Abstract
Background and aims
Repeated applications of glyphosate in short timeframes can lead to periodic accumulation of soilborne glyphosate residues. This study aimed to determine whether typical glyphosate residues observed in fields affect growth, plant metabolite composition and fungal root endophyte colonisation of wheat (Triticum aestivum).
Methods
Glyphosate was applied to a sandy soil at 0, 0.33, 1, 3, 9 and 27 times a recommended label rate (LR) to establish soil glyphosate concentrations of 0, 0.1, 0.4, 1, 4.7 and 14.8 mg kg−1 in topsoil (0–100 mm) after a 28 d plant-free incubation. Wheat plants were then grown to establish thresholds of soilborne glyphosate on seedling emergence, major alterations to plant metabolic responses and fungal root endophyte colonisation.
Results
Seedling emergence was unaffected by soil residual glyphosate treatments. Shoot biomass was significantly higher at 1 mg kg−1 compared to the control treatments (P < 0.05) and root biomass followed a similar trend. Leaf metabolite profiles of plants growing in soil containing 4.7–14.8 mg kg−1 glyphosate could be discriminated from the 0–0.4 mg kg−1 treatments due to significant (P < 0.05) effects on the relative concentrations of metabolites. Fungal root endophyte colonisation was significantly reduced to 10% at 14.8 mg kg−1 (P < 0.05) whereas shoot and root biomass remained unaffected.
Conclusions
Our study highlights differences in glyphosate sensitivity thresholds between plants and fungal symbionts. Sub-lethal concentrations of residual soilborne glyphosate can alter wheat metabolism and impair fungal root endophyte colonisation. Effect thresholds for glyphosate may be lower for fungal symbionts than for host plants. However, the soil glyphosate residue levels required to reach such thresholds are high and would only be approached in commercial fields with a history of repeated glyphosate application.
Similar content being viewed by others
References
Andréa MMD, Peres TB, Luchini LC et al (2003) Influence of repeated applications of glyphosate on its persistence and soil bioactivity. Pesq Agropec Bras 38:1329–1335
Barto EK, Hilker M, Müller F, Mohney BK, Weidenhamer JD, Rillig MC (2011) The fungal fast lane: common mycorrhizal networks extend bioactive zones of allelochemicals in soils. PLoS One 6:e27195
Blackshaw RE, Harker KN (2016) Wheat, field pea, and canola response to glyphosate and AMPA soil residues. Weed Technol 30:985–991
Boocock MR, Coggins JR (1983) Kinetics of 5-enolpyruvylshikimate-3-phosphate synthase inhibition by glyphosate. FEBS Lett 154:127–133
Bott S, Tesfamariam T, Kania A, et al (2011) Phytotoxicity of glyphosate soil residues re-mobilised by phosphate fertilisation. Plant Soil 342:249–263. https://doi.org/10.1007/s11104-010-0689-3
Brader G, Compant S, Vesico K et al (2017) Ecology and genomic insights on plant-pathogenic and nonpathogenic endophytes. Annu Rev Phytopathol 55:1–23
Brito IPFS, Tropaldi L, Carbonari CA, Velini ED (2018) Hormetic effects of glyphosate on plants. Pest Manag Sci 74:1064–1070. https://doi.org/10.1002/ps.4523
Bünemann EK, Schwenke GD, Van Zwieten L (2006) Impact of agricultural inputs on soil organisms – a review. Aust J Soil Res 44:379–406
Comby M, Lacoste S, Baillieul F, Profizi C, Dupont J (2016) Spatial and temporal variation of cultivable communities of co-occurring endophytes and pathogens in wheat. Front Microbiol 7
Compant S, Saikkonen K, Mitter B, Campisano A, Mercado-Blanco J (2016) Editorial special issue: soil, plants and endophytes. Plant Soil 405:1–11
Deshmukh S, Hückelhoven R, Schäfer P et al (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci U S A 103:18450–18457
Druille M, García-Parisi PA, Golluscio RA, Cavagnaro FP, Omacini M (2016) Repeated annual glyphosate applications may impair beneficial soil microorganisms in temperate grassland. Agric Ecosyst Environ 230:184–190
Franken P (2012) The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl Microbiol Biotechnol 96:1455–1464
Gallaud I (1905) Études sur les mycorhizes endotrophes. Rev Générale Bot 17:5–500
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Gomes MP, Smedbol E, Chalifour A, Hénault-Ethier L, Labrecque M, Lepage L, Lucotte M, Juneau P (2014) Alteration of plant physiology by glyphosate and its by-product aminomethylphosphonic acid: an overview. J Exp Bot 65:4691–4703
Gurulingappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55:34–41
Hiller K, Hangebrauk J, Jäger C et al (2009) Metabolite detector: comprehensive analysis tool for targeted and nontargeted GC/MS based metabolome analysis. Anal Chem 81:3429–3439
Hubbard M, Germida J, Vujanovic V (2014) Fungal endophytes enhance wheat heat and drought tolerance in terms of grain yield and second-generation seed viability. J Appl Microbiol 116:109–122
Isbell RF, McDonald WS, Ashton L (1997) Concepts & rationale of the Australian soil classification. CSIRO Publishing, Melbourne
Jacobsen CS, Hjelmsø MH (2014) Agricultural soils, pesticides and microbial diversity. Curr Opin Biotechnol 27:15–20
Johal GS, Rahe JE (1984) Effect of soilborne plant-pathogenic fungi on the herbicidal action of glyphosate on bean seedlings. Phytopathology 74:950–955
Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmuller E, Dormann P, Weckwerth W, Gibon Y, Stitt M, Willmitzer L, Fernie AR, Steinhauser D (2005) GMD@CSB.DB: the Golm metabolome database. Bioinformatics 21:1635–1638
Krzysko-Lupicka T, Orlik A (1997) 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 34:2601–2605
Krzysko-Lupicka T, Sudol T (2008) Interactions between glyphosate and autochthonous soil fungi surviving in aqueous solution of glyphosate. Chemosphere 71:1386–1391
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
Larran S, Perelló A, Simón MR, Moreno V (2007) The endophytic fungi from wheat (Triticum aestivum L.). World J Microbiol Biotechnol 23:565–572
Lenth R (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33
Lescano CI, Martini C, González CA, Desimone M (2016) Allantoin accumulation mediated by allantoinase downregulation and transport by Ureide permease 5 confers salt stress tolerance to Arabidopsis plants. Plant Mol Biol 91:581–595
Lévesque CA, Rahe JE (1992) Herbicide interactions with fungal root pathogens, with special reference to glyphosate. Annu Rev Phytopathol 30:579–602
Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1:387–396
Mayerhofer MS, Kernaghan G, Harper KA (2013) The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23:119–128
Mudhoo A, Garg VK (2011) Sorption, transport and transformation of atrazine in soils, minerals and composts: a review. Pedosphere 21:11–25
Ownley BH, Gwinn KD, Vega FE (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. BioControl 55:113–128
Peruzzo PJ, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environ Pollut 156:61–66
Peters G-JY (2017) userfriendlyscience: Quantitative analysis made accessible. R Packag version 06-1. https://doi.org/10.17605/OSF.IO/TXEQU
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161
Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315
Primost JE, Marino DJG, Aparicio VC, Costa JL, Carriquiriborde P (2017) Glyphosate and AMPA, “pseudo-persistent” pollutants under real-world agricultural management practices in the Mesopotamic pampas agroecosystem, Argentina. Environ Pollut 229:771–779
R Core Team (2016) R: A language and environment for statistical computing
Rai M, Rathod D, Agarkar G et al (2014) Fungal growth promotor endophytes: a pragmatic approach towards sustainable food and agriculture. Symbiosis 62:63–79
Rayment GE, Lyons DJ (2011) Soil chemical methods. CSIRO Publishing, Australasia
Rodriguez RJ, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114
Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330
Rohart F, Gautier B, Singh A, Lê Cao K-A (2017) mixOmics: an R package for ‘omics feature selection and multiple data integration. PLoS Comput Biol 13:e1005752
Rose TJ, Rengel Z, Ma Q, Bowden JW (2007) Differential accumulation patterns of phosphorus and potassium by canola cultivars compared to wheat. J Plant Nutr Soil Sci 170:404–411
Rose MT, Rose TJ, Pariasca-Tanaka J, Yoshihashi T, Neuweger H, Goesmann A, Frei M, Wissuwa M (2012) Root metabolic response of rice (Oryza sativa L.) genotypes with contrasting tolerance to zinc deficiency and bicarbonate excess. Planta 236:959–973
Rose MT, Cavagnaro TR, Scanlan C et al (2016) Impact of herbicides on soil biology and function. In: Advances in agronomy. Elsevier Inc, pp 133–220
Rose TJ, Van Zwieten L, Claassens A et al (2017) Phytotoxicity of soilborne glyphosate residues is influenced by the method of phosphorus fertiliser application. Plant Soil 422:455–465
Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99
Schulz B, Boyle C, Draeger S, Römmert AK, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004
Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523–531
Serra AA, Nuttens A, Larvor V, Renault D, Couée I, Sulmon C, Gouesbet G (2013) Low environmentally relevant levels of bioactive xenobiotics and associated degradation products cause cryptic perturbations of metabolism and molecular stress responses in Arabidopsis thaliana. J Exp Bot 64:2753–2766
Shushkova T, Ermakova I, Leontievsky A (2010) Glyphosate bioavailability in soil. Biodegradation 21:403–410
Silva V, Montanarella L, Jones A, Fernández-Ugalde O, Mol HGJ, Ritsema CJ, Geissen V (2018) Distribution of glyphosate and aminomethylphosphonic acid (AMPA) in agricultural topsoils of the European Union. Sci Total Environ 621:1352–1359
Smith SE, Read D (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press
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
Sylvia DM, Chellemi DO (2001) Interactions among root-inhabiting fungi and their implications for biological control of root pathogens. In: Advances in agronomy, pp 1–33
Taghinasab M, Imani J, Steffens D, Glaeser SP, Kogel KH (2018) The root endophytes Trametes versicolor and Piriformospora indica increase grain yield and P content in wheat. Plant Soil 426:339–348
Takagi H, Ishiga Y, Watanabe S, Konishi T, Egusa M, Akiyoshi N, Matsuura T, Mori IC, Hirayama T, Kaminaka H, Shimada H, Sakamoto A (2016) Allantoin, a stress-related purine metabolite, can activate jasmonate signaling in a MYC2-regulated and abscisic acid-dependent manner. J Exp Bot 67:2519–2532
Valluru R, Van den Ende W (2011) Myo-inositol and beyond - emerging networks under stress. Plant Sci 181:387–400
Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004) Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol Fertil Soils 40:36–43
Watanabe S, Matsumoto M, Hakomori Y et al (2014) The purine metabolite allantoin enhances abiotic stress tolerance through synergistic activation of abscisic acid metabolism. Plant Cell Environ 37:1022–1036
Weng Z, Rose MT, Tavakkoli E, van Zwieten L, Styles G, Bennett W, Lombi E (2019) Assessing plant-available glyphosate in contrasting soils by diffusive gradient in thin-films technique (DGT). Sci Total Environ 646:735–744
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Anna Maria Pirttila.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Supplementary Table 1
Normalised peak areas of detected metabolites in wheat tissues under grown under different doses of soilborne glyphosate residues (XLSX 51 kb)
Supplementary Table 2
ANOVA results for influential metabolites contributing high loadings to PLS-DA components 1 and 2 (XLSX 13 kb)
Rights and permissions
About this article
Cite this article
Claassens, A., Rose, M.T., Van Zwieten, L. et al. Soilborne glyphosate residue thresholds for wheat seedling metabolite profiles and fungal root endophyte colonisation are lower than for biomass production in a sandy soil. Plant Soil 438, 393–404 (2019). https://doi.org/10.1007/s11104-019-04023-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-019-04023-y