Abstract
It has been repeatedly demonstrated that phosphate (P) and the herbicide glyphosate compete for adsorption sites in soils. Surprisingly, the potential consequences of these interactions for plants e.g. re-solubilisation of phytotoxic glyphosate residues in soils by application of P fertilisers or by root-induced mechanisms for P mobilization have not been investigated so far. In model experiments under greenhouse conditions, the potential for glyphosate re-mobilisation by P-fertiliser application was evaluated by bio-indication with soybean (Glycine max L.) cultivated on five contrasting soils with or without glyphosate application at 10–35 days before sowing. Different levels of P-fertilisation (0, 20, 40, 80, 240 mg P kg−1 soil) were supplied at the date of sowing. Visual symptoms of glyphosate toxicity, plant biomass, intracellular shikimate accumulation as physiological indicator for glyphosate toxicity and the plant nutritional status were determined. On glyphosate-treated soils, P application induced significant plant damage. Expression of damage symptoms declined in the order Arenosol > Acrisol ≈ Ferralsol > Luvisol subsoil > Regosol. On the Arenosol, Ferralsol and Luvisol subsoil plant damage was associated with increased shikimate accumulation in the root tissue. On the Acrisol decline of germination and plant damage in absence of shikimate accumulation indicate toxicity of AMPA (aminomethylphosphonic acid) as the main metabolite of glyphosate in soils. On the Regosol, a growth-stimulating effect of glyphosate soil application (hormesis) was detected. The results suggest that re-mobilisation of glyphosate may represent an additional transfer pathway for glyphosate to non-target plants which is strongly influenced by soil characteristics such as P fixation potential, content of plant-available iron, pH, cation exchange capacity, sand content and soil organic matter.
Similar content being viewed by others
Abbreviations
- a.e.:
-
acid equivalent
- AMPA:
-
aminomethylphosphonic acid
- cv.:
-
cultivar
- DAS:
-
days after sowing
- n.d.:
-
not determined
- N.S.:
-
not significant
- SOM:
-
soil organic matter
- WHC:
-
water holding capacity
References
Albers CN, Banta GT, Hansen PE, Jacobsen OS (2009) The influence of organic matter on sorption and fate of glyphosate in soil—comparing different soils and humic substances. Environ Pollut 157:2865–2870
Alletto L, Coquet Y, Benoit P, Heddadj D, Barriuso E (2010) Tillage management effects on pesticide fate in soils. A review. Agron Sustain Dev 30:367–400
Allister C, Kogan M, Pino I (2005) Differential phytotoxicity of glyphosate in maize seedlings following applications to roots or shoot. Weed Research 45:27–32
Barja BC, Dos Santos AM (2005) Aminomethylphosphonic acid and glyphosate adsorption onto goethite: a comparative study. Environ Sci Tech 39:585–592
Barry GF (2009) Plants and plant cells exhibiting resistance to AMPA, and methods for making the same: United States Patent 7554012. Freepatentsonline, http://www.freepatentsonline.com/7554012.pdf Accessed 26 August 2010
Baylis AD (2000) Why glyphosate is a global herbicide: strengths, weaknesses and prospects. Pest Manage Sci 56:299–308
Borggaard OK, Gimsing AL (2008) Fate of glyphosate in soil and the possibility of leaching to ground and surface waters: a review. Pest Manage Sci 64:441–456
Bott S, Tesfamariam T, Candan H, Cakmak I, Römheld V, Neumann G (2008) Glyphosate-induced impairment of plant growth and micronutrient status in glyphosate-resistant soybean (Glycine max L.). Plant Soil 312:185–194
Bott S, Lebender U, Kania A, Yoon DJ, Tesfamariam T, Ceylan Y, Römheld V, Neumann G (2010) Rhizosphere transfer of glyphosate after pre-crop herbicide application. New Phytol (submitted)
Cakmak I, Yazici A, Tutus Y, Ozturk L (2009) Glyphosate reduced seed and leaf concentrations of calcium, manganese, magnesium, and iron in non-glyphosate resistant soybean. Europ J Agron 31:114–119
Candela L, Caballero J, Ronen D (2010) Glyphosate transport through weathered granite soils under irrigated and non-irrigated conditions—Barcelona, Spain. Sci Total Environ 408:2509–2516
Cornish PS (1992) Glyphosate residues in a sandy soil affect tomato transplants. Aust J Exp Agric 32:395–399
Dion HM, Harsh JB, Hill HH Jr (2001) Competitive sorption between glyphosate and inorganic phosphate on clay minerals and low organic matter soils. J Radioanal Nucl Chem 249:385–390
Doublet J, Mamy L, Barriuso E (2009) Delayed degradation in soil of foliar herbicides glyphosate and sulcotrione previously absorbed by plants: consequences on herbicide fate and risk assessment. Chemosphere 77:582–589
Drew MC (1975) Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol 75:479–490
Duke S, Wauchope R, Hoagland R, Wills G (1983) Influence of glyphosate on uptake and translocation of calcium ion in soybean seedlings. Weed Res 23:133–139
Eker S, Ozturk L, Yazici A, Erenoglu B, Romheld V, Cakmak I (2006) Foliar-applied glyphosate substantially reduced uptake and transport of iron and manganese in sunflower (Helianthus annuus L.) plants. J Agric Food Chem 54:10019–10025
Franz JE, Mao MK, Sikorski JA (1997) Glyphosate: A Unique Global Herbicide. American Chemical Society, Chap. 4, pp. 65–97
Fernandez MR, Zentner RP, Basnyat P, Gehl D, Selles F, Huber D (2009) Glyphosate associations with cereal diseases caused by Fusarium spp. in the Canadian Prairies. Europ J Agronomy 31:133–143
Geiger DR, Kapitan SW, Tucci MA (1986) Glyphosate inhibits photosynthesis and allocation of carbon to starch in sugar beet leaves. Plant Physiol 82:468–472
Gericke VS, Kurmies B (1952) Die kolorimetrische Phosphorsäurebestimmung mit Ammonium-Vanadat-Molybdat und ihre Anwendung in der Pflanzenanalyse. Z Pflanzenernähr Bodenkd 59:235–247
Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup® herbicide. Rev Environ Contam Toxicol 167:35–120
Gimsing AL, Borggaard OK (2002a) Competitive adsorption and desorption of glyphosate and phosphate on clay silicates and oxides. Clay Miner 37:509–515
Gimsing AL, Borggaard OK (2002b) Effect of phosphate on the adsorption of glyphosate on soils, clay minerals and oxides. Int J Environ Anal Chem 82:545–552
Gimsing AL, Borggaard OK, Bang M (2004) Influence of soil composition on adsorption of glyphosate and phosphate by contrasting Danish surface soils. Eur J Soil Sci 55:183–191
Gordon B (2007) Manganese nutrition of glyphosate-resistant and conventional soybeans. Better Crops 91(4):12–13
Hance RJ (1976) Adsorption of glyphosate by soils. Pestic Sci 7:363–366
Henry WB, Shaner DL, West MS (2007) Shikimate accumulation in sunflower, wheat, and proso millet after glyphosate application. Weed Sci 55:1–5
Johal GS, Huber DM (2009) Glyphosate effects on diseases of plants. Europ J Agronomy 31:144–152
Jursík M, Soukup J, Holec J, Venclová V (2010) Herbicide mode of actions and symptoms of plant injury by herbicides: inhibitors of amino acid biosynthesis | [Inhibitory biosyntézy aminokyselin]. Listy Cukrovarnicke a Reparske 126:250–253
Kremer RJ, Means NE (2009) Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms. Eur J Agron 31:153–161
Laitinen P, Siimes K, Rämö S, Jauhiainen L, Eronen L, Oinonen S, Hartikainen H (2008) Effects of soil phosporus status on environmental risk assessment of glyphosate and glufosinate-ammonium. J Environ Qual 37:830–838
Neumann G, Römheld V (2002) Root induced changes in the availability of nutrients in the rhizosphere. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots. The hidden half, 3rd edn. Dekker, New York, pp 617–649
Neumann G, Römheld V (2007) The release of root exudates as affected by the plant’s physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: Biochemistry and organic substances at the soil-plant interface, 1st edn. CRC, Boca Raton, pp 23–72
Neumann G, Kohls S, Landsberg E, Stock-Oliveira Souza K, Yamada T, Römheld V (2006) Relevance of glyphosate transfer to non-target plants via the rhizosphere. J Plant Dis Protect 20:963–969
Neumann G, Bott S, Tesfamariam T, Römheld V (2008) Fehler mit Totalherbiziden vermeiden. DLZ 9:44–48
Ozturk L, Yazici A, Eker S, Gokmen O, Römheld V, Cakmak I (2008) Glyphosate inhibition of ferric reductase activity in iron deficient sunflower roots. New Phytol 177:899–906
Piccolo A, Celano G, Pietramellara G (1992) Adsorption of the herbicide glyphosate on a metal-humic acid complex. Sci Total Environ 123:77–82
Piccolo A, Celano G, Arienzo M, Mirabella A (1994) Adsorption and desorption of glyphosate in some European soils. J Environ Sci Health, Part B, Pestic Food Contam Agric Wastes 29:1105–1115
Reddy KN, Rimando AM, Duke SO (2004) Aminomethylphosphonic acid, a metabolite of glyphosate, causes injury in glyphosate-treated, glyphosate-resistant soybean. J Agric Food Chem 52:5139–5143
Schnürer J, Clarholm M, Rosswall T (1985) Microbial biomass and activity in an agricultural soil with different organic matter contents. Soil Biol Biochem 17:611–618
Sergiev IG, Alexieva VS, Ivanov SV, Moskova II, Karanov EN (2006) The phenylurea cytokinin 4PU-30 protects maize plants against glyphosate action. Pestic Biochem Physiol 85:139–146
Sheals J, Sjöberg S, Persson P (2002) Adsorption of glyphosate on goethite: molecular characterization of surface complexes. Environ Sci Technol 36:3090–3095
Singh BK, Shaner DL (1998) Rapid determination of glyphosate injury to plants and identification of glyphosate-resistant plants. Weed Technol 12:527–530
Smiley RW, Ogg AG, Cook RJ (1992) Influence of glyphosate on Rhizoctonia root rot, growth, and yield of barley. Plant Dis 76:937–942
Sprankle P, Meggitt WF, Penner D (1975a) Rapid inactivation of glyphosate in the soil. Weed Sci 23:224–228
Sprankle P, Meggitt WF, Penner D (1975b) Adsorption, mobility, and microbial degradation of glyphosate in the soil. Weed Sci 23:229–234
Sprankle P, Meggitt WF, Penner D (1975c) Adsorption, action and translocation of glyphosate. Weed Sci 23:235–240
Subramaniam V, Hoggard PE (1988) Metal complexes of glyphosate. J Agric Food Chem 36:1326–1329
Tesfamariam T (2003) Effects of P-deficiency induced Root exudation on Mo-acquisition in leguminous plants. diploma thesis, University of Hohenheim
Tesfamariam T, Bott S, Cakmak I, Römheld V, Neumann G (2009) Glyphosate in the rhizosphere-role of waiting times and different glyphosate binding forms in soils for phytotoxicity to non-target plants. Europ J Agronomy 31:126–132
VDLUFA (2004) Bestimmung von Magnesium, Natrium und den Spurennährstoffen Kupfer, Mangan, Zink, und Bor im Calciumchlorid/DTPA-Auszug. VDLUFA-Methodenbuch I. VDLUFA DLUFA-Verlag, Darmstadt, p A 6.4.1
Velini ED, Alves E, Godoy MC, Meschede DK, Souza RT, Duke SO (2008) Glyphosate applied at low doses can stimulate plant growth. Pest Manage Sci 64:489–496
Vereecken H (2005) Mobility and leaching of glyphosate: a review. Pest Manag Sci 61:1139–1151
Zobiole LHS, de Oliveira Jr RS, Huber DM, Constantin J, de Castro C, de Oliveira FA, de Oliveira Jr A (2010a) Glyphosate reduces shoot concentrations of mineral nutrients in glyphosate-resistant soybeans. Plant Soil 328:57–69
Zobiole LHS, Oliveira RS Jr, Kremer RJ, Constantin J, Bonato CM, Muniz AS (2010b) Water use efficiency and photosynthesis of glyphosate-resistant soybean as affected by glyphosate. Pest Biochem Physiol 97:182–193
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Ismail Cakmak.
Rights and permissions
About this article
Cite this article
Bott, S., Tesfamariam, T., Kania, A. et al. Phytotoxicity of glyphosate soil residues re-mobilised by phosphate fertilisation. Plant Soil 342, 249–263 (2011). https://doi.org/10.1007/s11104-010-0689-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-010-0689-3