Effect of glyphosate on the tripartite symbiosis formed by Glomus intraradices, Bradyrhizobium japonicum, and genetically modified soybean

Applied Soil Ecology

Volumn 41, Issue 1, 2009, Pages 128-136

  Powell, Jeff R ^a   Campbell, Rachel G ^a   Dunfield, Kari E ^a   Gulden, Robert H ^a   Hart, Miranda M ^a   Levy Booth, David J ^a   Klironomos, John N ^a   Pauls, K Peter ^a   Swanton, Clarence J ^a   Trevors, Jack T ^a   Antunes, Pedro M ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Arbuscular mycorrhizal fungi; Glycine max; Herbicide tolerant crops; Rhizobia

Indexed keywords

ARBUSCULAR; BRADYRHIZOBIUM JAPONICUM; FUNGI; GLOMUS INTRARADICES; GLYCINE MAX; RHIZOBIACEAE;

EID: 57549097626     PISSN: 09291393     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.apsoil.2008.10.002     Document Type: Article

References (55)

1. Ames R.N., Mihara K.L., and Bethlenfalvay G.J. The establishment of microorganisms in vesicular-arbuscular mycorrhizal and control treatments. Biol. Fertil. Soils 3 (1987) 217-223
2. Anderson T.A., Guthrie E.A., and Walton B.T. Bioremediation in the rhizosphere. Environ. Sci. Technol. 27 (1993) 2630-2636
3. Antunes P.M., de Varennes A., Zhang T., and Goss M.J. The tripartite symbiosis formed by indigenous arbuscular mycorrhizal fungi, Bradyrhizobium japonicum and soya bean under field conditions. J. Agron. Crop Sci. 192 (2006) 373-378
4. Atkinson D. The toxicological properties of glyphosate-a summary. In: Grossbard E., and Atkinson D. (Eds). The Herbicide Glyphosate (1985), Butterworth and Co., Ltd, Boston, MA 127-133
5. Barea J.M., Azcon-Aguilar C., and Azcon R. Vesicular-arbuscular mycorrhiza improve both symbiotic nitrogen fixation and nitrogen uptake from soil as assessed with a nitrogen-15 technique under field conditions. New Phytol. 106 (1987) 717-726
6. Baucom R.S., and Mauricio R. Fitness costs and benefits of novel herbicide tolerance in a noxious weed. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 13386-13390
7. Bethlenfalvay G.J., Mihara K.L., Schreiner R.P., and McDaniel H. Mycorrhizae, biocides, and biocontrol. 1. Herbicide-mycorrhiza interactions in soybean and cocklebur treated with bentazon. Appl. Soil Ecol. 3 (1996) 197-204
8. Bethlenfalvay G.J., Schreiner R.P., Mihara K.L., and McDaniel H. Mycorrhizae, biocides, and biocontrol. 2. Mycorrhizal fungi enhance weed control and crop growth in a soybean-cocklebur association treated with the herbicide bentazon. Appl. Soil Ecol. 3 (1996) 205-214
9. Brundrett M.C., Piche Y., and Peterson R.L. A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Can. J. Bot. 62 (1984) 2128-2134
10. Chalk P.M., Souza R.D., Urquiaga S., Alves B.J.R., and Boddey R.M. The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol. Biochem. 38 (2006) 2944-2951
11. De Maria N., Becerril J.M., Garcia-Plazaola J.I., Hernandez A., De Felipe M.R., and Fernandez-Pascual M. New insights on glyphosate mode of action in nodular metabolism: role of shikimate accumulation. J. Agric. Food Chem. 54 (2006) 2621-2628
12. dos Santos J.B., Ferreira E.A., Kasuya M.C.M., da Silva A.A., and Procopio S.D.O. Tolerance of Bradyrhizobium strains to glyphosate formulations. Crop Prot. 24 (2005) 543-547
13. Duke S.O. Taking stock of herbicide-resistant crops ten years after introduction. Pest Manag. Sci. 61 (2005) 211-218
14. Faraway J.J. Extending the Linear Model with R: Generalized Linear, Mixed Effects and Nonparametric Regression Models (2006), CRC Press, Boca Raton, FL 301 pp
15. Feng P.C.C., Baley G.J., Clinton W.P., Bunkers G.J., Alibhai M.F., Paulitz T.C., and Kidwell K.K. Glyphosate inhibits rust diseases in glyphosate-resistant wheat and soybean. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17290-17295
16. Fried M., and Middelboe V. Measurement of amount of nitrogen fixed by a legume crop. Plant Soil 47 (1977) 713-716
17. Glass R.L. Adsorption of glyphosate by soils and clay-minerals. J. Agric. Food Chem. 35 (1987) 497-500
18. 2 fixation. Soil Biol. Biochem. 34 (2002) 1167-1173
19. 2 fixation by soybeans grown with different levels of mineral nitrogen, and the fertilizer replacement value for a following crop. Can. J. Soil Sci. 82 (2002) 139-145
20. Greweling T. Chemical Analysis of Plant Tissue. Research Bulletin 6(8) (1976), Cornell University Agricultural Experimental Station, Ithaca, NY 35 pp
21. Herrmann K.M., and Weaver L.M. The shikimate pathway. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 (1999) 473-503
22. James C. Global Status of Commercialized Biotech/GM crops: 2006. Brief 35-2006 (Executive Summary) (2006), ISAAA, Ithaca, NY 12 pp
23. Johansen A., and Jensen E.S. Transfer of N and P from intact or decomposing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol. Biochem. 28 (1996) 73-81
24. Johnson N.C. Can fertilization of soil select less mutualistic mycorrhizae. Ecol. Appl. 3 (1993) 749-757
25. Johnson N.C., Graham J.H., and Smith F.A. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135 (1997) 575-586
26. Khalvati M.A., Hu Y., Mozafar A., and Schmidhalter U. Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biol. 7 (2005) 706-712
27. Killham K. Soil Ecology (1994), Cambridge University Press, Cambridge, UK 242 pp
28. King C.A., Purcell L.C., and Vories E.D. Plant growth and nitrogenase activity of glyphosate-tolerant soybean in response to foliar glyphosate applications. Agron. J. 93 (2001) 179-186
29. Klironomos J.N. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84 (2003) 2292-2301
30. Kremer R.J., Means N.E., and Kim S. Glyphosate affects soybean root exudation and rhizosphere micro-organisms. Int. J. Environ. Anal. Chem. 85 (2005) 1165-1174
31. Linderman R.G. Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect 78 (1988) 366-371
32. Liu C.M., McLean P.A., Sookdeo C.C., and Cannon F.C. Degradation of the herbicide glyphosate by members of the family Rhizobiaceae. Appl. Environ. Microbiol. 57 (1991) 1799-1804
33. Long S.R. Genes and signals in the Rhizobium-legume symbiosis. Plant Physiol. 125 (2001) 69-72
34. Malty J.D., Siqueira J.O., and Moreira F.M.D. Effects of glyphosate on soybean symbiotic microorganisms, in culture media and in greenhouse. Pesqui. Agropecu. Bras. 41 (2006) 285-291
35. McGonigle T.P., Miller M.H., Evans D.G., Fairchild G.L., and Swan J.A. A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol. 115 (1990) 495-501
36. Moorman T.B., Becerril J.M., Lydon J., and Duke S.O. Production of hydroxybenzoic acids by Bradyrhizobium japonicum strains after treatment with glyphosate. J. Agric. Food Chem. 40 (1992) 289-293
37. Mujica M.T., Fracchia S., Ocampo J.A., and Godeas A. Influence of the herbicides chlorsulfuron and glyphosate on mycorrhizal soybean intercropped with the weeds Brassica campestris or Sorghum halepensis. Symbiosis 27 (1999) 73-81
38. Mulvaney R.L. Mass spectrometry. In: Knowles R., and Blackburn T.H. (Eds). Nitrogen Isotope Techniques (1993), Academic Press, San Diego, CA 11-57
39. NASS, 2006. Acreage. US Department of Agriculture, Washington, DC, 48 pp.
40. OMAFRA, 2006. Publication 75, Guide to Weed Control. Queen's Printer for Ontario, Guelph, ON, 348 pp.
41. Peoples M.B., and Craswell E.T. Biological nitrogen-fixation-investments, expectations and actual contributions to agriculture. Plant Soil 141 (1992) 13-39
42. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., 2006. nlme: Linear and nonlinear mixed effects models. R Package v. 3.1-78.
43. Pinheiro J.C., and Bates D.M. Mixed-Effects Models in S and S-Plus (2000), Springer Verlag, New York, NY 528 pp
44. R Development Core Team, 2006. R: A Language and Environment for Statistical Computing. v.1.16. R Foundation for Statistical Computing, Vienna, Austria.
45. Ravuri V., and Hume D.J. Performance of a superior Bradyrhizobium japonicum and a selected Sinorhizobium fredii strain with soybean cultivars. Agron. J. 84 (1992) 1051-1056
46. Reddy K.N., and Zablotowicz R.M. Glyphosate-resistant soybean response to various salts of glyphosate and glyphosate accumulation in soybean nodules. Weed Sci. 51 (2003) 496-502
47. Reddy K.N., Hoagland R.E., and Zablotowicz R.M. Effect of glyphosate on growth, chlorophyll, and nodulation in glyphosate-resistant and susceptible soybean (Glycine max) varieties. J. New Seeds 2 (2000) 37-52
48. Roberts F., Roberts C.W., Johnson J.J., Kyle D.E., Krell T., Coggins J.R., Coombs G.H., Milhous W.K., Tzipori S., Ferguson D.J.P., Chakrabarti D., and McLeod R. Evidence for the shikimate pathway in apicomplexan parasites. Nature 393 (1998) 801-805
49. Ryan M.H., and Graham J.H. Is there a role for arbuscular mycorrhizal fungi in production agriculture?. Plant Soil 244 (2002) 263-271
50. Smith S.E., and Read D.J. Mycorrhizal Symbiosis. 2nd ed. (1997), Academic Press, San Diego, CA 605 pp
51. Thomas R.L., Sheard R.W., and Moyer J.R. Comparison of conventional and automated procedures for N, P and K analysis of plant material using a single digestion. Agron. J. 59 (1967) 240-243
52. Wan M.T., Rahe J.E., and Watts R.G. A new technique for determining the sublethal toxicity of pesticides to the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. Environ. Toxicol. Chem. 17 (1998) 1421-1428
53. Xie Z.P., Staehelin C., Vierheilig H., Wiemken A., Jabbouri S., Broughton W.J., Vogellange R., and Boller T. Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol. 108 (1995) 1519-1525
54. Zablotowicz R.M., and Reddy K.N. Impact of glyphosate on the Bradyrhizobium japonicum symbiosis with glyphosate-resistant transgenic soybean: a minireview. J. Environ. Qual. 33 (2004) 825-831
55. Zablotowicz R.M., and Reddy K.N. Nitrogenase activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean. Crop Prot. 26 (2007) 370-376