Skip to main content
SpringerLink
Log in

Glyphosate reduces shoot concentrations of mineral nutrients in glyphosate-resistant soybeans

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Although glyphosate-resistant (GR) technology is used in most countries producing soybeans (Glycine max L.), there are no particular fertilize recommendations for use of this technology, and not much has been reported on the influence of glyphosate on GR soybean nutrient status. An evaluation of different cultivar maturity groups on different soil types, revealed a significant decrease in macro and micronutrients in leaf tissues, and in photosynthetic parameters (chlorophyll, photosynthetic rate, transpiration and stomatal conductance) with glyphosate use (single or sequential application). Irrespective of glyphosate applications, concentrations of shoot macro- and micronutrients were found lower in the near-isogenic GR-cultivars compared to their respective non-GR parental lines Shoot and root dry biomass were reduced by glyphosate with all GR cultivars evaluated in both soils. The lower biomass in GR soybeans compared to their isogenic normal lines probably represents additive effects from the decreased photosynthetic parameters as well as lower availability of nutrients in tissues of the glyphosate treated plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

A:

net photosynthesis

DAS:

days after sowing

E:

transpiration rate

Gs:

stomatal conductance

GR:

glyphosate-resistant soybean

Non-GR:

conventional soybean near-isogenic parental line

ICP-OES:

(inductively coupled plasma-optical emission spectrometer)

References

  • Ames BN (1998) Micronutrients prevent cancer and delay aging. Toxicol Lett 102–103:5–18. doi:10.1016/S0378-4274(98)00269-0

    Article  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15. doi:10.1104/pp. 24.1.1

    Article  CAS  PubMed  Google Scholar 

  • Arregui MC, Lenardón A, Sanchez D, Maitre MI, Scotta R, Enrique S (2004) Monitoring glyphosate residues in transgenic glyphosate-resistant soybean. Pest Manage Sci 60:163–166. doi:10.1002/ps.775

    Article  CAS  Google Scholar 

  • Baker WH, Thompson TL (1992) Determination of total nitrogen in plant samples by Kjeldahl. In: Plank, C.O. (ed.) Plant Analysis Reference Procedures for the Southern Region of the United States. Southern Cooperative Series Bulletin 368. Athens: The Georgia Agricultural Experiment Station, University of Georgia, pp 13–16

  • Beale SI (1978) δ-Aminolevulinic acid in plants: its biosynthesis, regulation and role in plastid development. Annu Rev Plant Physiol 29:95–120. doi:10.1146/annurev.pp. 29.060178.000523

    Article  CAS  Google Scholar 

  • Bellaloui N, Reddy KN, Zablotowicz RM, Mengistu A (2006) Simulated glyphosate drift influences nitrate assimilation and nitrogen fixation in non-glyphosate-resistant soybean. J Agric Food Chem 54:3357–3364

    Article  CAS  PubMed  Google Scholar 

  • Boocock MR, Coggins JR (1983) Kinetics of 5-enolpyruvylshikimate-3-phosphate synthase inhibition by glyphosate. FEBS Lett 154:127–133. doi:10.1016/0014-5793(83)80888-6

    Article  CAS  PubMed  Google Scholar 

  • Bott S, Tesfamariam T, Candan H, Cakmak I, Romheld 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. doi:10.1007/s11104-008-9760-8

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Campbell WF, Evans JO, Reed SC (1976) Effect of glyphosate on chloroplast ultrastructure of quackgrass mesophyll cells. Weed Sci 24:22–25

    CAS  Google Scholar 

  • Coutinho CFB, Mazo LH (2005) Complexos metálicos com o herbicida glyphosate: Revisão. Química Nova 28:1038–1045. doi:10.1590/S0100-40422005000600019

    Article  CAS  Google Scholar 

  • De Maria N, Becerril LM, Garcia-Plazaola JI, Hernandez A, De Felipe MR, Fernandez-Pascual M (2006) New insights on glyphosate mode of action in nodulant metabolism: role of shikimate accumulation. J Agric Food Chem 54:2621–2628

    Article  CAS  PubMed  Google Scholar 

  • Duke SO, Rimando AM, Pace PF, Reddy KN, Smeda RJ (2003) Isoflavone, glyphosate, and aminomethylphosphonic acid levels in seeds of glyphosate-treated, glyphosate-resistant soybean. J Agric Food Chem 51:340–344. doi:10.1021/jf025908i

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1021/jf0625196

    Article  CAS  PubMed  Google Scholar 

  • Embrapa (1997) Manual de métodos de análises do solo, 2nd edn. Centro Nacional de Pesquisa de Solos Embrapa. Rio de Janeiro, RJ, p 212

    Google Scholar 

  • Fageria NK (1976) Critical P, K, Ca and Mg contents in the tops of rice and peanut plants. Plant Soil 45:421–431. doi:10.1007/BF00011704

    Article  CAS  Google Scholar 

  • Fageria NK (1987) Variação em diferentes estádios de crescimento do nível critico de fósforo em plantas da arroz. R Bras Cie Solo 11:77–80

    Google Scholar 

  • Fonseca DM, Alvares VH, Neves JCL, Gomide JA, Novais RF, Barros NF (1988) Níveis críticos de fósforo em amostras de solos para o estabelecimento de Andropogon gayanus, Brachiaria decumbens e Hyparrhenia rufa. R Bras Ci Solo 12:49–58

    Google Scholar 

  • Ferreira DF (1999) Sistema de análise de variância (Sisvar). versão 4.6. Lavras: Universidade Federal de Lavras

  • Franz JE, Mao MK, Sikorski JA (1997) Glyphosate: A Unique Global Herbicide; ACS Monograph 189. American Chemical Society, Washington, DC

    Google Scholar 

  • Franzen DW, O’Barr JH, Zollinger RK (2003) Interaction of a foliar application of iron HEDTA and three postemergence broadleaf herbicides with soybeans stressed from chlorosis. J Plant Nutr 26:2365–2374. doi:10.1081/PLN-120025465

    Article  CAS  Google Scholar 

  • Gazziero DLP, Adegas F, Voll E (2008) Glifosate e soja transgênica. Londrina: Embrapa Soja, Circular Técnica 60, p 4

  • Glass RL (1984) Metal complex formation by glyphosate. J Agric Food Chem 32:1249–1253. doi:10.1021/jf00126a010

    Article  CAS  Google Scholar 

  • Gordon WB (2007a) Manganese nutrition of glyphosate-resistant and conventional soybeans. Better Crops 91:12–13

    Google Scholar 

  • Gordon WB (2007b) Does glyphosate gene affect manganese uptake in soybeans? Fluid J. Early Spring 12–13

  • Hernandez A, Garcia-Plazaola JI, Bacerril JM (1999) Glyphosate effects on phenolic metabolism of nodulated soybean (Glycine max L. Merril). J Agric Food Chem 47:2920–2925. doi:10.1021/jf981052z

    Article  CAS  PubMed  Google Scholar 

  • Homann PH (1967) Studies on the manganese of the chloroplast. Plant Physiol 42:997–1007. doi:10.1104/pp. 42.7.997

    Article  CAS  PubMed  Google Scholar 

  • Huber DM (2006) Strategies to ameliorate glyphosate immobilization of manganese and its impact on the rhizosphere and disease. In: Lorenz N, Dick R (eds) Proceedings of the Glyphosate Potassium Symposium 2006. Ohio State University, AG Spectrum, DeWitt

    Google Scholar 

  • Jaworski EG (1972) Mode of action of N-phosphonomethyl-glycine: inhibition of aromatic amino acid biosynthesis. J Agri Food Chem 20:1195–1198

    Article  CAS  Google Scholar 

  • Johal GS, Huber DM (2009) Glyphosate effects on diseases of plants. Euro J Agron (in press)

  • Kabachnik MI, TYa M, Dyatolva NM, Rudomino MV (1974) Organophosphorus complexones. Russian Chem Rev 43:733–744. doi:10.1070/RC1974v043n09ABEH001851

    Article  Google Scholar 

  • Kitchen LM, Witt WW, Rieck CE (1981a) Inhibition of chlorophyll accumulation by glyphosate. Weed Sci 29:513–516

    CAS  Google Scholar 

  • Kitchen LM, Witt WW, Rieck CE (1981b) Inhibition of δ-aminolevulinic acid synthesis by glyphosate. Weed Sci 29:571–577

    CAS  Google Scholar 

  • King CA, Purcell LC, Vories ED (2001) Plant growth and nitrogenase activity of glyphosate-tolerant soybean in response to foliar glyphosate applications. Agron J 93:79–186

    Google Scholar 

  • Kremer RJ, Means NE, Kim S (2005) Glyphosate affects soybean root exudation and rhizosphere microorganisms. Int J Environ Anal Chem 85:1165–1174. doi:10.1080/03067310500273146

    Article  CAS  Google Scholar 

  • Lee TT (1981) Effects of glyphosate on synthesis and degradation of chlorophyll in soybean and tobacco cells. Weed Res 21:161–164. doi:10.1111/j.1365-3180.1981.tb00111.x

    Article  CAS  Google Scholar 

  • Madsen HEL, Christensen HH, Gottlieb-Petersen C (1978) Stability constants of copper (II), zinc, manganese (II), calcium, and magnesium complexes of N-(phosphonomethyl)glycine (glyphosate). Acta Chem Scand 32a:79–83. doi:10.3891/acta.chem.scand.32a-0079

    Article  Google Scholar 

  • Malavolta E, Vitti GC, Oliveira AS (1997) Princípios, métodos e técnicas de avaliação do estado nutricional. In: Malavolta E, Vitti GC, Oliveira AS (eds) Avaliação do estado nutricional da planta: princípios e aplicações, 2nd edn. POTAFÓS, Piracicaba, pp 115–230

    Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London, United Kingdom

  • McCay-Buis TS, Huber DM, Graham RD, Phillips JD, Miskin KE (1995) Manganese seed content and take-all of cereals. J Plant Nutr 18:1711–1721

    Article  CAS  Google Scholar 

  • Mills HA, Jones JB (1996) Plant Analysis Handbook II: a practical sampling, preparation, analysis, and interpretation guide. MicroMacro Publishing, Inc, Athens

    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

    Article  CAS  Google Scholar 

  • Muniz AS, Novais RF, Barros NF, Neves JCL (1985) Nível crítico de fósforo na parte aérea da soja como variável do fator capacidade de fósforo no solo. R Bras Ci Solo 9:237–243

    Google Scholar 

  • Nilsson G (1985) Interactions between glyphosate and metals essential for plant growth. In: Grossbard E, Atkinson D (eds) The herbicide glyphosate. Butterworth, London, pp 35–47

    Google Scholar 

  • Novais RF, Kamprath EJ (1979) Parâmetros de isotermas de adsorção de fósforo como critério de adubação fosfatada. R Bras Ci Solo 3:37–41

    Google Scholar 

  • Oliveira FA, Sfredo GJ, Castro C, Klepker D (2007) Fertilidade do solo e nutrição da soja. Londrina: Embrapa Soja, Circular Técnica 50, p 8

  • Ozturk L, Yazici A, Eker S, Gokmen O, Roemheld V, Cakmak I (2008) Glyphosate inhibition of ferric reductase activity in iron deficient sunflower roots. New Phytol 17:899–906. doi:10.1111/j.1469-8137.2007.02340.x

    Article  CAS  Google Scholar 

  • Pline WA, Wu J, Hatzios KK (1999) Effects of temperature and chemical additives on the response of transgenic herbicide-resistant soybeans to glufosinate and glyphosate applications. Pestic Biochem Physiol 65:119–131. doi:10.1006/pest.1999.2437

    Article  CAS  Google Scholar 

  • Pihakaski S, Pihakaski K (1980) Effects of glyphosate on ultrastructure and photosynthesis of Pellia epiphylla. Annals Bot 46:133–141. doi:10.1016/j.foreco.2005.11.003

    CAS  Google Scholar 

  • Pinkard EA, Patel V, Mohammed C (2006) Chlorophyll and nitrogen determination for plantation-grown Eucaliptus nitens and E. glogulus using a non-destructive meter. Forest Ecol Manag 223:211–217

    Article  Google Scholar 

  • Reddy KN, Hoagland RE, Zablotowicz RM (2001) Effect of glyphosate on growth, chlorophyll, and nodulation in glyphosate-resistant and susceptible soybean (Glycine max) varieties. J New Seeds 2:37–52. doi:10.1300/J153v02n03_03

    Article  Google Scholar 

  • 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. doi:10.1021/jf049605v

    Article  CAS  PubMed  Google Scholar 

  • Richardson AD, Duigan SP, Berlyn GP (2002) An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytol 153:185–194. doi:10.1046/j.0028-646X.2001.00289.x

    Article  CAS  Google Scholar 

  • Santos JB, Santos EA, Fialho CMT, Silva AA, Freitas MAM (2007) Época de dessecação anterior à semeadura sobre o desenvolvimento da soja resistente ao glyphosate. Planta Daninha 25:869–875

    Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality. Biometrika 52:591–611

    Google Scholar 

  • Seybold CA, Herrick JE, Brejda JJ (1999) Soil resilience: A fundamental component of soil quality. Soil Sci 16:224–234. doi:10.1097/00010694-199904000-00002

    Article  Google Scholar 

  • Scherer EE (1998) Níveis críticos de potássio para a soja em Latossolo húmico de Santa Catarina. R Bras Ci Solo 22:57–62

    CAS  Google Scholar 

  • Shibles RM, Weber CR (1965) Leaf area, solar radiation interception, and dry matter production by various soybean planting patterns. Crop Sci 6:575–577

    Article  Google Scholar 

  • Singh BK, Siehl DL, Connelly JA (1991) Shikimate pathway: why does it mean so much to so many? Oxf Surv Plant Mol Cell Biol 7:143–185

    CAS  Google Scholar 

  • Singh B, Singh Y, Ladha JK, Bronson KF, Balasubramanian V, Singh J, Khind CS (2002) Chlorophyll meter-and leaf color chart-based nitrogen management for rice and wheat in Northwestern India. Agron J 94:821–89

    Article  Google Scholar 

  • Sprankle P, Meggitt WF, Penner D (1975) Absorption, action, and translocation of glyphosate. Weed Sci 23:235–240

    CAS  Google Scholar 

  • Taiz L, Zeiger E (1998) Mineral Nutrition. In: Plant Physiology, Sinauer Associates: Sunderland, pp 111–144

  • Thomson WW, Weier TE (1962) The fine structure of chloroplasts from mineral-deficient leaves of Phaseolus vulgaris. Am J Bot 49:1047–1056. doi:10.2307/2439150

    Article  CAS  Google Scholar 

  • Zablotowicz RM, Reddy KN (2004) Impact of glyphosate on the Bradyrhizobium japonicum symbiosis with glyphosate-resistant transgenic soybean. J. Environ. Qual 33:825–831

    CAS  PubMed  Google Scholar 

  • Zablotowicz RM, Reddy KN (2007) Nitrogenase activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean. Crop Protec 26:370–376. doi:10.1016/j.cropro.2005.05.013

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the National Council for Scientific and Technology Development (CNPq), for the graduate scholarship for the senior author and financial support for this research.

Author information

Authors and Affiliations

  1. Center for Advanced Studies in Weed Science (NAPD), State University of Maringá (UEM), Colombo Av., 5790, 87020-900, Maringá, Paraná, Brazil

    Luiz Henrique Saes Zobiole, Rubem Silvério de Oliveira Jr & Jamil Constantin

  2. Botany & Plant Pathology, Purdue University, 915 W. State Street, West Lafayette, IN, USA

    Don Morgan Huber

  3. Embrapa Soybean, Postcode 231, 86001-970, Londrina, Paraná, Brazil

    César de Castro, Fábio Alvares de Oliveira & Adilson de Oliveira Jr.

Authors
  1. Luiz Henrique Saes Zobiole
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rubem Silvério de Oliveira Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Don Morgan Huber
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jamil Constantin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. César de Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fábio Alvares de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Adilson de Oliveira Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luiz Henrique Saes Zobiole.

Additional information

Responsible Editor: Ismail Cakmak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Henrique Saes Zobiole, L., de Oliveira, R.S., Morgan Huber, D. et al. Glyphosate reduces shoot concentrations of mineral nutrients in glyphosate-resistant soybeans. Plant Soil 328, 57–69 (2010). https://doi.org/10.1007/s11104-009-0081-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-009-0081-3

Keywords

Search

Navigation