson WM (2000) Testing genetically engineered potato, producing the lectins GNA and Con A, on non-target soil organisms and processes. J Appl Ecol 37: 159-170.
36. Gschwendtner S, Reichmann M, Muller 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(1-2): 413-422. doi: 10. 1007/s11104-010-0430-2.
37. Gschwendtner S, Esperschütz J, Buegger F, Reichmann M, Müller M, Munch JC, Schloter M (2011) Effects of genetically modified starch metabolism in potato plants on photosynthate fluxes into the rhizosphere and on microbial degraders of root exudates. FEMS Microbiol Ecol 76(3): 564-575. doi: 10. 1111/j. 1574-6941. 2011. 01073. x.
38. 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(12): 2211-2223. doi: 10. 1016/j. soilbio. 2010. 08. 020.
39. 13C pulse-labeling assessment of the community structure of active fungi in the rhizosphere of a genetically starch-modified potato (Solanum tuberosum) cultivar and its parental isoline. New Phytol 194(3): 784-799. doi: 10. 1111/j. 1469-8137. 2012. 04089. x.
40. Hannula SE, de Boer W, van Veen J (2012b) A 3-year study reveals that plant growth stage, season and field site affect soil fungal communities while cultivar and GM-trait have minor effects. PloS ONE 7(4): e33819. doi: 10. 1371/journal. pone. 0033819.
41. Hannula SE, de Boer W, Baldrian P, van Veen JA (2013) Effects of genetically modified amylopectin-accumulating potato in decomposer processes and fungal diversity in litter and soil. Soil Biol Biochem 58: 88-98.
42. Hart MM, Powell JR, Gulden RH, Dunfield KE, Pauls KP, Swanton CJ, Klironomos JN, Antunes PM, Koch AM, Trevors JT (2009) Separating the effect of crop from herbicide on soil microbial communities in glyphosate-resistant corn. Pedobiologia 52(4): 253-262. doi: 10. 1016/j. pedobi. 2008. 10. 005.
43. Heinze S, Raupp J, Joergensen RG (2010) Effects of fertilizer and spatial heterogeneity in soil pH on microbial biomass indices in a long-term field trial of organic agriculture. Plant Soil 328(1-2): 203-215. doi: 10. 1007/s11104-009-0102-2.
44. Henault C, English LC, Halpin C, Andreux F, Hopkins DW (2006) Microbial community structure in soils with decomposing residues from plants with genetic modifications to lignin biosynthesis. FEMS Microbiol Lett 263(1): 68-75. doi: 10. 1111/j. 1574-6968. 2006. 00416. x.
45. Holland EA, Coleman DC (1987) Litter placement effects on microbial and organic-matter dynamics in an agroecosystem. Ecology 68(2): 425-433. doi: 10. 2307/1939274.
46. Icoz I, Stotzky G (2008) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biol Biochem 40(3): 559-586.
47. Icoz I, Saxena D, Andow DA, Zwahlen C, Stotzky G (2008) Microbial populations and enzyme activities in soil in situ under transgenic corn expressing Cry proteins from Bacillus thuringiensis. J Environ Qual 37: 647-662.
48. 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(11): 3675-3684. doi: 10. 1128/aem. 00040-10.
49. James C (2012) Global status of commercialized biotech/GM crops: 2012. ISAAA Brief No. 44. International Service for the Acquisition of Agri-Biotech Applications, Ithaca.
50. Jones JDG (2011) Why genetically modified crops? Phil Trans R Soc A 369(1942): 1807-1816. doi: 10. 1098/rsta. 2010. 0345.
51. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163: 459-480.
52. Jung HG, Sheaffer CC (2004) Influence of Bt transgenes on cell wall lignification and digestibility of maize stover for silage. Crop Sci 44(5): 1781-1789.
53. Kaldorf M, Fladung M, Muhs H-JM, Buscot F (2002) Mycorrhizal colonization of transgenic aspen in a field trial. Planta 214(4): 653-660. doi: 10. 1007/s004250100658.
54. Kennedy AC (1999) Bacterial diversity in agroecosystems. Agric Ecosyst Environ 74(1-3): 65-76.
55. Knox OGG, Nehl DB, Mor T, Roberts GN, Gupta VVSR (2008) Genetically modified cotton has no effect on arbuscular mycorrhizal colonisation of roots. Field Crops Res 109(1-3): 57-60. doi: 10. 1016/j. fcr. 2008. 06. 005.
56. Kowalchuk GA, Bruinsma M, van Veen JA (2003) Assessing responses of soil microorganisms to GM plants. Trends Ecol Evol 18(8): 403-410.
57. Kremer RJ, Means NE (2009) Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms. Eur J Agron 31(3): 153-161. doi: 10. 1016/j. eja. 2009. 06. 004.
58. Kuramae EE, Verbruggen E, Hillekens R, de Hollander M, Roling WFM, van der Heijden MGA, Kowalchuk GA (2013) Tracking Fungal Community Responses to Maize Plants by DNA- and RNA-Based Pyrosequencing. PloS ONE 8 (7). doi: 10. 1371/journal. pone. 0069973.
59. Lawhorn CN, Neher DA, Dively GP (2009) Impact of coleopteran targeting toxin (Cry3Bb1) of Bt corn on microbially mediated decomposition. Appl Soil Ecol 41(3): 364-368. doi: 10. 1016/j. apsoil. 2008. 12. 003.
60. Lee S-H, Kim C-G, Kang H (2011) Temporal dynamics of bacterial and fungal communities in a genetically modified (GM) rice ecosystem. Microb Ecol 61(3): 646-659. doi: 10. 1007/s00248-010-9776-5.
61. Li X, Liu B, Cui J, Liu D, Ding S, Gilna B, Luo J, Fang Z, Cao W, Han Z (2011) No evidence of persistent effects of continuously planted transgenic insect-resistant cotton on soil microorganisms. Plant Soil 339(1): 247-257. doi: 10. 1007/s11104-010-0572-2.
62. 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(1): 9-14.
63. Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, Kõljalg U, Pennanen T, Rosendahl S, Stenlid J, Kauserud H (2013) Fungal community analysis by high-throughput sequencing of amplified markers - a user's guide. New Phytol 199(1): 288-299. doi: 10. 1111/nph. 12243.
64. Liu WK (2010) Do genetically modified plants impact arbuscular mycorrhizal fungi? Ecotoxicology 19(2): 229-238. doi: 10. 1007/s10646-009-0423-1.
65. Liu B, Zeng Q, Yan FM, Xu HG, Xu CR (2005) Effects of transgenic plants on soil microorganisms. Plant Soil 271(1-2): 1-13.
66. Liu W, Hao Lu H, Wu W, Kun Wei Q, Xu Chen Y, Thies JE (2008) Transgenic Bt rice does not affect enzyme activities and microbial composition in the rhizosphere during crop development. Soil Biol Biochem 40(2): 475-486.
67. Loreau M, Downing A, Emmerson M, Gonzalez A, Hughes J, Inchausti P, Joshi J, Norberg J, Sala O (2002) A new look at the relationship between diversity and stability. In: Naeem S (ed) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford.
68. Lu YH, Abraham WR, Conrad R (2007) Spatial variation of active microbiota in the rice rhizosphere revealed by in situ stable isotope probing of phospholipid fatty acids. Environ Microbiol 9(2): 474-481.
69. Lu H, Wu W, Chen Y, Wang H, Devare M, Thies JE (2010a) Soil microbial community responses to Bt transgenic rice residue decomposition in a paddy field. J Soils Sed 10(8): 1598-1605. doi: 10. 1007/s11368-010-0264-9.
70. Lu H, Wu W, Chen Y, Zhang X, Devare M, Thies JE (2010b) Decomposition of Bt transgenic rice residues and response of soil microbial community in rapeseed-rice cropping system. Plant Soil 336(1-2): 279-290. doi: 10. 1007/s11104-010-0476-1.
71. Lukow T, Dunfield PF, Liesack W (2000) Use of the T-RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and non-transgenic potato plants. FEMS Microbiol Ecol 32(3): 241-247. doi: 10. 1111/j. 1574-6941. 2000. tb00717. x.
72. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129(1): 1-10.
73. 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(1-2): 23-39.
74. Naef A, Defago G (2006) Population structure of plant-pathogenic Fusarium species in overwintered stalk residues from Bt-transformed and non-transformed maize crops. Eur J Plant Pathol 116(2): 129-143.
75. Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships. Eur J Soil Sci 62(1): 105-116. doi: 10. 1111/j. 1365-2389. 2010. 01314. x.
76. O'Callaghan M, Gerard EM, Bell NL, Waipara NW, Aalders LT, David BB, Conner AJ (2008) Microbial and nematode communities associated with potatoes genetically modified to express the antimicrobial peptide magainin and unmodified potato cultivars. Soil Biol Biochem 40: 1446-1459. doi: 10. 1016/j. soilbio. 2007. 12. 028.
77. Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M, Sieverding E (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42(5): 724-738. doi: 10. 1016/j. soilbio. 2010. 01. 006.
78. Oger P, Petit A, Dessaux Y (1997) Genetically engineered plants producing opines alter their biological environment. Nat Biotechnol 15(4): 369-372.
79. 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(1-3): 351-357. doi: 10. 1016/j. scitotenv. 2008. 05. 046.
80. Powell JR, Gulden RH, Hart MM, Campbell RG, Levy-Booth DJ, Dunfield KE, Pauls KP, Swanton CJ, Trevors JT, Klironomos JN (2007) Mycorrhizal and rhizobial colonization of genetically modified and conventional soybeans. Appl Environ Microbiol 73(13): 4365-4367.
81. Powell JR, Levy-Booth DJ, Robert HG, Wendy LA, Rachel GC, Kari ED, Allan SH, Miranda MH, Sylvain L, Robert EN, Pauls KP, Peter HS, Clarence JS, Jack TT, John NK (2009) Effects of genetically modified, herbicide-tolerant crops and their management on soil food web properties and crop litter decomposition. J Appl Ecol 46(2): 388-396.
82. Prosser JI (2012) Ecosystem processes and interactions in a morass of diversity. FEMS Microbiol Ecol 81(3): 507-519. doi: 10. 1111/j. 1574-6941. 2012. 01435. x.
83. Raaijmakers J, Paulitz T, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321: 341-361.
84. Radajewski S, Ineson P, Parekh NR, Murrell JC (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403(6770): 646-649.
85. Rangel-Castro JI, Killham K, Ostle N, Nicol GW, Anderson IC, Scrimgeour CM, Ineson P, Meharg A, Prosser JI (2005) Stable isotope probing analysis of the influence of liming on root exudate utilization by soil microorganisms. Environ Microbiol 7(6): 828-838.
86. Rasche F, Lueders T, Schloter M, Schaefer S, Buegger F, Gattinger A, Hood-Nowotny RC, Sessitsch A (2009) DNA-based stable isotope probing enables the identification of active bacterial endophytes in potatoes. New Phytol 181(4): 802-807. doi: 10. 1111/j. 1469-8137. 2008. 02744. x.
87. Savka MA, Farrand SK (1997) Modification of rhizobacterial populations by engineering bacterium utilization of a novel plant-produced resource. Nat Biotechnol 15(4): 363-368.
88. Saxena D, Stotzky G (2001a) Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biol Biochem 33(9): 1225-1230. doi: 10. 1016/s0038-0717(01)00027-x.
89. Saxena D, Stotzky G (2001b) Bt corn has a higher lignin content than non-Bt corn. Am J Bot 88(9): 1704-1706. doi: 10. 2307/3558416.
90. Seppänen SK, Pasonen HL, Vauramo S, Vahala J, Toikka M, Kilpeläinen I, Setälä H, Teeri TH, Timonen S, Pappinen A (2007) Decomposition of the leaf litter and mycorrhiza forming ability of silver birch with a genetically modified lignin biosynthesis pathway. Appl Soil Ecol 36(2-3): 100-106.
91. Setälä H, McLean MA (2004) Decomposition rate of organic substrates in relation to the species diversity of soil saprophytic fungi. Oecologia 139(1): 98-107.
92. Singh BK, Munro S, Potts JM, Millard P (2007) Influence of grass species and soil type on rhizosphere microbial community structure in grassland soils. Appl Soil Ecol 36(2-3): 147-155. doi: 10. 1016/j. apsoil. 2007. 01. 004.
93. Tan FX, Wang JW, Feng YJ, Chi GL, Kong HL, Qiu HF, Wei SL (2010) Bt corn plants and their straw have no apparent impact on soil microbial communities. Plant Soil 329(1-2): 349-364. doi: 10. 1007/s11104-009-0163-2.
94. Tan F, Wang J, Chen Z, Feng Y, Chi G, Rehman SU (2011) Assessment of the arbuscular mycorrhizal fungal community in roots and rhizosphere soils of Bt corn and their non-Bt isolines. Soil Biol Biochem 43(12): 2473-2479. doi: 10. 1016/j. soilbio. 2011. 08. 014.
95. Tilston EL, Halpin C, Hopkins DW (2013) Simultaneous down-regulation of enzymes in the phenylpropanoid pathway of plants has aggregated effects on rhizosphere microbial communities. Biol Fertility Soils: 1-9. doi: 10. 1007/s00374-013-0862-y.
96. Turrini A, Sbrana C, Nuti MP, Pietrangeli BM, Giovannetti M (2004) Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant Soil 266(1-2): 69-75.
97. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396(6706): 69-72.
98. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11(3): 296-310. doi: 10. 1111/j. 1461-0248. 2007. 01139. x.
99. van der Wal A, Geydan TD, Kuyper TW, de Boer W (2013) A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiol Rev 37(4): 477-494.
100. Verbruggen E, Kiers TE (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3(5-6): 547-560. doi: 10. 1111/j. 1752-4571. 2010. 00145. x.
101. Verbruggen E, Röling WFM, Gamper HA, Kowalchuk GA, Verhoef HA, van der Heijden MGA (2010) Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytol 186(4): 968-979.
102. Verbruggen E, Kuramae EE, Hillekens R, de Hollander M, Kiers ET, Röling WFM, Kowalchuk GA, van der Heijden MGA (2012) Testing potential effects of maize expressing the Bacillus thuringiensis Cry1Ab endotoxin (Bt Maize) on mycorrhizal fungal communities via DNA- and RNA-based pyrosequencing and molecular fingerprinting. Appl Environ Microbiol 78(20): 7384-7392. doi: 10. 1128/aem. 01372-12.
103. Wang GH, Xu YX, Jin J, Liu JD, Zhang QY, Liu XB (2009) Effect of soil type and soybean genotype on fungal community in soybean rhizosphere during reproductive growth stages. Plant Soil 317(1-2): 135-144. doi: 10. 1007/s11104-008-9794-y.
104. Wang Y, Xu J, Shen J, Luo Y, Scheu S, Ke X (2010) Tillage, residue burning and crop rotation alter soil fungal community and water-stable aggregation in arable fields. Soil Till Res 107(2): 71-79. doi: 10. 1016/j. still. 2010. 02. 008.
105. Weaver MA, Krutz LJ, Zablotowicz RM, Reddy KN (2007) Effects of glyphosate on soil microbial communities and its mineralization in a Mississippi soil. Pest Manage Sci 63(4): 388-393. doi: 10. 1002/ps. 1351.
106. Wei XD, Zou HL, Chu LM, Liao B, Ye CM, Lan CY (2006) Field released transgenic papaya affects microbial communities and enzyme activities in soil. Plant Soil 285(1-2): 347-358.
107. 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(12): 3859-3865. doi: 10. 1128/aem. 00414-09.
108. Wolfenbarger LL, Phifer PR (2000) Biotechnology and ecology - the ecological risks and benefits of genetically engineered plants. Science 290(5499): 2088-2093.
109. Wrobel-Kwiatkowska M, Turnau K, Goralska K, Anielska T, Szopa J (2012) Effects of genetic modifications to flax (Linum usitatissimum) on arbuscular mycorrhiza and plant performance. Mycorrhiza 22(7): 493-499. doi: 10. 1007/s00572-011-0427-6.
110. Wu WX, Ye QF, Min H (2004) Effect of straws from Bt-transgenic rice on selected biological activities in water-flooded soil. Eur J Soil Biol 40(1): 15-22.
111. Wu WX, Liu W, Lu HH, Chen YX, Devare M, Thies J (2009) Use of C-13 labeling to assess carbon partitioning in transgenic and nontransgenic (parental) rice and their rhizosphere soil microbial communities. FEMS Microbiol Ecol 67(1): 93-102. doi: 10. 1111/j. 1574-6941. 2008. 00599. x.
112. Xue K, Luo HF, Qi HY, Zhang HX (2005) Changes in soil microbial community structure associated with two types of genetically engineered plants analyzing by PLFA. J Environ Sci (China) 17(1): 130-134.
113. Xue K, Serohijos RC, Devare M, Thies JE (2011) Decomposition rates and residue-colonizing microbial communities of Bacillus thuringiensis insecticidal protein Cry3Bb-expressing (Bt) and non-Bt corn hybrids in the field. Appl Environ Microbiol 77(3): 839-846. doi: 10. 1128/aem. 01954-10.
114. Zurbrügg C, Hoenemann L, Meissle M, Romeis J, Nentwig W (2010) Decomposition dynamics and structural plant components of genetically modified Bt maize leaves do not differ from leaves of conventional hybrids. Transgenic Res 19(2): 257-267. doi: 10. 1007/s11248-009-9304-x.
115. Zwahlen C, Hilbeck A, Nentwig W (2007) Field decomposition of transgenic Bt maize residue and the impact on non-target soil invertebrates. Plant Soil 300(1-2): 245-257.