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RESEARCH ARTICLE

Field evaluation of the effects of cotton variety and GM status on rhizosphere microbial diversity and function in Australian soils

Oliver G. G. Knox A C E , Vadakattu V. S. R. Gupta B C and Richard Lardner B D
+ Author Affiliations
- Author Affiliations

A Scotland’s Rural College (SRUC), Crop and Soil Systems Group, Edinburgh, EH9 3JG, UK.

B CSIRO Ecosystem Sciences, Waite Road, Urrbrae, SA 5066, Australia.

C Cotton Catchment Communities CRC, Myall Vale, Wee Waa Road, Narrabri, NSW 2390, Australia.

D Ministry of Agriculture and Forestry, Pastoral House, PO Box 2526, Wellington, New Zealand.

E Corresponding author. Email: oliver.knox@sruc.ac.uk

Soil Research 52(2) 203-215 https://doi.org/10.1071/SR12361
Submitted: 12 December 2012  Accepted: 22 October 2013   Published: 6 March 2014

Abstract

Despite the high level of adoption of genetically modified (GM) cultivars in the Australian cotton production system, concerns remain over the use of GM technology, particularly with regard to potential non-target effects. To address the hypothesis that GM cotton causes shifts in rhizosphere microbial diversity or function, we assessed rhizosphere soil samples from a range of conventional and GM cotton cultivars for diversity of bacteria and fungi, populations of ammonium oxidisers, rhizosphere basal and selective substrate-induced respiration, and non-symbiotic N2 fixation and nitrification. Comparison of results for GM and conventional cotton cultivars, both between and within seasons, indicated that the cotton rhizosphere plant–microbial interactions are variable in nature and significantly influenced by cultivar type. The GM status of the plant did not result in rhizosphere bacterial or fungal DNA-based grouping, but MicroResp data did show some grouping based on GM status, although this was not consistent by trait, suggesting that the GM trait is not greater than cultivar selection in causing rhizosphere change, especially when measured in the field environment with all the associative management practices.

Additional keywords: cotton, microbial diversity, rhizosphere, transgenic plants.


References

Adamczyk JJ, Hardee DD, Adams LC, Sumerford DV (2001) Correlating differences in larval survival and development of bollworm (Lepidoptera: Noctuidae) and fall armyworm (Lepidoptera: Noctuidae) to differential expression of Cry1A(c) delta-endotoxin in various plant parts among commercial cultivars of transgenic Bacillus thuringiensis cotton. Journal of Economic Entomology 94, 284–290.
Correlating differences in larval survival and development of bollworm (Lepidoptera: Noctuidae) and fall armyworm (Lepidoptera: Noctuidae) to differential expression of Cry1A(c) delta-endotoxin in various plant parts among commercial cultivars of transgenic Bacillus thuringiensis cotton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtVKnt7g%3D&md5=2c97e9cd963303fe7d6a878f0ab3b14dCAS | 11233127PubMed |

Andow DA, Lovei GL, Arpaia S (2006) Ecological risk assessment for Bt crops. Nature Biotechnology 24, 749–751.
Ecological risk assessment for Bt crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvFagtbw%3D&md5=238ab7879c7c8bc72d55a05c421d3aa0CAS | 16841050PubMed |

Aslam M, Nielson K, Travis RL, Rains DW (1997) Nitrate uptake, efflux, and in vivo reduction by Pima and Acala cotton cultivars. Crop Science 37, 1795–1801.
Nitrate uptake, efflux, and in vivo reduction by Pima and Acala cotton cultivars.Crossref | GoogleScholarGoogle Scholar |

Aslam M, Travis RL, Rains DW (2001) Inhibition of net nitrate uptake by ammonium in Pima and Acala cotton roots. Crop Science 41, 1130–1136.
Inhibition of net nitrate uptake by ammonium in Pima and Acala cotton roots.Crossref | GoogleScholarGoogle Scholar |

Betz FS, Hammond BG, Fuchs RL (2000) Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. Regulatory Toxicology and Pharmacology 32, 156–173.
Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnslygu78%3D&md5=01c982e7c371b7e90c5a8462e7734bacCAS | 11067772PubMed |

Brookes G, Barfoot P (2005) GM crops: The global economic and environmental impact—the first nine years 1996–2004. AgBioForum 8, 187–196.

Brookes G, Barfoot P (2006) ‘GM crops: The first ten years—Global socio-economic and environmental impacts.’ ISAAA Brief No. 36. (International Service for Acquisition of Agri-biotech Applications: Ithaca, NY, USA)

Buyanovsky GA, Kucera CL, Wagner GH (1987) Comparative analysis of carbon dynamics in native and cultivated ecosystems. Ecology 68, 2023–2031.
Comparative analysis of carbon dynamics in native and cultivated ecosystems.Crossref | GoogleScholarGoogle Scholar |

Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved From carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Applied and Environmental Microbiology 69, 3593–3599.
A rapid microtiter plate method to measure carbon dioxide evolved From carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1Glu7k%3D&md5=160bc1f0aea384c13b810aa48add6e6fCAS | 12788767PubMed |

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 and on beneficial mycorrhizal symbiosis in experimental microcosms. Applied and Environmental Microbiology 71, 6719–6729.
Impact of Bt corn on rhizospheric and soil eubacterial communities and on beneficial mycorrhizal symbiosis in experimental microcosms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1ekur7N&md5=591c88b9792434e359df8d41bb055578CAS | 16269702PubMed |

Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.
Non-parametric multivariate analyses of changes in community structure.Crossref | GoogleScholarGoogle Scholar |

Constable GA, Preston C, Gupta VVSR (2007) GM cotton: benefits, risks and challenges. Journal of the Australian Institute of Agricultural Science. 20, 28–32.

de Man JC (1983) MPN tables, corrected. Applied Microbiology and Biotechnology 17, 301–305.
MPN tables, corrected.Crossref | GoogleScholarGoogle Scholar |

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. Applied Soil Ecology 2, 111–124.
Changes in levels, species and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var. Kurstaki endotoxin.Crossref | GoogleScholarGoogle Scholar |

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 Research 5, 25–35.
Microbial populations, fungal species diversity and plant pathogen levels in field plots of potato plants expressing the Bacillus thuringiensis var. Tenebrionis endotoxin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xos1eltw%3D%3D&md5=e6d132e5f084b5a0ef7e9530b9331cd5CAS |

Duineveld BM, Kowalchuk GA, Keijzer A, van Elsas JD, van Veen JA (2001) Analysis of bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Applied and Environmental Microbiology 67, 172–178.
Analysis of bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVWgtg%3D%3D&md5=153db77f363bb96d96ffd98543bad280CAS | 11133442PubMed |

Dunfield KE, Germida JJ (2004) Impact of genetically modified crops on soil- and plant-associated microbial communities. Journal of Environmental Quality 33, 806–815.
Impact of genetically modified crops on soil- and plant-associated microbial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVyls78%3D&md5=d4480955039af5346be9e78513d4a9ecCAS | 15224914PubMed |

Fan TWM, Lane AN, Shenker M, Bartley JP, Crowley D, Higashi RM (2001) Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS. Phytochemistry 57, 209–221.
Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFCnuro%3D&md5=a04400df605faf29e2a91e6f8aa44775CAS |

Federici BA (2003) Effects of Bt on non-target organisms. Journal of New Seeds 5, 11–30.
Effects of Bt on non-target organisms.Crossref | GoogleScholarGoogle Scholar |

Fitt GP (2000) An Australian approach to IPM in cotton: Integrating new technologies to minimise insecticide dependence. Crop Protection 19, 793–800.
An Australian approach to IPM in cotton: Integrating new technologies to minimise insecticide dependence.Crossref | GoogleScholarGoogle Scholar |

Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Molecular Ecology Notes 2, 113–118.
ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslOmsro%3D&md5=d08b204f30dd1b99940e7e7011d742f6CAS |

Gardi C, Montanarella L, Arrouays D, Bispo A, Lemanceau P, Jolivet C, Mulder C, Ranjard L, Römbke J, Rutgers M, Menta C (2009) Soil biodiversity monitoring in Europe: ongoing activities and challenges. European Journal of Soil Science 60, 807–819.
Soil biodiversity monitoring in Europe: ongoing activities and challenges.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1ylsLfF&md5=46b236c6caf95fa7d3ea6ac5eb34d282CAS |

Glandorf DCM, Bakker PAHM, VanLoon LC (1997) Influence of the production of antibacterial and antifungal proteins by transgenic plants on the saprophytic soil microflora. Acta Botanica Neerlandica 46, 85–104.

Greenplate JT (1999) Quantification of Bacillus thuringiensis insect control protein Cry1Ac over time in Bollgard cotton fruit and terminals. Journal of Economic Entomology 92, 1377–1383.

Griess P (1879) Bemerkungen zu der abhandlung der H.H. Weselsky und Benedikt “Ueber einige azoverbindungen.” Chemische Berichte 12, 426–428.

Gupta VVSR, Knox OGG (2010) How best can we design rhizosphere plant–microbe interactions for the benefit of plant growth? In ‘The Rovira Rhizosphere Symposium–Celebrating 50 years of rhizosphere research’. pp. 11–24. (The Crawford Fund: Deakin, ACT)

Gupta VVSR, Watson SK (2004) Ecological impacts of GM cotton on soil biodiversity – Below ground production of Bt by GM cotton and Bt cotton impacts on soil biological processes. CSIRO Land and Water Report to Australian Government Department of the Environment and Heritage, Canberra, ACT. Available at: http://www.environment.gov.au/settlements/biotechnology/publications/bt-cotton.html

Gupta VVSR, Roper MM, Roget DK (2006) Potential for non-symbiotic N2-fixation in different agroecological zones of southern Australia. Australian Journal of Soil Research 44, 343–354.
Potential for non-symbiotic N2-fixation in different agroecological zones of southern Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtFKgs7k%3D&md5=111c1518f1a57190658a84188910d684CAS |

Gupta VVSR, Roget DK, Davoren CW, Llewellyn R, Whitbread A (2008) ‘Farming system impacts on microbial activity and soil organic matter in southern Australian Mallee.’ (Ed. M Unkovich) (The Regional Institute Ltd: Gosford, NSW)

Gupta VVSR, Kroker SK, Hicks M, Coppi JC, Roget DK (2009) Rhizosphere microbial composition is influenced by crop varieties. In ‘5th Australasian Soilborne Disease Symposium–Extended abstracts’. pp. 42–44. (Australasian Soilborne Disease Symposium Secretariat: Kingston, ACT)

Gupta VVSR, Rovira AD, Roget DK (2010) Principles and management of soil biological factors for sustainable rainfed farming systems. In ‘Rainfed farming systems’. (Eds P Tow, I Cooper, I Partridge, C Birch) (Springer Science and Business Media: Berlin, Heidelberg)

Hilbeck A, Schmidt JEU (2006) Another view of Bt proteins—How specific are they and what else might they do? Biopesticides International 2, 1–50.

Holland JN (1995) Effects of above-ground herbivory on soil microbial biomass in conventional and no-tillage agroecosystems. Applied Soil Ecology 2, 275–279.
Effects of above-ground herbivory on soil microbial biomass in conventional and no-tillage agroecosystems.Crossref | GoogleScholarGoogle Scholar |

Hoque Z, Dillon M, Farquharson B (2002) Three seasons of IPM in an area wide management group–a comparative analysis of field level profitability. In ‘11th Australian Cotton Conference’. pp. 749–755. (Australian Cotton Growers Research Association: Orange, NSW)

Hulugalle NR, Weaver TB, Finlay LA, Luelf NW, Tan DKY (2009) Potential contribution by cotton roots to soil carbon stocks in irrigated Vertosols. Soil Research 47, 243–252.
Potential contribution by cotton roots to soil carbon stocks in irrigated Vertosols.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlWrurk%3D&md5=2e9640d674eb60e29b03788589d70bd2CAS |

Knox OGG, Gupta VVSR, Roberts GN (2004) Genetically modified cotton influence on soil microbiota. In ‘Proceedings of the 3rd Australian Soilborne Disease Conference’. (Eds K Ophel, B Keller, B Hall) pp. 166–167 (SARDI, Adelaide)

Knox OGG, Constable GA, Pyke B, Gupta VVSR (2006) Environmental impact of conventional and Bt insecticidal cotton expressing one and two Cry genes in Australia. Australian Journal of Agricultural Research 57, 501–509.
Environmental impact of conventional and Bt insecticidal cotton expressing one and two Cry genes in Australia.Crossref | GoogleScholarGoogle Scholar |

Knox OGG, Gupta VVSR, Nehl DB, Stiller WN (2007) Constitutive expression of Cry proteins in roots and border cells of transgenic cotton. Euphytica 154, 83–90.
Constitutive expression of Cry proteins in roots and border cells of transgenic cotton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1Cktr0%3D&md5=ee3c944c967d4ccaf7efc85bf8f84127CAS |

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 Research 109, 57–60.
Genetically modified cotton has no effect on arbuscular mycorrhizal colonisation of roots.Crossref | GoogleScholarGoogle Scholar |

Knox OGG, Gupta VVSR, Lardner R (2009) ‘Cotton cultivar selection impacts on micorbial diversity and function.’ (Eds M Andrews, ME Andrews) pp. 129–136. (Association of Applied Biologists: Wellesbourne, UK)

Liu W (2010) Do genetically modified plants impact arbuscular mycorrhizal fungi? Ecotoxicology (London, England) 19, 229–238.
Do genetically modified plants impact arbuscular mycorrhizal fungi?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVSmsbg%3D&md5=71bd499898406897a6e40a3956061d15CAS |

Monsanto Company (2003a) Safety assessment of Bollgard II cotton event 15985. Monsanto Company, St. Louis, MO, USA. Avialable at: http://www.monsanto.com/products/Documents/safety-summaries/bollgard_II_pss.pdf

Monsanto Company (2003b) ‘Bollgard II® cotton technical manual.’ (Monsanto Company: St. Louis, MO, USA)

Paterson E, Thornton B, Midwood AJ, Sim A (2005) Defoliation alters the relative contributions of recent and non-recent assimilate to root exudation from Festuca rubra. Plant, Cell & Environment 28, 1525–1533.
Defoliation alters the relative contributions of recent and non-recent assimilate to root exudation from Festuca rubra.Crossref | GoogleScholarGoogle Scholar |

Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytologist 173, 600–610.
Rhizodeposition shapes rhizosphere microbial community structure in organic soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlGqu7s%3D&md5=d281503062058855391685fe35fa7cf5CAS | 17244055PubMed |

Powlson DS, Brookes PC, Christensen BT (1987) Measurement of soil microbial biomass provides an early indication of changes in total soil organic matter due to straw incorporation. Soil Biology & Biochemistry 19, 159–164.
Measurement of soil microbial biomass provides an early indication of changes in total soil organic matter due to straw incorporation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktlyls7w%3D&md5=cad14d7ba576cb2674ea985667e87e8dCAS |

Prinčič A, Mahne I, Megušar F, Paul EA, Tiedje JM (1998) Effects of pH and oxygen and ammonium concentrations on the community structure of nitrifying bacteria from wastewater. Applied and Environmental Microbiology 64, 3584–3590.

Rösch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Applied and Environmental Microbiology 68, 3818–3829.
Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil.Crossref | GoogleScholarGoogle Scholar | 12147477PubMed |

Saxena D, Stotzky G (2001) 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 Biology & Biochemistry 33, 1225–1230.
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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsV2js74%3D&md5=a24b3cedf926d0fd6489bd45ce245d66CAS |

Saxena D, Flores S, Stotzky G (2002) Bt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events. Soil Biology & Biochemistry 34, 133–137.
Bt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksVag&md5=a722331a97702f67a19169ec8ec65bd7CAS |

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 and Soil 285, 149–159.
Transgenic Bt cotton has no apparent effect on enzymatic activities or functional diversity of microbial communities in rhizosphere soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsFWlsr4%3D&md5=fdc1b3b6126b05f357ae0037b61b7c0cCAS |

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. Canadian Journal of Microbiology 44, 844–851.
Differences in the microbial communities associated with the roots of different cultivars of canola and wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvFyksbg%3D&md5=5be56cd90c496aad59f7d68e59197a50CAS |

Sims SR (1995) Bacillus thuringiensis var Kurstaki [Cryia(C)] protein expressed in transgenic cotton: Effects on beneficial and other non-target insects. The Southwestern Entomologist 20, 493–500.

Sims SR (1997) Host activity spectrum of the CryIIa Bacillus thuringiensis subsp. kurstaki protein. Effects on Lepidoptera, Diptera, and non-target arthropods. The Southwestern Entomologist 22, 395–404.

Sisterson M, Biggs R, Olson C, Carriere Y, Dennehy T, Tabashnik B (2004) Arthropod abundance and diversity in Bt and non-Bt cotton fields. Environmental Entomology 33, 921–929.
Arthropod abundance and diversity in Bt and non-Bt cotton fields.Crossref | GoogleScholarGoogle Scholar |

Sparling GP, Gupta VVSR, Chunya Z (1993) Release of ninhydrin-reactive compounds during fumigation of soil to estimate microbial C and N. Soil Biology & Biochemistry 25, 1803–1805.

Stephen JR, Chang YJ, Macnaughton SJ, Kowalchuk GA, Leung KT, Flemming CA, White DC (1999) Effect of toxic metals on indigenous soil beta-subgroup proteobacterium ammonia oxidizer community structure and protection against toxicity by inoculated metal-resistant bacteria. Applied and Environmental Microbiology 65, 95–101.

Turrini A, Sbrana C, Nuti MP, Pietrangeli BM, Giovannetti M (2005) Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant and Soil 266, 69–75.
Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

U.S. EPA (2001) Biopesticides Registration Action Document—Bacillus thuringiensis plant-incorporated protectants. 16 October 2001. United States Environmental Protection Agency, Washington, DC. Available at: www.epa.gov/oppbppd1/biopesticides/pips/bt_brad.htm

U.S. EPA (2002) Biopesticide Registration Action Document—Bacillus thuringiensis Cry2Ab2 protein and the genetic material necessary for its production in cotton. United States Environmental Protection Agency, Washington, DC. Availabe at: http://www.epa.gov/opp00001/chem_search/reg_actions/registration/decision_PC-006487_4-Mar-03.pdf

Villanyi I, Fuzy A, Biro B (2006) Non-target microorganisms affected in the rhizosphere of the transgenic Bt corn. Cereal Research Communications 34, 105–108.

von Wirén N, Gazzarrini S, Frommer WB (1997) Regulation of mineral nitrogen uptake in plants. Plant and Soil 196, 191–199.
Regulation of mineral nitrogen uptake in plants.Crossref | GoogleScholarGoogle Scholar |

Wakelin SA, Gregg AL, Simpson RJ, Li GD, Riley IT, McKay AC (2009) Pasture management clearly affects soil microbial community structure and N-cycling bacteria. Pedobiologia 52, 237–251.
Pasture management clearly affects soil microbial community structure and N-cycling bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlKqsLY%3D&md5=6072992b9a400eac2a9c3e7872d4189eCAS |

Watt M, Kirkegaard JA, Passioura JB (2006) Rhizosphere biology and crop productivity a review. Australian Journal of Soil Research 44, 299–317.
Rhizosphere biology and crop productivity a review.Crossref | GoogleScholarGoogle Scholar |

Weber M, Nentwig W (2006) Impact of Bt Corn on the diplopod Allajulus latestriatus. Pedobiologia - International Journal of Soil Biology 50, 357–368.
Impact of Bt Corn on the diplopod Allajulus latestriatus.Crossref | GoogleScholarGoogle Scholar |

Werner D, Berggold R, Jaeger D, Krotzky A, Papen H, Schenk S, Thierfelder H (1989) Plant, microbial and soil factors, determining nitrogen fixation in the rhizosphere. Zeitschrift für Pflanzenernährung und Bodenkunde 152, 231–236.
Plant, microbial and soil factors, determining nitrogen fixation in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFemtrk%3D&md5=43eb3d827d46be30a6018242354fe78aCAS |

Werth JA, Preston C, Roberts GN, Taylor IN (2006) Weed management practices in glyphosate-tolerant and conventional cotton fields in Australia. Australian Journal of Experimental Agriculture 46, 1177–1183.
Weed management practices in glyphosate-tolerant and conventional cotton fields in Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnslWjtr8%3D&md5=91a2fda42b46f4283feca5ea188b4dfaCAS |

Li X, Liu B, Heia S, Liu D, Han Z, Zhou K, Cui J, Luo J, Zheng Y (2009) The effect of root exudates from two transgenic insect-resistant cotton lines on the growth of Fusarium oxysporum. Transgenic Research 18, 757–767.
The effect of root exudates from two transgenic insect-resistant cotton lines on the growth of Fusarium oxysporum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVWrsrfJ&md5=cbaa0a6ddc65ea38755ceee3f70e28afCAS | 19396562PubMed |