Cropping practices modulate the impact of glyphosate on arbuscular mycorrhizal fungi and rhizosphere bacteria in agroecosystems of the semiarid prairie

Canadian Journal of Microbiology

Volumn 58, Issue 8, 2012, Pages 990-1001

  Sheng, Min ^a,b   Hamel, Chantal ^b   Fernandez, Myriam R ^b  

^a NORTHWEST A F UNIVERSITY   (China)

^b SWIFT CURRENT RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

Arbuscular mycorrhiza fungi; Cropping practices; Glyphosate; Rhizosphere microbial community; Tillage

Indexed keywords

3 PHOSPHOSHIKIMATE 1 CARBOXYVINYLTRANSFERASE; AMMONIA; BIOLOGICAL MARKER; FATTY ACID; GLYPHOSATE; PHOSPHOLIPID;

AGRICULTURAL ECOSYSTEM; ARBUSCULAR MYCORRHIZA; BACTERIUM; CROPPING PRACTICE; FUNGUS; GLYPHOSATE; GROWTH RATE; MICROBIAL COMMUNITY; PRAIRIE; RHIZOSPHERE; SEMIARID REGION; SOIL MICROORGANISM; TILLAGE; WHEAT;

AGROECOSYSTEM; ARBUSCULAR MYCORRHIZA; ARTICLE; BACTERIAL GROWTH; CANADA; CROPPING SYSTEM; DROUGHT; GENE SEQUENCE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; MICROBIAL COMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PEA; PLANT ENVIRONMENT INTERACTION; PRAIRIE; PRIORITY JOURNAL; RHIZOSPHERE BACTERIUM; SEMIARID CLIMATE; SOIL FERTILITY; SOIL ORGANISM; TILLAGE; WHEAT;

3-PHOSPHOSHIKIMATE 1-CARBOXYVINYLTRANSFERASE; AGRICULTURE; BACTERIA; CANADA; ECOSYSTEM; FUNGI; GLYCINE; MYCORRHIZAE; PEAS; RHIZOSPHERE; SOIL MICROBIOLOGY; TRITICUM;

CANADA;

ARBUSCULAR; BACTERIA (MICROORGANISMS); FUNGI; NEGIBACTERIA; PISUM SATIVUM; TRITICUM AESTIVUM; TRITICUM TURGIDUM SUBSP. DURUM;

EID: 84864774989     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/W2012-080     Document Type: Article

References (66)

1. Alexa, E., Sumalan, R., Negrea, M., Bragea, M., Poiana, M.A., Radulov, I., and Lazureanu, A. 2010. Studies on the biodegradation capacity of 14C-labelled glyphosate in vine plantation soils. J. Food Agric. Environ. 8(2): 1193-1198.
2. Allison, V.J., Miller, R.M., Jastrow, J.D., Matamala, R., and Zak, D.R. 2005. Changes in soil microbial community structure in a tallgrass prairie chronosequence. Soil Sci. Soc. Am. J. 69(5): 1412-1421. doi:10.2136/sssaj2004.0252.
3. Altieri, M.A. 1999. The ecological role of biodiversity in agroecosystems. Agric. Ecosyst. Environ. 74(1-3): 19-31. doi:10.1016/S0167-8809(99)00028-6.
4. Ayres, K.W., Acton, D.F., and Ellis, J.G. 1985. The soils of the Swift Current Map Area 72J Saskatchewan. Saskatchewan Institute of Pedology Publication S6. University of Saskatchewan, Saskatoon. Available from http://sis.agr.gc.ca/cansis/publications/surveys/sk/sks6/sks6_report.pdf.
5. Baumgartner, K., Fujiyoshi, P., Smith, R., and Bettiga, L. 2010. Weed flora and dormant-season cover crops have no effects on arbuscular mycorrhizae of grapevine. Weed Res. 50(5): 456-466. doi:10.1111/j.1365-3180.2010.00793.x.
6. Beckie, H.J. 2011. Herbicide-resistant weed management: focus on glyphosate. Pest Manag. Sci. 67(9): 1037-1048. doi:10.1002/ps.2195. PMID:21548004.
7. Blilou, I., Ocampo, J.A., and García-Garrido, J.M. 2000. Induction of Ltp (lipid transfer protein) and Pal (phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J. Exp. Bot. 51(353): 1969-1977. doi:10.1093/jexbot/51.353.1969. PMID:11141171.
8. Borcard, D., Gillet, F., and Legendre, P. 2011. Numerical ecology with R. Springer, N.Y., USA.
9. Busse, M.D., Ratcliff, A.W., Shestak, C.J., and Powers, R.F. 2001. Glyphosate toxicity and the effects of long-term vegetation control on soil microbial communities. Soil Biol. Biochem. 33(12-13): 1777-1789. doi:10.1016/S0038-0717(01)00103-1.
10. Campos-Soriano, L., and Segundo, B.S. 2011. New insights into the signaling pathways controlling defense gene expression in rice roots during the arbuscular mycorrhizal symbiosis. Plant Signal. Behav. 6(4): 553-557. doi:10.4161/psb.6.4.14914. PMID: 21422823.
11. Campos-Soriano, L., García-Garrido, J.M., and San Segundo, B. 2010. Activation of basal defense mechanisms of rice plants by Glomus intraradices does not affect the arbuscular mycorrhizal symbiosis. New Phytol. 188(2): 597-614. doi:10.1111/j.1469-8137.2010.03386.x. PMID:20659300.
12. Cornejo, P., Azcón-Aguilar, C., Barea, J.M., and Ferrol, N. 2004. Temporal temperature gradient gel electrophoresis (TTGE) as a tool for the characterization of arbuscular mycorrhizal fungi. FEMS Microbiol. Lett. 241: 265-270. doi:10.1016/j.femsle.2004. 10.030. PMID:15598542.
13. Dai, M., Hamel, C., St. Arnaud M., He, Y., Grant, C., Lupwayi, N., et al. 2012. Arbuscular mycorrhizal fungi assemblages in Chernozem great groups revealed by massively parallel pyrosequencing. Can. J. Microbiol. 58(1): 81-92. doi:10.1139/w11-111. PMID:22220554.
14. de María, N., Becerril, J.M., García-Plazaola, J.I., Hernández, A., de Felipe, M.R., and Fernández-Pascual, M. 2006. New insights on glyphosate mode of action in nodular metabolism: role of shikimate accumulation. J. Agric. Food Chem. 54(7): 2621-2628. doi:10.1021/jf058166c. PMID:16569053.
15. Dong, X., and Reddy, G.B. 2010. Soil bacterial communities in constructed wetlands treated with swine wastewater using PCR-DGGE technique. Bioresour. Technol. 101(4): 1175-1182. doi:10.1016/j.biortech.2009.09.071. PMID:19822421.
16. Du, W., Wallis, N.G., Mazzulla, M.J., Chalker, A.F., Zhang, L., Liu, W.S., et al. 2000. Characterization of Streptococcus pneumonia 5-enolpyruvylshikimate 3-phosphate synthase and its activation by univalent cations. Eur. J. Biochem. 267(1): 222-227. doi:10.1046/j.1432-1327.2000.00994.x. PMID:10601870.
17. Fernandez, M.R., Zentner, R.P., Basnyat, P., Gehl, D., Selles, F., and Huber, D. 2009. Glyphosate associations with cereal diseases caused by Fusarium spp. in the Canadian Prairies. Eur. J. Agron. 31(3): 133-143. doi:10.1016/j.eja.2009.07.003.
18. Fitzgibbon, J.E., and Braymer, H.D. 1990. Cloning of a gene from Pseudomonas sp. strain PG2982 conferring increased glyphosate resistance. Appl. Environ. Microbiol. 56(11): 3382-3388. PMID: 2268152.
19. Frostegård, Å., Tunlid, A., and Bååth, E. 2011. Use and misuse of PLFA measurements in soils. Soil Biol. Biochem. 43(8): 1621-1625. doi:10.1016/j.soilbio.2010.11.021.
20. Funke, T., Han, H., Healy-Fried, M.L., Fischer, M., and Schönbrunn, E. 2006. Molecular basis for the herbicide resistance of Roundup Ready crops. Proc. Natl. Acad. Sci. U.S.A. 103(35): 13010-13015. doi:10.1073/pnas.0603638103. PMID:16916934.
21. Gianinazzi, S., Gollotte, A., Binet, M.-N., van Tuinen, D., Redecker, D., and Wipf, D. 2010. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza, 20(8): 519-530. doi:10.1007/s00572-010-0333-3. PMID:20697748.
22. Giovannetti, M., and Mosse, B. 1980. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 84(3): 489-500. doi:10.1111/j.1469-8137.1980.tb04556.x.
23. Gorlach-Lira, K., Stefaniak, O., Slizak, W., and Owedyk, I. 1997. The response of forest soil microflora to the herbicide formulations Fusilade and Roundup. Microbiol. Res. 152(4): 319-329. doi:10.1016/S0944-5013(97)80047-X.
24. Haney, R.L., Senseman, S.A., Hons, E.M., and Zuberer, D.A. 2000. Effect of glyphosate on soil microbial activity and biomass. Weed Sci. 48(1): 89-93. doi:10.1614/0043-1745(2000)048[0089: EOGOSM]2.0.CO;2.
25. He, M., Nie, Y.F., and Xu, P. 2003. A T42M substitution in bacterial 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) generates enzymes with increased resistance to glyphosate. Biosci. Biotechnol. Biochem. 67(6): 1405-1409. doi:10.1271/bbb.67.1405. PMID:12843673.
26. Helgason, T., Daniell, T.J., Husband, R., Fitter, A.H., and Young, J.P. W. 1998. Ploughing up the wood-wide web? Nature, 394(6692): 431. doi:10.1038/28764. PMID:9697763.
27. Herrera Medina, M.J., Gagnon, H., Piché, Y., Ocampo, J.A., García Garrido, J.M., and Vierheilig, H. 2003. Root colonization by arbuscular mycorrhizal fungi is affected by the salicylic acid content of the plant. Plant Sci. 164(6): 993-998. doi:10.1016/S0168-9452(03)00083-9.
28. Hobbs, P.R., Sayre, K., and Gupta, R. 2008. The role of conservation agriculture in sustainable agriculture. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363(1491): 543-555. doi:10.1098/rstb.2007.2169. PMID:17720669.
29. Irvine, I.C., Witter, M.S., Brigham, C.A., and Martiny, J.B.H. 2011. Relationships between methylobacteria and glyphosate with native and invasive plant species: implications for restoration. Restor. Ecol. no. doi:10.1111/j.1526-100X.2011.00850.x.
30. Johal, G.S., and Huber, D.M. 2009. Glyphosate effects on diseases of plants. Eur. J. Agron. 31(3): 144-152. doi:10.1016/j.eja.2009.04.004.
31. Kowalchuk, G.A., Gerards, S., and Woldendorp, J.W. 1997. Detection and characterization of fungal infections of Ammophila arenaria (marram grass) roots by denaturing gradient gel electrophoresis of specifically amplified 18S rDNA. Appl. Environ. Microbiol. 63(10): 3858-3865. PMID:9327549.
32. Kremer, R.J., and Means, N.E. 2009. Glyphosate and glyphosateresistant crop interactions with rhizosphere microorganisms. Eur. J. Agron. 31(3): 153-161. doi:10.1016/j.eja.2009.06.004.
33. Legendre, P., and Legendre, L. 1998. Numerical ecology. Developments in environmental modelling 20. Elsevier, Amsterdam, Netherlands.
34. Liu, P.P., Yang, Y., Pichersky, E., and Klessig, D.F. 2010. Altering expression of benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMPtriggered immunity in Arabidopsis. Mol. Plant-Microbe Interact. 23(1): 82-90. doi:10.1094/MPMI-23-1-0082. PMID:19958141.
35. Liu, L., Gan, Y., Bueckert, R., and van Rees, K. 2011. Rooting systems of oilseed and pulse crops I: temporal growth patterns across the plant developmental periods. Field Crops Res. 122(3): 256-263. doi:10.1016/j.fcr.2011.04.002.
36. Lupwayi, N.Z., Clayton, G.W., Hanson, K.G., Rice, W.A., and Biederbeck, V.O. 2004. Endophytic rhizobia in barley, wheat and canola roots. Can. J. Plant Sci. 84(1): 37-45. doi:10.4141/P03-087.
37. Malty, J.D., Siqueira, J.O., and Moreira, F.M.S. 2006. Effects of glyphosate on soybean symbiotic microorganisms, in culture media and in greenhouse. Pesquisa Agropecu. Bras. 41(2): 285-291. doi:10.1590/S0100-204X2006000200013.[In Spanish.]
38. McCune, B., and Grace, J.B. 2002. Analysis of ecological communities. MJM Software Design, Gleneden Beach, Oreg., USA.
39. Mujica, M.T., Fracchia, S., Ocampo, J.A., and Godeas, A. 1999. Influence of the herbicides chlorsulfuron and glyphosate on mycorrhizal soybean intercropped with the weeds Brassica campestris or Sorghum halepensis. Symbiosis, 27(1): 73-81.
40. Nayyar, A., Hamel, C., Forge, T., Selles, F., Jefferson, P.G., Hanson, K., and Germida, J. 2008. Arbuscular mycorrhizal fungi and nematodes are involved in negative feedback on a dual culture of alfalfa and Russian wildrye. Appl. Soil Ecol. 40(1): 30-36. doi:10.1016/j.apsoil.2008.03.004.
41. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., O'Hara, R.B., Simpson, G.L., et al. 2011. vegan: community ecology package. R package version 1.17-11. Available from http://cran.r-project.org/web/packages/vegan/index.html
42. Pasaribu, A., Mohamad, R.B., Awang, Y., Othman, R., and Puteh, A. 2011. Growth and development of symbiotic arbuscular mycorrhizal fungi, Glomus mosseae (Nicol., and Gerd.), in alachlor and glyphosate treated soils. Afr. J. Biotechnol. 10(55): 11 520-11 526. [Available from http://www.academicjournals.org/AJB.]
43. Petersen, S.O., and Klug, M.J. 1994. Effects of sieving, storage, and incubation temperature on the phospholipid fatty acid profile of a soil microbial community. Appl. Environ. Microbiol. 60(7): 2421-2430. PMID:16349325.
44. Pivato, B., Offre, P., Marchelli, S., Barbonaglia, B., Mougel, C., Lemanceau, P., and Berta, G. 2009. Bacterial effects on arbuscular mycorrhizal fungi and mycorrhiza development as influenced by the bacteria, fungi, and host plant. Mycorrhiza, 19(2): 81-90. doi:10.1007/s00572-008-0205-2. PMID:18941805.
45. Potts, M., Slaughter, S.M., Hunneke, F.-U., Garst, J.F., and Helm, R.F. 2005. Desiccation tolerance of prokaryotes: application of principles to human cells. Integr. Comp. Biol. 45(5): 800-809. doi:10.1093/icb/45.5.800. PMID:21676831.
46. Powell, H.A., Kerby, N.W., and Rowell, P. 1991. Natural tolerance of cyanobacteria to the herbicide glyphosate. New Phytol. 119(3): 421-426. doi:10.1111/j.1469-8137.1991.tb00042.x.
47. Powell, J.R., Campbell, R.G., Dunfield, K.E., Gulden, R.H., Hart M.M., Levy-Booth, D.J., et al. 2009. Effect of glyphosate on the tripartite symbiosis formed by Glomus intraradices, Bradyrhizobium japonicum, and genetically modified soybean. Appl. Soil Ecol. 41(1): 128-136. doi:10.1016/j.apsoil.2008.10.002.
48. Priestman, M.A., Funke, T., Singh, I.M., Crupper, S.S., and Schönbrunn, E. 2005. 5-Enolpyruvylshikimate-3-phosphate synthase from Staphylococcus aureus is insensitive to glyphosate. FEBS Lett. 579(3): 728-732. doi:10.1016/j.febslet.2004.12.057. PMID:15670836.
49. R Development Core Team. 2011. R: alanguage and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.r-project.org/.
50. Ratcliff, A.W., Busse, M.D., and Shestak, C.J. 2006. Changes in microbial community structure following herbicide (glyphosate) additions to forest soils. Appl. Soil Ecol. 34(2-3): 114-124. doi:10.1016/j.apsoil.2006.03.002.
51. Roberts, C.W., Roberts, F., Lyons, R.E., Kirisits, M.J., Mui, E.J., Finnerty, J., et al. 2002. The shikimate pathway and its branches in apicomplexan parasites. J. Infect. Dis. 185(Suppl. 1): S25-S36. doi:10.1086/338004. PMID:11865437.
52. SAS Institute Inc. 2001. SAS/STAT software. Version 9.1 [computer program]. SAS Institute Inc., Cary, N.C., USA.
53. Savin, M.C., Purcell, L.C., Daigh, A., and Manfredini, A. 2009. Response of mycorrhizal infection to glyphosate applications and P fertilization in glyphosate-tolerant soybean, maize, and cotton. J. Plant Nutr. 32(10): 1702-1717. doi:10.1080/01904160903150941.
54. Schulz, A., Krüper, A., and Kruper, A. 1985. Differential sensitivity of bacterial 5-enolpyruvylshikimate-3-phosphate synthases to the herbicide glyphosate. FEMS Microbiol. Lett. 28(3): 297-301. doi:10.1111/j.1574-6968.1985.tb00809.x.
55. Schwarzott, D., and Schüßler, A. 2001. A simple and reliable method for SSU rRNA gene DNA extraction, amplification, and cloning from single AM fungal spores. Mycorrhiza, 10(4): 203-207. doi:10.1007/PL00009996.
56. Siddiqui, Z.A., and Akhtar, M.S. 2008. Synergistic effects of antagonistic fungi and a plant growth promoting rhizobacterium, an arbuscular mycorrhizal fungus, or composted cow manure on populations of Meloidogyne incognita and growth of tomato. Biocontrol Sci. Technol. 18(3): 279-290. doi:10.1080/09583150801896043.
57. Simon, L., Lalonde, M., and Bruns, T.D. 1992. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl. Environ. Microbiol. 58(1): 291-295. PMID:1339260.
58. Spring, S., Schulze, R., Overmann, J., and Schleifer, K.H. 2000. Identification and characterization of ecologically significant prokaryotes in the sediment of freshwater lakes: molecular and cultivation studies. FEMS Microbiol. Rev. 24(5): 573-590. doi:10.1111/j.1574-6976.2000.tb00559.x. PMID:11077151.
59. Steinrücken, H.C., and Amrhein, N. 1980. The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl-shikimic acid-3-phosphate synthase. Biochem. Biophys. Res. Commun. 94(4): 1207-1212. doi:10.1016/0006-291X(80)90547-1. PMID:7396959.
60. Sundh, I., Nilsson, M., and Borga, P. 1997. Variation in microbial community structure in two boreal peatlands as determined by analysis of phospholipid fatty acid profiles. Appl. Environ. Microbiol. 63(4): 1476-1482. PMID:16535574.
61. Tanney, J.B., and Hutchison, L.J. 2010. The effects of glyphosate on the in vitro linear growth of selected microfungi from a boreal forest soil. Can. J. Microbiol. 56(2): 138-144. doi:10.1139/W09-122. PMID:20237575.
62. Vierheilig, H., and Piché, Y. 1998. A modified procedure for staining arbuscular mycorrhizal fungi in roots. J. Plant Nutr. Soil Sci. 161(5): 601-602. doi:10.1002/jpln.1998.3581610515.
63. Wardle, D.A., and Parkinson, D. 1990a. Effects of three herbicides on soil microbial biomass and activity. Plant Soil, 122(1): 21-28. doi:10.1007/BF02851906.
64. Wardle, D.A., and Parkinson, D. 1990b. Influence of the herbicide glyphosate on soil microbial community structure. Plant Soil, 122(1): 29-37. doi:10.1007/BF02851907.
65. White, D.C., Stair, J.O., and Ringelberg, D.B. 1996. Quantitative comparisons of in situ microbial biodiversity by signature biomarker analysis. J. Ind. Microbiol. 17(3-4): 185-196. doi:10. 1007/BF01574692.
66. Zentner, R.P., Lafond, G.P., Derksen, D.A., and Campbell, C.A. 2002. Tillage method and crop diversification: effect on economic returns and riskiness of cropping systems in a thin black Chernozem of the Canadian Prairies. Soil Tillage Res. 67(1): 9-21. doi:10.1016/S0167-1987(02)00028-4.