Plant and Soil

, Volume 336, Issue 1–2, pp 251–265 | Cite as

Glyphosate affects photosynthesis in first and second generation of glyphosate-resistant soybeans

  • Luiz Henrique Saes ZobioleEmail author
  • Robert John Kremer
  • Rubem Silvério de OliveiraJr
  • Jamil Constantin
Regular Article


The crop area planted to conventional soybeans has decreased annually while that planted to glyphosate-resistant (RR) soybean has drastically increased mainly due to the wide adoption of glyphosate in current weed management systems. With the extensive use of glyphosate, many farmers have noted visual plant injury in RR soybean varieties after glyphosate application. A new generation designated as “second generation—RR2” has been recently developed and these RR2 cultivars already are commercially available for farmers and promoted as higher yielding relative to the previous RR cultivars. However, little information is currently available about the performance of RR2 soybean beyond commercial and farmer testimonial data. Thus, an evaluation of different glyphosate rates applied in different growth stages of the first and second generation of RR soybeans, revealed a significant decrease in photosynthesis. In general, increased glyphosate rate and late applications (V6) pronounced decrease photosynthetic parameters and consequently decreased in leaf area and shoot biomass production. In contrast, low rate and early applications were less damage for the RR soybean plants, suggesting that with early applications (V2), plants probably have more time to recover from glyphosate or its metabolites effects regarding late applications.


Glyphosate resistant soybean (Glycine max L.) Glyphosate Photosynthesis Biomass 



Days after sowing


Photosynthetic rate


Transpiration rate


Stomatal conductance


Sub-stomatal CO2


Photosynthetic electron transport rates


Minimal fluorescence of a light adapted leaf


Maximal fluorescence of a light adapted leaf


Steady state fluorescence of a light adapted leaf


Intrinsic efficiency of photosystem 2


Photosystem 2


Quantum efficiencies of photosynthetic electron transport through photosystem 2


Quantum yield based on CO2 assimilation


Non-photochemical quenching of chlorophyll fluorescence


Proportion of open reaction centers


Glyphosate-resistant soybean—first generation


Glyphosate-resistant soybean—second generation


Conventional soybean near-isogenic parental line



We thank the National Council for Scientific and Technology Development (CNPq-Brasilia, DF, Brazil) for the scholarship and financial support for this research. The authors also thank Dr. Bruce Hibbard, USDA, Agricultural Research Service for use of greenhouse facilities and Carey Page, University of Missouri for assistance with herbicide applications. Trade names are used for clarity and do not represent endorsement by USDA-ARS, the State University of Maringá, or the University of Missouri.


  1. Arregui MC, Lenardón A, Sanchez D, Maitre MI, Scotta R, Enrique S (2004) Monitoring glyphosate residues in transgenic glyphosate-resistant soybean. Pest Manage Sci 60:163–166CrossRefGoogle Scholar
  2. Bellaloui N, Reddy KN, Zablotowicz RM, Abbas HK, Abel CA (2009) Effects of glyphosate on seed iron and root ferric (III) reductase in soybean cultivars. J Agric Food Chem. doi: 10.1021/jf902175y Google Scholar
  3. 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 312:185–194CrossRefGoogle Scholar
  4. 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 37:39–47CrossRefGoogle Scholar
  5. 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. Eur J Agron 31:114–119CrossRefGoogle Scholar
  6. Campbell WF, Evans JO, Reed SC (1976) Effect of glyphosate on chloroplast ultrastructure of quackgrass mesophyll cells. Weed Sci 24:22–25Google Scholar
  7. Centritto M, Magnani F, Lee HSJ, Jarvis PG (1999) Interactive effects of elevated [CO2] and drougth on cherry (Prunus avium) seedlings: II. Photosynthetic capacity and water relations. New Phytol 141:141–153CrossRefGoogle Scholar
  8. Cheng L, Fuchigami LH, Breen PJ (2001) The relationship between photosystem II efficiency and quantum yield for CO2 assimilation is not affected by nitrogen content in apple leaves. J Exp Bot 52:1865–1872CrossRefPubMedGoogle Scholar
  9. Cole DJ (1985) Mode of action of glyphosate—a literature analysis. In: Grossbard E, Atkinson D (eds) The herbicide glyphosate. Butterworths, London, pp 48–74Google Scholar
  10. Coutinho CFB, Mazo LH (2005) Complexos metálicos com o herbicida glyphosate: Revisão. Química Nova 28:1038–1045CrossRefGoogle Scholar
  11. Da Matta FM, Loos RA, Rodrigues R, Barros RS (2001) Actual and potential photosynthetic rates of tropical crop species. R Bras Fisiol Veg 13:24–32Google Scholar
  12. Demming-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Ann Rev Plant Physiol Plant Mol Biol 43:599–626CrossRefGoogle Scholar
  13. Duke SO (2005) Taking stock of herbicide-resistant crops ten years after introduction. Pest Manage Sci 61:211–218CrossRefGoogle Scholar
  14. 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 51:340–344CrossRefPubMedGoogle Scholar
  15. Franz JE, Mao MK, Sikorski JA (1997) Glyphosate: a unique global herbicide; ACS Monograph 189. American Chemical Society, Washington, DCGoogle Scholar
  16. Fritschi FB, Ray JD (2007) Soybean leaf nitrogen, chlorophyll content, and chlorophyll a/b ratio. Photosynthetica 45:92–98CrossRefGoogle Scholar
  17. Gazziero DLP, Adegas F, Voll E (2008) Glifosate e soja transgênica. Londrina: Embrapa Soja, Circular Técnica 60, p 4Google Scholar
  18. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92Google Scholar
  19. Gianessi LP, Carpenter JE (2000) Agricultural biotechnology: benefits of transgenic soybeans. National Center for Food and Agricultural PolicyGoogle Scholar
  20. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Ann Rev Plant Physiol Plant Mol Biol 4:655–684CrossRefGoogle Scholar
  21. 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, DeWittGoogle Scholar
  22. Jaworski EG (1972) Mode of action of N-phosphonomethyl-glycine: inhibition of aromatic amino acid biosynthesis. J Agric Food Chem 20:1195–1198CrossRefGoogle Scholar
  23. Jiang C-D, Gao H-Y, Zou Q, Jiang G-M, Li L-H (2006) Leaf orientation, photorespiration and xanthophyll cycle protect young soybean against high irradiance in field. Environ Exp Bot 55:87–96CrossRefGoogle Scholar
  24. Johal GS, Huber DM (2009) Glyphosate effects on diseases of plants. Eur J Agron 31:144–152CrossRefGoogle Scholar
  25. Kabachnik MI, TYa M, Dyatolva NM, Rudomino MV (1974) Organophosphorus complexones. Russ Chem Rev 43:733–744CrossRefGoogle Scholar
  26. King AC, Purcell LC, Vories ED (2001) Plant growth and nitrogenase activity of glyphosate-tolerant soybean in response to glyphosate applications. Agron J 93:179–186CrossRefGoogle Scholar
  27. Kitchen LM, Witt WW, Rieck CE (1981) Inhibition of chlorophyll accumulation by glyphosate. Weed Sci 29:513–516Google Scholar
  28. Körner C (1995) Leaf diffusive conductances in the major vegetation types on the globe. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 463–490Google Scholar
  29. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Physiol Plant Mol Biol 42:313–349CrossRefGoogle Scholar
  30. Kumudini S, Prior E, Omielan J, Tollenaar M (2008) Impact of Phakospsora pachyrhizi infection on soybean leaf photosynthesis and radiation absorption. Crop Sci 48:2343–2350CrossRefGoogle Scholar
  31. Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54:2393–2401CrossRefPubMedGoogle Scholar
  32. Long SP, Humphries SW, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662CrossRefGoogle Scholar
  33. Magalhães Filho JR, Amaral LR, Machado DFSP, Medina CL, Machado EC (2008) Deficiência hídrica, trocas gasosas e crescimento de raízes em laranjeira “Valencia” sobre dois tipos de porta enxerto. Bragantia 67:75–82CrossRefGoogle Scholar
  34. Martinell BJ, Julson LS, Emler CA, Huang Y, McCabe DE, Williams EJ (2002) Soybean Agrobacterium transformation method. United States Patent 6(384):301Google Scholar
  35. Martínez-Ferri E, Manrique E, Valladares F, Balaguer L (2004) Winter photoinhibition in the field involves different processes on four co-occurring Mediterranean tree species. Tree Physiol 24:981–990PubMedGoogle Scholar
  36. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence, a practical guide. J Exp Bot 51:659–668CrossRefPubMedGoogle Scholar
  37. Nilsson G (1985) Interactions between glyphosate and metals essential for plant growth. In: Grossbard E, Atkinson D (eds) The herbicide glyphosate. Butterworth, London, pp 35–47Google Scholar
  38. Paschal EH (1997) Soybean cultivar 88154622393. United States Patent 5,659,114Google Scholar
  39. Pihakaski S, Pihakaski K (1980) Effects of glyphosate on ultrastructure and photosynthesis of Pellia epiphylla. Ann Bot 46:133–141Google Scholar
  40. Pinkard EA, Patel V, Mohammed C (2006) Chlorophyll and nitrogen determination for plantation-grown Eucaliptus nitens and E. glogulus using a non-destructive meter. For Ecol Manag 223:211–217CrossRefGoogle Scholar
  41. Queiroz CGS, Garcia QS, Lemos Filho JP (2002) Atividade fotossintética e peroxidação de lipidios de membrana em plantas de aroreira-do-sertão sob estresse hídrico e após reidratação. Braz J Plant Physiol 14:59–63CrossRefGoogle Scholar
  42. Reddy KN, Zablotowicz RM (2003) Glyphosate-resistant soybean response to various salts of glyphosate and glyphosate accumulation in soybean nodules. Weed Sci 51:496–502CrossRefGoogle Scholar
  43. Reddy KN, Hoagland RE, Zablotowicz RM (2000) Effect of glyphosate on growth, chlorophyll content and nodulation in glyphosate-resistant soybeans (Glycine max) varieties. J New Seeds 2:37–52CrossRefGoogle Scholar
  44. 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 52:5139–5143CrossRefPubMedGoogle Scholar
  45. Richardson AD, Duigan SP, Berlyn GP (2002) An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytol 153:185–194CrossRefGoogle Scholar
  46. SAS Institute (2006) SAS/STAT version 9.1, SAS Institute, Cary, NCGoogle Scholar
  47. Shibles RM, Weber CR (1965) Leaf area, solar radiation interception, and dry matter production by various soybean planting patterns. Crop Sci 6:575–577CrossRefGoogle Scholar
  48. 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 94:821–89CrossRefGoogle Scholar
  49. SPSS (2000), SysStat © for Windows, Version 10Google Scholar
  50. Taiz L, Zeiger E (1998) Mineral nutrition. In: Plant physiology. Sinauer Associates, Sunderland, pp 111–144Google Scholar
  51. Taylor M, Hartnell G, Lucas D, Davis S, Nemeth M (2007) Comparison of broiler performance and carcass parameters when fed diets containing soybean meal produced from glyphosate-tolerant (MON 89788) control, or conventional reference soybeans. Poult Sci 86:2608–2614CrossRefPubMedGoogle Scholar
  52. Thompson JA, Schweitzer LE, Nelson RL (1996) Association of specific leaf weight, an estimate of chlorophyll, and chlorophyll content with apparent photosynthesis in soybean. Photosynth Res 49:1–10CrossRefGoogle Scholar
  53. von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387CrossRefGoogle Scholar
  54. Zablotowicz RM, Reddy KN (2007) Nitrogenase activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean. Crop Protec 26:370–376CrossRefGoogle Scholar
  55. Zaidi A, Khan MS, Rizvi PQ (2005) Effect of herbicides on growth, nodulation and nitrogen content of greengram. Agron Sustain Dev 25:497–504CrossRefGoogle Scholar
  56. Zlatev ZS, Yordanov IT (2004) Effects of soil drought on photosynthesis and chlorophyll fluorescence in bean plants. Bulg J Plant Physiol 30:3–18Google Scholar
  57. Zobiole LHS, Oliveira RS Jr, Huber DM, Constantin J, de Castro C, Oliveira FA, Oliveira A Jr (2010a) Glyphosate reduces shoot concentration of mineral nutrients in glyphosate-resistant soybeans. Plant Soil 328:57–69CrossRefGoogle Scholar
  58. 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. Pestic Biochem Physiol. doi: 10.1016/j.pestbp.2010.01.004 Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Luiz Henrique Saes Zobiole
    • 1
    Email author
  • Robert John Kremer
    • 2
  • Rubem Silvério de OliveiraJr
    • 1
  • Jamil Constantin
    • 1
  1. 1.Center for Advanced Studies in Weed Research (NAPD)State University of Maringá (UEM)MaringáBrazil
  2. 2.United States Department of Agriculture, Agricultural Research Service, Cropping Systems & Water Quality Research UnitUniversity of MissouriColumbiaUSA

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