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Rhizosphere Microbial Community Dynamics in Glyphosate-Treated Susceptible and Resistant Biotypes of Giant Ragweed (Ambrosia trifida)

Published online by Cambridge University Press:  20 January 2017

Jessica R. Schafer ,
Steven G. Hallett  and
William G. Johnson
Jessica R. Schafer*
Affiliation:
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907
Steven G. Hallett
Affiliation:
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907
William G. Johnson
Affiliation:
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907
*
Corresponding author's E-mail: jessica.r.bugg@dupont.com
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Abstract

In a previous study, glyphosate-susceptible and -resistant giant ragweed biotypes grown in sterile field soil survived a higher rate of glyphosate than those grown in unsterile field soil, and the roots of the susceptible biotype were colonized by a larger number of soil microorganisms than those of the resistant biotype when treated with 1.6 kg ae ha−1 glyphosate. Thus, we concluded that soil-borne microbes play a role in glyphosate activity and now hypothesize that the ability of the resistant biotype to tolerate glyphosate may involve microbial interactions in the rhizosphere. The objective of this study was to evaluate differences in the rhizosphere microbial communities of glyphosate-susceptible and -resistant giant ragweed biotypes 3 d after a glyphosate treatment. Giant ragweed biotypes were grown in the greenhouse in unsterile field soil and glyphosate was applied at either 0 or 1.6 kg ha−1. Rhizosphere soil was sampled 3 d after the glyphosate treatment, and DNA was extracted, purified, and sequenced with the use of Illumina Genome Analyzer next-generation sequencing. The taxonomic distribution of the microbial community, diversity, genera abundance, and community structure within the rhizosphere of the two giant ragweed biotypes in response to a glyphosate application was evaluated by metagenomics analysis. Bacteria comprised approximately 96% of the total microbial community in both biotypes, and differences in the distribution of some microbes at the phyla level were observed. Select soil-borne plant pathogens (Verticillium and Xanthomonas) and plant-growth–promoting rhizobacteria (Burkholderia) present in the rhizosphere were influenced by either biotype or glyphosate application. We did not, however, observe large differences in the diversity or structure of soil microbial communities among our treatments. The results of this study indicate that challenging giant ragweed biotypes with glyphosate causes perturbations in rhizosphere microbial communities and that the perturbations differ between the susceptible and resistant biotypes. However, biological relevance of the rhizosphere microbial community data that we obtained by next-generation sequencing remains unclear.

Keywords

Glyphosategiant ragweed, Ambrosia trifida L.Glyphosate-susceptibleglyphosate-resistantmetagenomicsnext-generation sequencingsoil microorganisms
Type
Soil, Air, and Water
Information
Weed Science , Volume 62 , Issue 2 , June 2014 , pp. 370 - 381
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Altman, J, Campbell, CL (1977) Effect of herbicides on plant diseases. Annu Rev Phytopathol. 15:361–385.Google Scholar
Altschul, SF, Gish, W, Miller, W, Myers, EW, Lipman, DJ (1990) Basic local alignment search tool. J Mol Biol. 215:403–410.Google Scholar
Andrews, S (2010) FastQC: A Quality Control Tool for High Throughput Sequence Data. http://www.bioinformatics.bbsrc.ac.uk/projects/fastqc. Accessed April 29, 2013.Google Scholar
Barriuso, J, Marín, S, Mellado, RP (2010) Effect of the herbicide glyphosate on glyphosate-tolerant maize rhizobacterial communities: a comparison with pre-emergency applied herbicide consisting of a combination of acetochlor and terbuthylazine. Environ Microbiol. 12:1021–1030.Google Scholar
Bentley, R (1990) The shikimate pathway—a metabolic tree with many branches. CRC Crit Rev Biochem Mol Biol. 25:307–384.Google Scholar
Bohm, GM, Alves, BJR, Urquiaga, S, Boddey, RM, Xavier, GR, Hax, F, Rambaldi, CV (2009) Glyphosate- and imazethapyr-induced effects on yield, nodule mass and biological nitrogen fixation in field-grown glyphosate-resistant soybean. Soil Biol Biochem. 41:420–422.Google Scholar
Bromilow, RH, Chamberlain, K, Tench, AJ, Williams, RH (1993) Phloem translocation of strong acids-glyphosate, substituted phosphonic and sulfonic acids in Ricinus communis L. Pestic Sci. 37:39–47.Google Scholar
Buckley, DH, Schmidt, TM (2001) Environmental factors influencing the distribution of rRNA from Verrucomicrobia in soil. FEMS Microbiol Ecol. 35:105–112.Google Scholar
Busse, MD, Ratcliff, AW, Shestak, CJ, Powers, RF (2001) Glyphosate toxicity and the effects of long-term vegetation control on soil microbial communities. Soil Biol Biochem. 33:1777–1789.Google Scholar
Clemensson-Lindell, A, Persson, H (1992) Effect of freezing on rhizosphere and root nutrient content using two soil sampling methods. Plant Soil. 139:39–45.Google Scholar
Coupland, D, Caseley, JC (1979) Presence of 14C activity in root exudates and guttation fluid from Agropyron repens treated with 14C-labeled glyphosate. New Phytol. 83:17–22.Google Scholar
Descalzo, RC, Punja, ZK, Lévesque, CA, Rahe, JE (1998) Glyphosate treatment of bean seedlings causes short-term increases in Pythium populations and damping off potential in soils. Appl Soil Ecol. 8:25–33.Google Scholar
Dill, GM, CaJacob, CA, Padgette, SR (2008) Glyphosate-resistant crops: adoption, use, and future considerations. Pest Manag Sci. 64:326–331.Google Scholar
Duke, SO, Powles, SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci. 64:319–325.Google Scholar
Franco, DAS, Almeida, SDB, Cerdeira, AL, Duke, SO, Moraes, RM, Lacerda, ALS, Matallo, MB (2012) Evaluation of glyphosate application on transgenic soybean and its relationship with shikimic acid. Planta Daninha. 30:659–666.Google Scholar
Haney, RL, Senseman, SA, Hons, FM, Zuberer, DA (2000) Effect of glyphosate on soil microbial activity and biomass. Weed Sci. 48:89–93.Google Scholar
Haney, RL, Senseman, SA, Krutz, LJ, Hons, FM (2002) Soil carbon and nitrogen mineralization as affected by atrazine and glyphosate. Biol Fertil Soils. 35:35–40.Google Scholar
Heap, I (2013) The international survey of herbicide resistant weeds. http://www.weedscience.org. Accessed November 3, 2013.Google Scholar
Hetherington, PR, Reynolds, TL, Marshall, G, Kirkwood, RC (1999) The absorption, translocation and distribution of the herbicide glyphosate in maize expressing the CP-4 transgene. J Exp Bot. 50:1567–1576.Google Scholar
Janssen, PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol. 72:1719–1728.Google Scholar
Johal, GS, Rahe, JE (1984) Effect of soilborne plant-pathogenic fungi on the herbicidal action of glyphosate on bean seedlings. Phytopathology. 74:950–955.Google Scholar
Johal, GS, Rahe, JE (1988) Glyphosate, hypersensitivity, and phytoalexin accumulation in the incompatible bean anthracnose host–parasite interaction. Physiol Mol Plant Pathol. 32:267–281.Google Scholar
Johal, GS, Rahe, JE (1990) Role of phytoalexins in the suppression of resistance of Phaseolus vulgaris to Colletotrichum lindemuthianum by glyphosate. Can J Plant Pathol. 12:225–235.Google Scholar
Keen, NT, Holliday, MJ, Yoshikawa, M (1982) Effects of glyphosate on glyceollin production and the expression of resistance to Phytophthora megasperma f. sp. glycinea in soybean. Phytopathology. 72:1467–1470.Google Scholar
Kersters, K, De Vos, P, Gillis, M, Swings, J, Vandamme, P, Stackebrandt, E (2006) Introduction to the Proteobacteria. Pages 3–37 in Dwarkin, M, Falkow, S, Rosenberg, E, Schleifer, KH, and Stackebrandt, , eds. The Prokaryotes. 3rd edn, Volume 5. New York Springer.Google Scholar
King, CA, Purcell, LC, Vories, DE (2001) Plant growth and nitrogenase activity of glyphosate-tolerant soybean in response to foliar glyphosate applications. Agron J. 93:179–186.Google Scholar
Kremer, RJ, Means, NE, Kim, S (2005) Glyphosate affects soybean root exudation and rhizosphere micro-organisms. Int J Environ Anal Chem. 85:1165–1174.Google Scholar
Kremer, RJ, Means, NE (2009) Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms. Eur J Agron. 31:153–161.Google Scholar
Laitinen, P, Rämö, S, Siimes, K (2007) Glyphosate translocation from plants to soil—does this constitute a significant proportion of residues in soil? Plant Soil. 300:51–60.Google Scholar
Lane, M, Lorenz, N, Saxena, J, Ramsier, C, Dick, RP (2012) The effect of glyphosate on soil microbial activity, microbial community structure, and soil potassium. Pedobiologia. 55:335–342.Google Scholar
Lancaster, SH, Hollister, EB, Senseman, SA, Gentry, TJ (2010) Effects of repeated glyphosate applications on soil microbial community composition and the mineralization of glyphosate. Pest Manag Sci. 66:59–64.Google Scholar
Liesack, W, Stackebrandt, E (1992) Occurrence of novel groups of the domain bacteria as revealed by analysis of genetic material isolated from an Australian terrestrial environment. J Bacteriol. 174:5072–5078.Google Scholar
Lévesque, CA, Rahe, JE, Eaves, DM (1987) Effect of glyphosate on Fusarium spp: its influence on root colonization of weeds, propagule density in the soils, and crop emergence. Can J Plant Pathol. 33:354–360.Google Scholar
Liu, L, Punja, ZK, Rahe, JE (1995) Effect of Pythium spp. and glyphosate on phytoalexin production and excudation by bean (Phaseolus vulgaris L.) roots grown in different media. Physiol Mol Plant Pathol. 47:391–405.Google Scholar
Liu, L, Punja, ZK, Rahe, JE (1997) 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. 51:111–127.Google Scholar
Lugtenberg, B, Kamilova, F (2009) Plant-growth-promoting Rhizobacteria. Annu Rev Microbiol. 63:541–56.Google Scholar
Lupwayi, NZ, Harker, KN, Clayton, GW, O'Donovan, JT, Blackshaw, RE (2009) Soil microbial response to herbicides applied to glyphosate-resistant canola. Agric Ecosyst Environ. 129:171–176.Google Scholar
Meyer, F, Paarmann, D, D'Souza, M, Olson, R, Glass, EM, Kubal, M, Paczian, T, Rodriguez, A, Stevens, R, Wilke, A, Wilkening, J, Edwards, RA (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinf. 9:386.Google Scholar
Mijangosa, I, Becerril, JM, Albizu, I, Epelde, L, 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.Google Scholar
Moorman, TB, Becerril, JM, Lydon, J, Duke, SO (1992) Production of hydroxybenzoic acids by Bradyrhizobium japonicum strains after treatment with glyphosate. J Agric Food Chem. 40:289–293.Google Scholar
Olson, BM, Lindwall, CW (1991) Soil microbial activity under chemical fallow conditions: effects of 2,4-D and glyphosate. Soil Biol Biochem. 23:1071–1075.Google Scholar
Parks, DH, Beiko, RG (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics. 26:715–721.Google Scholar
Pollegioni, L, Schonbrunn, E, Siehl, D (2011) Molecular basis of glyphosate resistance—different approaches through protein engineering. FEBS J. 278:2753–2766.Google Scholar
Powell, JR, Campbell, RG, Dunfield, KE, Gulden, RH, Hart, MM, Levy-Booth, DJ, Klironomos, JN, Pauls, KP, Swanton, CJ, Trevors, JT, Antunes, PM (2009) Effect of glyphosate on the tripartite symbiosis formed by Glomus intraradices, Bradyrhizobium japonicum, and genetically modified soybean. Appl Soil Ecol. 41:128–136.Google Scholar
Powles, SB, Preston, C (2006) Evolved glyphosate resistance in plants: biochemical and genetic basis of resistance. Weed Technol. 20:282–289.Google Scholar
Ratcliff, AW, Busse, MD, Shestak, CJ (2006) Changes in microbial community structure following herbicide (glyphosate) additions to forest soils. Appl Soil Ecol. 34:114–124.Google Scholar
Reddy, KN, Zablotowicz, RM, (2003) Glyphosate-resistant soybean response to various salts of glyphosate and glyphosate accumulation in soybean nodules. Weed Sci. 51:496–502.Google Scholar
Robertson, RR (2010) Physiological and biochemical characterization of glyphosate resistant Ambrosia trifida L. . West Lafayette, IN Purdue University. 83 p.Google Scholar
Rodrigues, JJV, Worsham, AD, Corbin, FT (1982) Exudation of glyphosate from wheat (Triticum aestivum) plants and its effects on interplanted corn (Zea mays) and soybeans (Glycine max). Weed Sci. 30:316–320.Google Scholar
Sanogo, S, Yang, XB, Scherm, H (2000) Effects of herbicides on Fusarium solani f. sp. glycines and development of sudden death syndrome in glyphosate-tolerant soybean. Phytopathology. 90:57–66.Google Scholar
Savin, MC, Purcell, LC, Daigh, A, Manfredini, A (2009) Response of mycorrhizal infection to glyphosate applications and P fertilization in glyphosate-tolerant soybean, maize, and cotton. J Plant Nutr. 32:1702–1717.Google Scholar
Schafer, JR, Hallett, SG, Johnson, WG (2012) Response of giant ragweed (Ambrosia trifida), horseweed (Conyza canadensis), and common lambsquarters (Chenopodium album) biotypes to glyphosate in the presence and absence of soil microorganisms. Weed Sci. 60:641–649.Google Scholar
Schafer, JR, Hallett, SG, Johnson, WG (2013) Soil microbial root colonization of glyphosate-treated giant ragweed (Ambrosia trifida), horseweed (Conyza canadensis), and common lambsquarters (Chenopodium album) biotypes. Weed Sci. 61:289–295.Google Scholar
Sharon, A, Amsellem, Z, Gressel, J (1992) Glyphosate suppression of an elicited defense response: increased susceptibility of Cassia obtusifolia to a mycoherbicide. Plant Physiol. 98:654–659.Google Scholar
Smith, DA, Hallett, SG (2006) Interactions between chemical herbicides and the candidate bioherbicide Microsphaeropsis amaranthi . Weed Sci. 54:532–537.Google Scholar
Stachler, JM (2008) Characterization and management of glyphosate-resistant giant ragweed (Ambrosia trifida (L.)) and horseweed [Conyza canadensis (L.) Cronq.]. Ph.D Dissertation. Columbus, OH The Ohio State University. 124 p.Google Scholar
Stackebrandt, E, Liesack, W, Goebel, BM (1993) Bacterial diversity in a soil sample from a subtropical Australian environment as determined by 16S rDNA analysis. FASEB J. 7:232–236.Google Scholar
Steinrücken, HC, Amrhein, N (1980) The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid-3-phosphate synthase. Biochem Biophys Res Commun. 94:1207–1212.Google Scholar
Stratton, GW, Stewart, KW (1992) Glyphosate effects on microbial biomass in coniferous forest soil. Environ Toxicol Water Qual. 7:223–236.Google Scholar
[USDA-NASS] U.S. Department of Agriculture–National Agricultural Statistics Service (2012) Acreage. Washington, DC U.S. Department of Agriculture–National Agricultural Statistics Service. Pp 1–42.Google Scholar
Wardle, DA, Parkinson, D (1990a) Effects of three herbicides on soil microbial biomass and activity. Plant Soil. 122:21–28.Google Scholar
Wardle, DA, Parkinson, D (1990b) Influence of the herbicide glyphosate on soil microbial community structure. Plant Soil. 122:29–37.Google Scholar
Weaver, LM, Herrmann, KM (1997) Dynamics of the shikimate pathway in plants. Trends in Plant Sci. 2:346–351.Google Scholar
Weaver, MA, Krutz, LJ, Zablotowicz, RM, Reddy, KN (2007) Effects of glyphosate on soil microbial communities and its mineralization in a Mississippi soil. Pest Manag Sci. 63:388–393.Google Scholar
Westhoven, AM, Davis, VM, Gibson, KD, Weller, SC, Johnson, WG (2008) Field presence of glyphosate-resistant horseweed (Conyza canadensis), common lambsquarters (Chenopodium album), and giant ragweed (Ambrosia trifida) biotypes with elevated tolerance to glyphosate. Weed Technol. 22:544–548.Google Scholar
Zabaloy, MC, Garland, JL, Gómez, MA (2008) An integrated approach to evaluate the impacts of the herbicides glyphosate, 2,4-D and metsulfuron-methyl on soil microbial communities in the Pampas region, Argentina. Appl Soil Ecol. 40:1–12.Google Scholar
Zablotowicz, RM, Reddy, KN (2004) Impact of glyphosate on the Bradyrhizobium japonicum symbiosis with glyphosate-resistant transgenic soybean: a mini review. J Environ Qual. 33:825–831.Google Scholar
Zhao, Y, Tang, H, Ye, Y (2012) RAPSearch2: a fast and memory-efficient protein similarity search tool for next-generation sequencing data. Bioinformatics. 28:125–126.Google Scholar
Zhou, J, Davey, ME, Figueras, JB, Rivkina, E, Gilichinsky, D, Tiedje, JM (1997) Phylogenetic diversity of a bacterial community determined from Siberian tundra soil DNA. Microbiology. 143:3913–3919.Google Scholar