Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms

European Journal of Agronomy

Volumn 31, Issue 3, 2009, Pages 153-161

  Kremer, Robert J ^a   Means, Nathan E ^b  

^a UNIVERSITY OF MISSOURI   (United States)

^b Department of Computer and Mathematical Sciences   (United States)

Author keywords

Fusarium spp.; Genetically modified crop; Glycine max (L.) Merr.; Maize; Microbial ecology; Mn transformation; Polyphasic microbial analyses; Pseudomonad; Soybean; Zea mays L.

Indexed keywords

ANTAGONISM; CROP PRODUCTION; CULTIVAR; FUNGUS; GERMINATION; GLYPHOSATE; GROWING SEASON; HOST-PATHOGEN INTERACTION; MAIZE; MANGANESE; MICROBIAL ECOLOGY; NODULATION; NUTRIENT AVAILABILITY; PESTICIDE RESISTANCE; PROPAGULE; RHIZOBACTERIUM; RHIZOSPHERE; ROOT COLONIZATION; SOIL MICROORGANISM; SOYBEAN; TEMPORAL RECORD; TRANSGENIC PLANT;

MISSOURI; NORTH AMERICA; UNITED STATES;

BACTERIA (MICROORGANISMS); FUNGI; FUSARIUM; GLYCINE MAX; ZEA MAYS;

EID: 69249206582     PISSN: 11610301     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eja.2009.06.004     Document Type: Article

References (91)

1. Aoki T., O'Donnell K., Homma Y., and Lattanzi A.R. Sudden-death syndrome of soybean is caused by two morphologically and phylogenetically distinct species within the Fusarium solani species complex-F. virguliforme in North America and F. tucumaniae in South America. Mycologia 95 (2003) 660-684
2. Arregui M.C., Lenardon A., Sanchez D., Maitre A.M., Scotta R., and Enrique S. Monitoring glyphosate residues in transgenic glyphosate-resistant soybean. Pest Manage. Sci. 60 (2003) 163-166
3. Azevedo J.L., and Araujo W.L. Genetically modified crops: environmental and human health concerns. Mutat. Res. 544 (2003) 223-233
4. Benbrook, C.M., 2004. Genetically engineered crops and pesticide use in the United States: the first nine years. Technical Paper No. 7. BioTech InfoNet.
5. Bohm G.M., Alves B.J.R., Urquiaga S., Boddey R.M., Xavier G.R., Hax F., and Rombaldi C.V. Glyphosate- and imazethapyr-induced effects on yield, nodule mass and biological nitrogen fixation in field-grown glyphosate-resistant soybean. Soil Biol. Biochem. 41 (2009) 420-422
6. Brammall R.A., and Higgins V.J. The effect of glyphosate on resistance of tomato to Fusarium crown and root rot disease and on the formation of host structural defensive barriers. Can. J. Bot. 66 (1988) 1547-1555
7. Broeckling C.D., Broz A.K., Bergelson J., Manter D.K., and Vivanco J.M. Root exudates regulate soil fungal community composition and diversity. Appl. Environ. Microbiol. 74 (2008) 738-744
8. Castro J.V., Peralba M.C.R., and Ayub M.A.Z. Biodegradation of the herbicide glyphosate by filamentous fungi in platform shaker and batch bioreactor. J. Environ. Sci. Health B 42 (2007) 883-886
9. Cerdeira A.L., and Duke S.O. The current status and environmental impacts of glyphosate-resistant crops: a review. J. Environ. Qual. 35 (2006) 1633-1658
10. 14C-labelled glyphosate. New Phytol. 83 (1979) 17-22
11. Descalzo R.C., Punja Z.K., Lévesque C.A., and Rahe J.E. Glyphosate treatment of bean seedlings causes short-term increases in Pythium populations and damping off potential in soils. Appl. Soil Ecol. 8 (1998) 25-33
12. Dick R.E., and Quinn J.P. Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation. Appl. Microbiol. Biotechnol. 43 (1995) 545-550
13. Duke S.O. Herbicide Resistant Crops: Agricultural, Environmental, Economic, Regulatory, and Technical Aspects (1996), CRC Press, Boca Raton, FL
14. Duke S.O., Baerson S.R., and Rimando A.M. Herbicides: glyphosate. In: Plimmer J.R., Gammon D.W., and Ragsdale N.N. (Eds). Encyclopedia of Agrochemicals, (2003), John Wiley & Sons, New York. http://www.mrw.interscience.wiley.com/eoa/articles/agr119/frame.html (Accessed September 12, 2008)
15. Duke S.O., Rimando A.M., Pace P.F., Reddy K.N., and Smeda R.J. Isoflavone, glyphosate, and aminomethylphosphonic acid levels in seeds of glyphosate-treated, glyphosate-resistant soybean. J. Agric. Food Chem. 51 (2003) 340-344
16. Duke S.O., and Powles S.B. Glyphosate: a once-in-a-century herbicide. Pest Manage. Sci. 64 (2008) 319-325
17. Eker S., Ozturk L., Yazici A., Erenoglu B., Römheld V., and Cakmak I. Foliar-applied glyphosate substantially reduced uptake and transport of iron and manganese in sunflower (Helianthus annuus L.) plants. J. Agric. Food Chem. 54 (2006) 10019-10025
18. El-Shatnawi M.K.J., and Makhadmeh I.M. Ecophysiology of the plant-rhizosphere system. J. Agron. Crop Sci. 187 (2001) 1-9
19. Fomsgaard I.S., Spilid N.H., and Felding G. Leaching of pesticides through normal-tillage soil-a lysimeter study. II. Glyphosate. J. Environ. Sci. Health B 38 (2003) 19-35
20. Franz J.E., Mao M.K., and Sikorski J.A. Glyphosate: A Unique Global Herbicide. ACS Monograph 189 (1997), American Chemical Society, Washington, DC, USA
21. Funke T., Han H., Healy-Fried M.L., Fischer M., and Schönbrunn E. Molecular basis for the herbicide resistance of Roundup Ready crops. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 13010-13015
22. Gimsing A.L., Borggaard O.K., Jacobsen O.S., Aamand J., and Sørensen J. Chemical and microbiological soil characteristics controlling glyphosate mineralization in Danish surface soils. Appl. Soil Ecol. 27 (2004) 233-242
23. Gould W.D., Hagedorn C., Bardinelli T.R., and Zablotowicz R.M. New selective medium for enumeration and recovery of fluorescent pseudomonads from various habitats. Appl. Environ. Microbiol. 49 (1985) 28-32
24. Grayston S.J., Wang S.Q., Campbell C.D., and Edwards A.C. Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol. Biochem. 30 (1998) 369-378
25. Griffiths B.S., Ritz K., Ebblewhite N., and Dobson G. Soil microbial community structure: effects of substrate loading rates. Soil Biol. Biochem. 31 (1999) 145-153
26. Haney R.L., Senseman S.A., Hons F.M., and Zuberer D.A. Effect of glyphosate on soil microbial activity and biomass. Weed Sci. 48 (2000) 89-93
27. Harley J.P., and Prescott L.M. Laboratory Exercises in Microbiology. 4th ed. (1999), McGraw-Hill, Boston, MA pp. 95-98
28. Hart M.M., Powell J.R., Gulden R.H., Dunfield K.E., Pauls K.P., Swanton C.J., Klironomos J.N., Antunes P.M., Koch A.M., and Trevors J.T. Separating the effect of crop from herbicide on soil microbial communities in glyphosate-resistant corn. Pedobiologia 52 (2009) 253-262
29. Huber D.M., Cheng M., and Winsor B. Association of severe Corynespora root rot of soybean with glyphosate-killed ragweed. Phytopathology 95 (2005) S45
30. Huber D.M., and Graham R.D. Techniques for studying nutrient-disease interactions. In: Singleton L.L., Mihail J.D., and Rush C.M. (Eds). Methods for Research on Soilborne Phytopathogenic Fungi (1992), APS Press, St. Paul, MN 204-214
31. Huber D.M., and McCay-Buis T.S. A multiple component analysis of the take-all disease of cereals. Plant Dis. 77 (1993) 437-447
32. James, C., 2007. Global status of commercialized biotech/GM crops: 2007. ISAAA Brief No. 37. International Service for the Acquisition of Agri-biotech Associations, Ithaca, NY, USA.
33. Johal G.S., and Huber D.M. Glyphosate effects on diseases of plants. Eur. J. Agron. 31 (2009) 144-152
34. Johal G.S., and Rahe J.E. Effects of soilborne plant-pathogenic fungi on the herbicidal action of glyphosate on bean seedlings. Phytopathology 74 (1984) 950-955
35. Jolley V.D., Hansen N.C., and Shiffler A.K. Nutritional and management related interactions with iron-deficiency stress response mechanisms. Soil Sci. Plant Nutr. 50 (2004) 973-981
36. Kawate M.K., Colwell S.G., Ogg Jr. A.G., and Kraft J.M. Effect of glyphosate-treated henbit (Lamium amplexicaule) and downy brome (Bromus tectorum) on Fusarium solani f. sp. pisi and Pythium ultimum. Weed Sci. 45 (1997) 739-743
37. Keen N.T., Holliday M.J., and Yoshikawa M. Effects of glyphosate on glyceollin production and the expression of resistance to Phytophthera megasperma f. sp. glycinea in soybean. Phytopathology 72 (1982) 1467-1470
38. Kelman A. The relationship of pathogenicity in Pseudomonas solanacearum to colony appearance on a tetrazolium chloride medium. Phytopathology 44 (1954) 693-695
39. Kennedy A.C. The rhizosphere. In: Sylvia D.M., Hartel P.G., Fuhrmann J.J., and Zuberer D.A. (Eds). Principles and Applications of Soil Microbiology. 2nd ed. (2005), Pearson-Prentice Hall, Upper Saddle River, NJ 242-262
40. Kennedy A.C. Carbon utilization and fatty acid profiles for characterization of bacteria. In: Weaver R.W., Angle J.S., and Bottomley P.S. (Eds). Methods of Soil Analysis, Part 2-Microbiological and Biochemical Properties (1994), Soil Science Society of America, Madison, WI 543-556
41. King A.C., Purcell L.C., and Vories E.D. Plant growth and nitrogenase activity of glyphosate-tolerant soybean in response to glyphosate applications. Agron. J. 93 (2001) 179-186
42. Kowalchuk G.A., Bruinsma M., and van Veen J.A. Assessing responses of soil microorganisms to GM plants. Trends Ecol. Evol. 18 (2003) 403-410
43. Kremer R.J., Means N.E., and Kim S.-J. Glyphosate affects soybean root exudation and rhizosphere microorganisms. Int. J. Environ. Anal. Chem. 85 (2005) 1165-1174
44. Kremer R.J. Soil biological processes are influenced by Roundup Ready soybean production. Phytopathology 93 (2003) S104
45. Kremer R.J., Begonia M.F.T., Stanley L., and Lanham E.T. Characterization of rhizobacteria associated with weed seedlings. Appl. Environ. Microbiol. 56 (1990) 1649-1655
46. Krzysko-Lupicka T., and Sudol T. Interactions between glyphosate and autochthonous soil fungi surviving in aqueous solution of glyphosate. Chemosphere 71 (2008) 1386-1391
47. Krzysko-Lupicka T., and Orlik A. The use of glyphosate as the sole source of phosphorus or carbon for the selection of soil-borne fungal strains capable to degrade this herbicide. Chemosphere 34 (1997) 2601-2605
48. Kuklinshy-Sobral J., Welington L.A., Mendes R., Pizzirani-Kleiner A.A., and Azevedo J.L. Isolation and characterization of endophytic bacteria from soybean (Glycine max) grown in soil treated with glyphosate herbicide. Plant Soil 273 (2005) 91-99
49. Kuklinsky-Sobral J., Araualjo W.L., Mendes R., Geraldi I.O., Pizzirani-Kleiner A.A., and Azevedo J.L. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ. Microbiol. 6 (2004) 1244-1251
50. Larson R.L., Hill A.L., Fenwick A., Kniss A.R., Hanson L.E., and Miller S.D. Influence of glyphosate on Rhizoctonia and Fusarium root rot in sugar beet. Pest Manage. Sci. 62 (2006) 1182-1192
51. Lee C.D., Penner D., and Hammerschmidt R. Influence of formulated glyphosate and activator adjuvants on Sclerotinia sclerotium in glyphosate-resistant and susceptible Glycine max. Weed Sci. 48 (2002) 710-715
52. Lévesque C.A., Rahe J.E., and Eaves D.M. Fungal colonization of glyphosate-treated seedlings using a new root plating technique. Mycol. Res. 97 (1993) 299-306
53. Lévesque C.A., and Rahe J.E. Herbicide interactions with fungal root pathogens, with special reference to glyphosate. Annu. Rev. Phytopathol. 30 (1992) 597-602
54. Lévesque C.A., Rahe J.E., and Eaves D.M. Effects of glyphosate on Fusarium spp.: its influence on root colonization of weeds, propagule density in the soil, and crop emergence. Can. J. Microbiol. 33 (1987) 354-360
55. Liphadzi K.B., Al-Khatib K., Bensch C.N., Stahlman P.W., Dille S.J., Todd T., Rice C.W., Horak M.J., and Head G. Soil microbial and nematode communities as affected by glyphosate and tillage practices in a glyphosate-resistant cropping system. Weed Sci. 53 (2005) 536-545
56. 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
57. Liu L., Punja Z.K., and Rahe J.E. Altered root exudation and suppression of induced lignification as mechanisms of predisposition by glyphosate of bean roots (Phaseolus vulgaris L.) to colonization by Pythium spp. Physiol. Mol. Plant Pathol. 51 (1997) 111-127
58. Locke M.A., Zablotowicz R.M., and Reddy K.N. Integrating soil conservation practices and glyphosate-resistant crops: impacts on soil. Pest Manage. Sci. 64 (2008) 457-469
59. Lupwayi N.Z., Harker K.N., Clayton G.W., O'Donovan J.T., and Blackshaw R.E. Soil microbial response to herbicides applied to glyphosate-resistant canola. Agric. Ecosyst. Environ. 129 (2009) 171-176
60. Lupwayi N.Z., Hanson K.G., Harker K.N., Clayton G.W., Blackshaw R.E., O'Donovan J.T., Johnson E.N., Gan Y., Irvine R.B., and Monreal M.A. Soil microbial biomass, functional diversity and enzyme activity in glyphosate-resistant wheat-canola rotations under low-disturbance direct seeding and conventional tillage. Soil Biol. Biochem. 39 (2007) 1418-1427
61. Matthysse A.G. The genus Agrobacterium. Prokaryotes 5 (2006) 91-114
62. Means, N.E., 2004. Effects of glyphosate and foliar amendments on soil microorganisms in soybean. Doctoral Dissertation. University of Missouri, Columbia, 131 pp.
63. Means N.E., and Kremer R.J. Influence of soil moisture on root colonization of glyphosate-treated soybean by Fusarium species. Comm. Soil Sci. Plant Anal. 38 (2007) 1713-1720
64. Means N.E., Kremer R.J., and Ramsier C. Effects of glyphosate and foliar amendments on activity of microorganisms in the soybean rhizosphere. J. Environ. Sci. Health B 42 (2007) 125-132
65. Meriles J.M., Vargas Gil S., Haro R.J., March G.J., and Guzmán C.A. Glyphosate and previous crop residue effect on deleterious and beneficial soil-borne fungi from peanut-corn-soybean rotations. J. Phytopathol. 154 (2006) 309-316
66. Mijangos I., Becerril J.M., Albizu I., Epelde L., and Garbisu C. Effects of glyphosate on rhizosphere soil microbial communities under two different plant compositions by cultivation-dependent and -independent methodologies. Soil Biol. Biochem. 41 (2009) 505-513
67. Nash S.M., and Snyder W.C. Quantitative estimations by plate counts of propagules of the bean root rot Fusarium in the field. Phytopathology 52 (1962) 567-572
68. Nelson E.B. Exudate molecules initiating fungal responses to seeds and roots. Plant Soil 129 (1990) 61-73
69. Nelson P.E., Toussoun T.A., and Marasas W.F.O. Fusarium Species, an Illustrated Manual for Identification (1983), Pennsylvania State University Press, University Park, PA
70. Neumann G., Kohls S., Landsberg E., Stock-Oliveira Souza K., Yamada T., and Römheld V. Relevance of glyphosate transfer to non-target plants via the rhizosphere. J. Plant Dis. Protect. 20 (2006) 963-969 (Special issue)
71. Njiti V.N., Myers Jr. O., Schroeder D., and Lightfoot D.A. Roundup Ready soybean: glyphosate effects on Fusarium solani root colonization and sudden death syndrome. Agron. J. 95 (2003) 1140-1145
72. Ozturk L., Yazici A., Eker S., Gokem O., Römheld V., and Cakmak I. Glyphosate inhibition of ferric reductase activity in iron deficient sunflower roots. New Phytol. 177 (2007) 899-906
73. Powell J.R. Linking soil organisms within food webs to ecosystem functioning and environmental change. Adv. Agron. 96 (2007) 307-349
74. Powell J.R., and Swanton C.J. A critique of studies evaluating glyphosate effects on diseases associated with Fusarium spp. Weed Res. 48 (2008) 307-318
75. 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
76. Reddy K.N., Hoagland R.E., and Zablotowicz R.M. Effect of glyphosate on growth, chlorophyll content and nodulation in glyphosate-resistant soybean (Glycine max) varieties. J. New Seeds 2 (2000) 37-52
77. Rengel Z. Root exudation and microflora populations in rhizosphere of crop genotypes differing in tolerance to micronutrient deficiency. Plant Soil 196 (1997) 255-260
78. Sanogo S., Yang X.B., and Scherm H. Effects of herbicides on Fusarium solani f. sp. glycines and development of sudden death syndrome in glyphosate-tolerant soybean. Phytopathology 90 (2000) 57-66
79. Schroth M.N., Hildebrand D.C., and Panopoulos N. Phytopathogenic pseudomonads and related plant-associated pseudomonads. Prokaryotes 6 (2006) 714-740
80. Schroth M.N., and Hancock J.G. Disease-suppressive soil and root-colonizing bacteria. Science 216 (1982) 1376-1381
81. Schulz A., Krüper A., and Amrhein N. Differential sensitivity of bacterial 5-enolpyruvylshikimate-3-phosphate synthases to the herbicide glyphosate. FEMS Microbiol. Lett. 28 (1985) 297-301
82. Simonsen L., Fomsgaard I.S., Svensmark B., and Spliid N.H. Fate and availability of glyphosate and AMPA in agricultural soil. J. Environ. Sci. Health B 43 (2008) 365-375
83. Skovgaard K., Nireberg H.I., O'Donnell K., and Rosendahl S. Evolution of Fusarium oxysporum f. sp. vasinfectum races inferred from multigene genealogies. Phytopathology 91 (2001) 1231-1237
84. Smiley R.W., Ogg Jr. A.G., and Cook R.J. Influence of glyphosate on Rhizoctonia root rot, growth, and yield of barley. Plant Dis. 76 (1992) 937-942
85. Toner B., Fakra S., Villalobos M., Warwick T., and Sposito G. Spatially resolved characterization of biogenic manganese oxide production within a bacterial biofilm. Appl. Environ. Microbiol. 71 (2005) 1300-1310
86. Thompson I.A., and Huber D.M. Manganese and plant disease. In: Datnoff L.E., Elmer W.E., and Huber D.M. (Eds). Mineral Nutrition and Plant Disease (2007), American Phytopathological Society, St. Paul, MN 139-153
87. Wardle D.A. Impacts of disturbance on detritus food webs in agroecosystems of contrasting tillage and weed management practices. Adv. Ecol. Res. 26 (1995) 105-185
88. Wardle D.A., and Parkinson D. The influence of the herbicide glyphosate on interspecific interactions between four fungal species. Mycol. Res. 96 (1992) 180-186
89. Wardle D.A., and Parkinson D. Effects of three herbicides on soil microbial biomass and activity. Plant Soil 122 (1990) 21-28
90. Zablotowicz R.M., and Reddy K.N. Nitrogen activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean. Crop Protect. 26 (2007) 370-376
91. 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