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

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Abstract

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.

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Abbreviations

DAS:

Days after sowing

A:

Photosynthetic rate

E:

Transpiration rate

gs:

Stomatal conductance

Ci:

Sub-stomatal CO2

ETR:

Photosynthetic electron transport rates

Fo′:

Minimal fluorescence of a light adapted leaf

Fm′:

Maximal fluorescence of a light adapted leaf

Fs:

Steady state fluorescence of a light adapted leaf

Fv′/Fm′:

Intrinsic efficiency of photosystem 2

PS2:

Photosystem 2

PhiPS2:

Quantum efficiencies of photosynthetic electron transport through photosystem 2

PhiCO2:

Quantum yield based on CO2 assimilation

qN:

Non-photochemical quenching of chlorophyll fluorescence

qP:

Proportion of open reaction centers

RR1:

Glyphosate-resistant soybean—first generation

RR2:

Glyphosate-resistant soybean—second generation

Non-RR:

Conventional soybean near-isogenic parental line

References

  • 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

    Article  CAS  Google Scholar 

  • 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 

  • 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

    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 

  • 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 31:114–119

    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 

  • 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 141:141–153

    Article  Google Scholar 

  • 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 52:1865–1872

    Article  CAS  PubMed  Google Scholar 

  • Cole DJ (1985) Mode of action of glyphosate—a literature analysis. In: Grossbard E, Atkinson D (eds) The herbicide glyphosate. Butterworths, London, pp 48–74

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Da Matta FM, Loos RA, Rodrigues R, Barros RS (2001) Actual and potential photosynthetic rates of tropical crop species. R Bras Fisiol Veg 13:24–32

    Google Scholar 

  • Demming-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Ann Rev Plant Physiol Plant Mol Biol 43:599–626

    Article  Google Scholar 

  • Duke SO (2005) Taking stock of herbicide-resistant crops ten years after introduction. Pest Manage Sci 61:211–218

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Franz JE, Mao MK, Sikorski JA (1997) Glyphosate: a unique global herbicide; ACS Monograph 189. American Chemical Society, Washington, DC

    Google Scholar 

  • Fritschi FB, Ray JD (2007) Soybean leaf nitrogen, chlorophyll content, and chlorophyll a/b ratio. Photosynthetica 45:92–98

    Article  CAS  Google Scholar 

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

  • 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 990:87–92

    CAS  Google Scholar 

  • Gianessi LP, Carpenter JE (2000) Agricultural biotechnology: benefits of transgenic soybeans. National Center for Food and Agricultural Policy

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Ann Rev Plant Physiol Plant Mol Biol 4:655–684

    Article  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 Agric Food Chem 20:1195–1198

    Article  CAS  Google Scholar 

  • 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 55:87–96

    Article  CAS  Google Scholar 

  • Johal GS, Huber DM (2009) Glyphosate effects on diseases of plants. Eur J Agron 31:144–152

    Article  CAS  Google Scholar 

  • Kabachnik MI, TYa M, Dyatolva NM, Rudomino MV (1974) Organophosphorus complexones. Russ Chem Rev 43:733–744

    Article  Google Scholar 

  • King AC, Purcell LC, Vories ED (2001) Plant growth and nitrogenase activity of glyphosate-tolerant soybean in response to glyphosate applications. Agron J 93:179–186

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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 463–490

    Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Kumudini S, Prior E, Omielan J, Tollenaar M (2008) Impact of Phakospsora pachyrhizi infection on soybean leaf photosynthesis and radiation absorption. Crop Sci 48:2343–2350

    Article  Google Scholar 

  • 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 54:2393–2401

    Article  CAS  PubMed  Google Scholar 

  • Long SP, Humphries SW, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662

    Article  CAS  Google Scholar 

  • 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 67:75–82

    Article  Google Scholar 

  • Martinell BJ, Julson LS, Emler CA, Huang Y, McCabe DE, Williams EJ (2002) Soybean Agrobacterium transformation method. United States Patent 6(384):301

    Google Scholar 

  • 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 24:981–990

    PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence, a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  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 

  • Paschal EH (1997) Soybean cultivar 88154622393. United States Patent 5,659,114

  • Pihakaski S, Pihakaski K (1980) Effects of glyphosate on ultrastructure and photosynthesis of Pellia epiphylla. Ann Bot 46:133–141

    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. For Ecol Manag 223:211–217

    Article  Google Scholar 

  • 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 14:59–63

    Article  CAS  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

    Article  CAS  Google Scholar 

  • 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 2:37–52

    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

    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

    Article  CAS  Google Scholar 

  • SAS Institute (2006) SAS/STAT version 9.1, SAS Institute, Cary, NC

  • 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 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 

  • SPSS (2000), SysStat © for Windows, Version 10

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

  • 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 86:2608–2614

    Article  CAS  PubMed  Google Scholar 

  • 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 49:1–10

    Article  CAS  Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  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

    Article  CAS  Google Scholar 

  • Zaidi A, Khan MS, Rizvi PQ (2005) Effect of herbicides on growth, nodulation and nitrogen content of greengram. Agron Sustain Dev 25:497–504

    Article  CAS  Google Scholar 

  • Zlatev ZS, Yordanov IT (2004) Effects of soil drought on photosynthesis and chlorophyll fluorescence in bean plants. Bulg J Plant Physiol 30:3–18

    CAS  Google Scholar 

  • 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 328:57–69

    Article  CAS  Google Scholar 

  • 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 

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Acknowledgements

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.

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Authors and Affiliations

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

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

  2. United States Department of Agriculture, Agricultural Research Service, Cropping Systems & Water Quality Research Unit, University of Missouri, 327 Anheuser-Busch Natural Resources Building, Columbia, MO, 65211, USA

    Robert John Kremer

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  1. Luiz Henrique Saes Zobiole
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  3. Rubem Silvério de Oliveira Jr
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Correspondence to Luiz Henrique Saes Zobiole.

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Zobiole, L.H.S., Kremer, R.J., de Oliveira, R.S. et al. Glyphosate affects photosynthesis in first and second generation of glyphosate-resistant soybeans. Plant Soil 336, 251–265 (2010). https://doi.org/10.1007/s11104-010-0474-3

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