Glyphosate affects micro-organisms in rhizospheres of glyphosate-resistant soybeans

Journal of Applied Microbiology

Volumn 110, Issue 1, 2011, Pages 118-127

  Zobiole, L H S ^a   Kremer, R J ^b   Oliveira, R S ^a   Constantin, J ^a  

^a STATE UNIVERSITY OF MARINGÁ   (Brazil)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Fusarium spp.; Glyphosate; Glyphosate resistant soybean (Glycine max L.); Indoleacetic acid; Mn; Plant biomass; Rhizobacteria

Indexed keywords

AMINO ACIDS; BACTERIA; FUNGI; HERBICIDES; NITROGEN FIXATION; SILT;

FUSARIUM; FUSARIUM SPP.; GLYCINE MAX L; GLYPHOSATE-RESISTANT; GLYPHOSATE-RESISTANT SOYBEAN (GLYCINE MAX L); GLYPHOSATES; INDOLEACETIC ACID; MN; PLANT BIOMASS; RHIZOBACTERIA;

ECOLOGY;

GLYPHOSATE;

BIOCHEMISTRY; CROP PRODUCTION; CROP YIELD; CROPPING PRACTICE; CULTIVAR; GLYPHOSATE; HARVESTING; HORMONE; MICROBIAL COMMUNITY; PESTICIDE RESISTANCE; PHYTOMASS; RHIZOBACTERIUM; RHIZOSPHERE; ROOT COLONIZATION; SILTY LOAM; SOYBEAN; WEED CONTROL; YIELD RESPONSE;

ARTICLE; BIOMASS; CULTIVAR; DRY WEIGHT; FUSARIUM; GREENHOUSE; GROWTH CURVE; HERBICIDE RESISTANCE; LOAM SOIL; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; NONHUMAN; ORGANISMAL INTERACTION; PLANT GROWTH; PLANT ROOT; PSEUDOMONADACEAE; RHIZOSPHERE; SHOOT; SOYBEAN;

FUSARIUM; GLYCINE MAX; PSEUDOMONAS FLUORESCENS GROUP; RHIZOBIALES;

EID: 78650083132     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2010.04864.x     Document Type: Article

References (50)

1. Araújo, A.S.F., Monteiro, R.T.R. and Abarkeli, R.B. (2003) Effect of glyphosate on the microbial activity of two Brazilian soils. Chemosphere 52, 799-804.
2. Bott, S., Tesfamariam, T., Candan, H., Cakmak, I., Romheld, V. and Neumann, G. (2008) Glyphosate-induced impairment of plant growth and micronutrient status in glyphosate-resistant soybean (Glycine max L.). Plant Soil 312, 185-194.
3. Bric, J.M., Bostock, R.M. and Silverstone, S.E. (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57, 535-538.
4. Castro, J.V., Peralba, M.C.R. and Ayub, M.A.Z. (2007) Biodegradation of the herbicide glyphosate by filamentous fungi in platform shaker and batch bioreactor. J Environ Sci Health 42, 883-886.
5. Cerdeira, A.L. and Duke, S.O. (2006) The current status and environmental impacts of glyphosate-resistant crops: a review. J Environ Qual 35, 1633-1658.
6. Clarkson, D.T. (1988) The uptake and translocation of manganese by plant roots. In Manganese in Soils and Plants ed. Graham, R.D., Hannam, R.J. and Uren, N.C. pp. 101-111. Boston: Kluwer Academic Publishers.
7. Duke, S.O. (2005) Taking stock of herbicide-resistant crops ten years after introduction. Pest Manag Sci 61, 211-218.
8. Franz, J.E., Mao, M.K. and Sikorski, J.A. (1997) Glyphosate: A Unique Global Herbicide; ACS Monograph 189. Washington, DC: American Chemical Society.
9. Gazziero, D.L.P., Adegas, F. and Voll, E. (2008) Glifosate e soja transgênica. p. 4. Londrina: Embrapa Soja, Circular Técnica 60.
10. Gordon, S.A. and Weber, R.P. (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26, 192-195.
11. Gould, W.D., Hagedorn, C., Bardinelli, T.R. and Zablotowicz, R.M. (1985) New selective medium for enumeration and recover of fluorescent pseudomonads from various habitats. Appl Environ Microbiol, 49, 29-32.
12. Gressel, J. (2002) Molecular Biology of Weed Control. p. 504. London, UK: Taylor & Francis Group.
13. Harper, M. (2007) The Review of the Moratorium on GM Canola. Australia. 45, 1-36.
14. Huber, D.M. and Graham, R.D. (1992) Techniques for studying nutrient-disease interactions. In Methods for Research on Soilborne Phytopathogens ed. Singleton, L.L., Mihail, J.D. and Rush, C.M. pp. 204-214. St. Paul, Minnesota: American Phytopathological Society.
15. Huber, D.M., Leuck, J.D., Smith, W.C. and Christmas, E.P. (2004) Induced manganese deficiency in GM soybeans. In: Proceedings of the thirty-fourth North Central Extension - Industry Soil Fertility Conference, Vol. 20, pp. 80-83. Des Moines, IA, USA, November 2004. Brookings, SD: Potash & Phosphate Institute.
16. Johal, G.S. and Huber, D.M. (2009) Glyphosate effects on diseases of plants. Eur J Agron 31, 144-152.
17. Johal, G.S. and Rahe, J.E. (1988) Glyphosate, hypersensitivity and phytoalexin accumulation in the incompatible bean anthracnose host-parasite interaction. Physiol Mol Plant Pathol, 32, 267-281.
18. Kennedy, A.C. (1994) Carbon utilization and fatty acid profiles for characterization of bacteria. In Methods of Soil Analysis, Part 2 - Microbiological and Biochemical Properties ed. Weaver, R.W., Angle, J.S. and Bottomley, P.S. pp. 543-556. Madison, Wisconsin: Soil Science Society of America.
19. Khalid, A., Arshad, M. and Zahir, Z.A. (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96, 473-480.
20. Kim, S.-J. (2006) Rhizobacterial populations of glyphosate-resistant soybean (Glycine max) as affected by glyphosate and foliar amendment. Korean J Environ Agric 25, 262-267.
21. King, A.C., Purcell, L.C. and Vories, E.D. (2001) Plant growth and nitrogenase activity of glyphosate-tolerant soybean in response to glyphosate applications. Agron J 93, 179-186.
22. Kremer, R.J. and Means, N.E. (2009) Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms. Eur J Agron 31, 153-161.
23. Kremer, R.J., Means, N.E. and Kim, S.J. (2005) Glyphosate affects soybean root exudation and rhizosphere microorganisms. Int J Environ Anal Chem 85, 1165-1174.
24. Kuklinsky-Sobral, J., Welington, L.A., Mendes, R., Pizzirani-Kleiner, A.A. and Azevedo, J.L. (2005) Isolation and characterization of endophytic bacteria from soybean (Glycine max) grown in soil treated with glyphosate herbicide. Plant Soil 273, 91-99.
25. Lévesque, C.A., Rahe, J.E. and Eaves, D.M. (1993) Fungal colonization of glyphosate-treated seedlings using a new root plating technique. Mycol Res 97, 299-306.
26. Marschner, H. (1988) Mechanisms of manganese acquisition by roots from soils. In Manganese in Soils and Plants ed. Graham, R.D., Hannam, R.J. and Uren, N.C. pp. 191-204. Boston: Kluwer Academix Publishers.
27. Marschner, H. (1995) Mineral Nutrition of Higher Plants, 2nd edn. p. 889. London: Academic Press.
28. Means, N.E. and Kremer, R.J. (2007) Influence of soil moisture on root colonization of glyphosate-treated soybean by Fusarium species. Commun Soil Sci Plant Anal 38, 1713-1720.
29. Mijangos, I., Becerril, J.M., Albizu, I., Epelde, L. and Garbisu, C. (2009) Effects of glyphosate on rhizosphere soil microbial communities under two different plant compositions by cultivation-dependent and -independent methodologies. Soil Biol Biochem 41, 505-513.
30. Nash, S.M. and Snyder, W.C. (1962) Quantitative estimations by plate counts of propagules of the bean root rot Fusarium in the field. Phytopathology 52, 567-572.
31. Nelson, P.E., Toussoun, T.A. and Marasas, W.F.O. (1983) Fusarium Species: An Illustrated Manual for Identification. University Park, Pennsylvania: Pennsylvania State University Press.
32. Padgette, S.R., Kolacz, K.H., Delannay, X., Re, D.B., La Vallee, B.J., Tinius, C.N. and Rhodes, W.K. (1995) Development, identification, and characterization of a glyphosate-tolerant soybean line. Crop Sci 35, 1451-1461.
33. Patten, D.L. and Glick, B.R. (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42, 207-220.
34. Reddy, K.N. and Zablotowicz, R.M. (2003) Glyphosate-resistant soybean response to various salts of glyphosate and glyphosate accumulation in soybean nodules. Weed Sci 51, 496-502.
35. Reddy, K.N., Hoagland, R.E. and Zablotowicz, R.M. (2001) Effect of glyphosate on growth, chlorophyll, and nodulation in glyphosate-resistant and susceptible soybean (Glycine max) varieties. J New Seeds 2, 37-52.
36. Reddy, K.N., Rimando, A.M. and Duke, S.O. (2004) Aminomethylphosphonic acid, a metabolite of glyphosate, causes injury in glyphosate-treated, glyphosate-resistant soybean. J Agric Food Chem 52, 5139-5143.
37. Rengel, Z. (1997) Root exudation and microflora populations in rhizosphere of crop genotypes differing in tolerance to micronutrient deficiency. Plant Soil 196, 255-260.
38. Schroth, M.N. and Hancock, J.G. (1982) Disease-suppressive soil and root-colonizing bacteria. Science 216, 1376-1381.
39. Schroth, M.N., Hildebrand, D.C. and Panopoulos, N. (2006) Phytopathogenic pseudomonads and related plant-associated pseudomonads. Prokaryotes 6, 714-740.
40. Schulz, A., Krüper, A. and Amrhein, N. (1985) Differential sensitivity of bacterial 5-enolpyruvylshikimate-3-phosphate synthases to the herbicide glyphosate. FEMS Microbiol Lett 28, 297-301.
41. Shapiro, S.S. and Wilk, M.B. (1965) An analysis of variance test for normality. Biometrika 52, 591-611.
42. Skovgaard, K., Nireberg, H.I., O'Donnell, K. and Rosendahl, S. (2001) Evolution of Fusarium oxysporum f. sp. vasinfectum races inferred from multigene genealogies. Phytopathology, 91, 1231-1237.
43. Taiz, L. and Zeiger, E. (1998) Plant Physiology, 2nd edn. Sunderland, MA: Sinauer Associates.
44. Thompson, I.A. and Huber, D.M. (2007) Manganese and plant disease. In Mineral Nutrition and Plant Disease ed. Datnoff, L.E., Elmer, W.E. and Huber, D.M. pp. 139-153. St. Paul, MN: American Phytopathological Society.
45. Treseder, K.K., Morris, S.J. and Allen, M.F. (2005) The contribution of root exudates, symbionts, and detritus to carbon sequestration in the soil. In Roots and Soil Management: Interactions between Roots and the Soil ed. Zobel, R.W. and Wright, S.F. pp. 145-162. Madison, Wisconsin: American Society of Agronomy.
46. Wardle, D.A. and Parkinson, D. (1992) The influence of the herbicide glyphosate on interspecific interactions between four fungal species. Mycol Res 96, 180-186.
47. Zablotowicz, R.M. and Reddy, K.N. (2007) Nitrogenase activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean. Crop Prot 26, 370-376.
48. Zobiole, L.H.S., Bonini, E.A., Oliveira, R.S. Jr, Kremer, R.J. and Ferrarese-Filho, O. (2010a) Glyphosate affects lignin content and amino acid production in glyphosate-resistant soybean. Acta Physiol Plant. doi:
49. Zobiole, L.H.S., Oliveira., R.S. Jr, Huber, D.M., Constantin, J., De Castro, C., Oliveira, F.A. and Oliveira, A. Jr (2010b) Glyphosate reduces shoot concentration of mineral nutrients in glyphosate-resistant soybeans. Plant Soil 328, 57-69.
50. Zobiole, L.H.S., Kremer, R.J., Oliveira, R.S. Jr and Constantin, J. (2010c) Glyphosate affects photosynthesis in first and second generation of glyphosate-resistant soybeans. Plant Soil. doi: