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Tolerance of DAS-444ø6-6 and DAS-444ø6-6 x DAS-81419-2 Soybeans to 2,4-D and Glyphosate in the Cerrado Region of Brazil

Tolerância da Soja DAS-444Ø6-6 e DAS-444Ø6-6 x DAS-81419-2 ao 2,4-D e Glifosato na Região do Cerrado Brasileiro

ABSTRACT:

The DAS-444Ø6-6 soybean expresses AAD-12, 2mEPSPS and PAT enzymes to provide, respectively, tolerance to 2,4-D, glyphosate and ammonium glufosinate. This event is also associated with DAS-81419-2 expressing Cry1Ac and Cry1F proteins to provide protection against a broad spectrum of soybean lepidopteran insect species. Successful adoption by growers of these technologies relies on the traits performing in the diverse environments of Brazil, especially under adverse weather conditions. The objective of this study was to characterize the tolerance of DAS 444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 soybeans to 2,4-D and glyphosate in the Cerrado region of Brazil. Eight trials across four sites were conducted in the 2015/2016 summer rainy season using a randomized complete block design, with a factorial arrangement of treatments. Factor A was 2,4-D choline salt (456 g a.e. L-1) + glyphosate DMA salt (480 g a.e. L-1) at 975 + 1,025 and 1,950 + 2,050 g a.e. ha-1, respectively and ready-mix of (2,4-D choline salt 195 g a.e. L-1 + glyphosate DMA salt 205 g a.e. L-1) at 2,000 (975 + 1,025) and 4,000 (1,950 + 2,050) g a.e. ha-1. Factor B was application timing at V3, V6 and R2 soybean growth stages. No visible symptoms of leaf chlorosis, epinasty, or growth inhibition were observed. Slight leaf droop was observed at 1 day after treatment (DAT), but it was null at 7 DAT. Less than 6% and 13% of leaf necrosis or injury were observed at 7 DAT, respectively, at 975 + 1,025 and 1,950 + 2,050 g a.e. ha-1 of 2,4-D choline salt + glyphosate DMA salt, regardless of applied as a ready-mix or not, but it was always 2% or less at 28 DAT. Crop grain yield was not influenced by herbicide treatments, application timing and their interaction, regardless of the soybean event and experimental site. DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 soybeans showed high tolerance to 2,4-D choline salt and glyphosate DMA in the Cerrado region of Brazil.

Keywords:
2,4-Dichlorophenoxyacetic acid; aryloxyalkanoate dioxygenase-12; ConkestaTM + Enlist E3TM; Enlist E3TM; Glycine max; injury

RESUMO:

A soja DAS-444Ø6-6 expressa as enzimas AAD-12, 2mEPSPS e PAT, conferindo, respectivamente, tolerância aos herbicidas 2,4-D, glifosato e glufosinato de amônio. Esse evento também pode ser combinado à soja DAS-81419-2, que expressa as enzimas Cry1Ac e Cry1F e confere resistência a amplo espectro de insetos lepidópteros. A adoção bem-sucedida dessas tecnologias requer eventos biotecnológicos que atuem nas diferentes regiões climáticas do país, sobretudo sob condições ambientais adversas. O objetivo deste estudo foi caracterizar a tolerância das sojas DAS 444Ø6-6 e DAS-444Ø6-6 x DAS-81419-2 aos herbicidas 2,4-D e glifosato na região do cerrado brasileiro. Oito ensaios foram realizados em campo em quatro locais durante a safra 2015/2016, usando-se delineamento de blocos ao acaso com tratamentos em esquema fatorial. O fator A foi 2,4-D sal colina (456 g e.a. L-1) + glifosato sal DMA (480 g e.a. L-1) nas doses de 975 + 1.025 e 1.950 + 2.050 g e.a. ha-1, e a mistura formulada de 2,4-D sal colina (195 g e.a. L-1) + glifosato sal DMA (205 g e.a. L-1) nas doses de 2.000 (975 + 1.025) e 4.000 (1.950 + 2.050) g e.a. ha-1. O fator B foi a aplicação nos estádios V3, V6 e R2. Não se observou clorose, epinastia e inibição de crescimento nas plantas de soja. Foi observado leve murchamento um dia após o tratamento (DAT), mas não aos 7 DAT. O 2,4-D sal colina + glifosato sal DMA nas doses de 975 + 1.025 e 1.950 + 2.050 g e.a. ha-1 causou, respectivamente, menos de 6 e 13% de necrose ou injúria aos 7 DAT, e menos de 2% na avaliação realizada aos 28 DAT, independentemente da formulação aplicada. O rendimento de grãos não foi afetado pelos fatores testados ou pela sua interação, independentemente da composição de eventos da soja e da localização da área experimental. A soja DAS-444Ø6-6, combinada ou não com a DAS-81419-2, mostrou elevada tolerância ao 2,4-D sal colina e glifosato sal DMA na região do cerrado no Brasil.

Palavras-chave:
2,4-Diclorofenoxiacetato; ácido; ariloxialcanoato dioxigenase-12; ConkestaTM + Enlist E3TM; Enlist E3TM; Glycine max; injúria

INTRODUCTION

Soybean, Glycine max (L.) Merrill, has considerable economic importance in the Cerrado region of Brazil, where it was grown in 20 million hectares in the 2015/2016 season (USDA, 2016USDA. Department of Agriculture. 2016. World Agricultural Supply and Demand Estimates (WASDE-552) Washington, DC. [accessed: 30 Nov. 2016]. Available at: Available at: http://usda.mannlib.cornell.edu/usda/waob/wasde/2010s/2016/wasde-04-12-2016.pdf
http://usda.mannlib.cornell.edu/usda/wao...
). In this region, glyphosate-resistant cultivars were highly adopted by soybean growers, gaining widespread acceptance by providing a convenient weed control system. However, extensive use of this herbicide as a “one-size-fits-all” approach led to selection by eight glyphosate-resistant weeds from 2003/2004 to 2017/2018 seasons (Heap, 2018Heap I. The international survey of herbicide resistant weeds. [accessed: 02 Mar. 2018]. Available from: Available from: http://www.weedscience.com .
http://www.weedscience.com...
). In addition, the same approach has induced significant biotype shifts to weed species with inherent tolerance to glyphosate (Marchi et al., 2013Marchi S.R. et al. Associações entre glifosato e herbicidas pós-emergentes para o controle de trapoeraba em soja RR®1. Rev Bras Herbic. 2013;12:23-30.; Takano et al., 2013Takano H.K. et al. Efeito da adição do 2,4-D ao glyphosate para o controle de espécies de plantas daninhas de difícil controle. Rev Bras Herbic. 2013;12:1-13.). Glyphosate-resistant and tolerant weeds are increasingly prevalent in soybean fields, and a diverse weed control system is needed to sustain soybean cropping in the Cerrado.

The 2,4-D (2,4-Dichlorophenoxyacetic) was the first organic and selective herbicide developed in the world, and since the 1970s it has been used in agriculture in more than 100 countries. Over the last decade, the discovery of genes from soil bacteria confering tolerance to 2,4-D and their transfer to crops have enabled the development of crops tolerant to this herbicide. 2,4-D-tolerant soybeans cultivars have been developed by insertion of the aryloxyalkanoate dioxygenase-12 (aad-12) gene from Delftia acidovorans (Wright et al., 2010Wright T.R. et al. Robust crop resistance to broadleaf and grass herbicides provided by aryloxyalkanoate dioxygenase transgenes. Proc Nat Acad Sci USA. 2010;107:20240-5.). The AAD-12 enzyme can metabolize 2,4-D by a rapid, single step, metabolic detoxification mediated by an Fe(II)/α-ketoglutarate-dependent dioxygenase (Griffin et al., 2013Griffin S.L. et al. Characterization of aryloxyalkanoate dioxygenase-12, a nonheme fe(ii)/α-ketoglutarate-dependent dioxygenase, expressed in transgenic soybean and Pseudomonas fluorescens. J Agric Food Chem. 2013;61:6589-96.). The introduction of AAD-12 soybean will cause changes in 2,4-D using and allow its pre and post-emergence spray to control broadleaf weeds on soybean (Robinson et al., 2012Robinson A.P. et al. Summer annual weed control with 2,4-D and glyphosate. Weed Technol. 2012;26:657-60.).

The DAS-444Ø6-6 soybean is the first triple-gene herbicide tolerant technology (Enlist E3TM) that expresses AAD 12, 2-mutant 5-enolpyruvyl shikimate-3-phosphate synthase (2mEPSPS) and phosphinothricin acetyltransferase (PAT) enzymes, which provide, respectively, tolerance to 2,4-D, glyphosate and ammonium glufosinate herbicides (Lepping et al., 2013Lepping M.D., Herman R.A., Potts B.L. Compositional equivalence of DAS 444Ø6 6 (AAD-12 + 2mEPSPS + PAT) herbicide-tolerant soybean and nontransgenic soybean. J Agric Food Chem. 2013;61:11180-90.). In Brazil, this novel herbicide trait package is also associated with the soybean event DAS-81419-2 (ConkestaTM), which consists of insect-resistant technology that expresses Cry1Ac and Cry1F proteins and provides protection against a broad spectrum of soybean lepidopteran insect species (Fast et al. 2015Fast B.J. et al. Insect-protected event DAS-81419-2 soybean (Glycine max L.) grown in the United States and Brazil is compositionally equivalent to non-transgenic soybean. J Agric Food Chem. 2015;63:2063-73.; Marques et al., 2016Marques L.H. et al. Efficacy of soybean’s event DAS-81419-2 expressing Cry1F and Cry1Ac to manage key tropical Lepidopteran pests under field conditions in Brazil. J Econ Entomol. 2016;109:1922-8.). The combination of these advanced technologies will provide Brazilian soybean growers with a convenient and more diverse system for management of both weeds and insects.

Herbicide-resistant crops treated with the associated herbicides at situations of high doses or in adverse weather conditions have eventually shown reduction on their performance parameters. Glyphosate-resistant soybean had a significant reduction in root, shoot, and nodule biomass when glyphosate was applied at 1,200 or 2,400 g a.e. ha-1 (Zobiole et al., 2012Zobiole L.H.S. et al. Glyphosate effects on photosynthesis, nutrient accumulation, and nodulation in glyphosate-resistant soybean. J Plant Nutr Soil Sci. 2012;175:319-30). Moreover, drought stress condition following two 1,680 g a.e. ha-1 glyphosate treatments to glyphosate-resistant soybean reduced crop grain yield by 12 to 25% (King et al., 2001King C.A. et al. Plant growth and nitrogenase activity of glyphosate-resistant soybean in response to foliar glyphosate applications. Agron J. 2001;93:179-86.). Thus, successful adoption by growers of DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 soybeans events relies on the traits performing in the diverse climates conditions. In particular, these technologies need to be evaluated in the Cerrado region of Brazil, where drought and high temperature might often cause intense plant stress on soybean crops.

Therefore, the objective of this research was to characterize the tolerance of DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 soybeans after foliar application of 2,4-D and glyphosate in the Cerrado region of Brazil.

MATERIALS AND METHODS

Eight trials were conducted under conventional field conditions during the 2015/2016 summer rainy season, at four different sites distributed across the Cerrado region of Brazil (Table 1). In each site, two trials were equally conducted side by side, testing the same list of herbicide treatments, with the composition of soybean events being the only difference between trials. The selection of sites was based on the commercial importance of soybean production and reflected the environmental conditions normally found in the Brazilian Cerrado. Air temperature and rainfall rate were monitored by automated remote weather stations, and Figure 1 shows the data collected daily for each site throughout the season. The trials always followed strict adherence to regulatory requirements of Brazil and were conducted at accredited certified sites containing Quality Certificate Biosafety.

Table 1
Experimental sites and three soil characteristics

Figure 1
Daily air temperature(1) and natural rainfall rate along the season observed in Indianópolis (MG), Rio Verde (GO), Rondonópolis (MT) and Sorriso (MT).

The soybean cultivars used in the trials come from breeding programs of Sementes Don Mário (GDM) and Tropical Melhoramento e Genética Ltda. (TMG) for the Brazilian Cerrado (Table 2). These cultivars contained the soybean event DAS-444Ø6-6 (Enlist E3TM) and its stack with DAS-81419-2 (ConkestaTM) (Dow AgroSciences LLC, Indianapolis, IN). The fields were planted in all situations at row spacing of 45 cm, and in-row spacing from 6 to 7 cm, with seed rate ranging from 320,000 to 360,000 seeds ha-1. Agronomic practices and inputs used for crop establishment and maintenance were those recommended for the crop in the Central region of Brazil (Embrapa, 2011Empresa Brasileira de Pesquisa Agropecuária - Embrapa. Tecnologias de produção de soja - Região Central do Brasil, 2012 e 2013. Londrina: Embrapa Soja, 2011. 261p. (Sistemas de Produção/Embrapa Soja, 15).). The trials relied on natural rainfall coming from the summer rainy season, and artificial irrigation was not implemented even in periods of severe water deficit stress.

Table 2
Soybean cultivars and their maturation group

The trials were arranged in a complete randomized block design and the treatments were arranged as a factorial (4 x 3), using four replications, except one case, which had three replications. Factor A was four post-emergence herbicide treatments: 2,4-D choline salt (456 g a.e. L-1) + glyphosate dimethylamine (DMA) salt (480 g a.e. L-1) at 975 + 1,025 and 1,950 + 2,050 g a.e. ha-1, respectively; and, ready-mix formulation of (2,4-D choline salt 195 g a.e. L-1 + glyphosate DMA salt 205 g a.e. L-1) at 2,000 (975 + 1,025) and 4,000 (1,950 + 2,050) g a.e. ha-1. In addition, an untreated-check plot was added as a standard of comparison of the herbicides, which was permanently maintained weed free through periodic manual weeding. The twice rate (1,950 + 2,050 g a.e. ha-1) was included to determine the extent of tolerance enabled by DAS-444Ø6-6 event in a field situation in which overlap application occurs. Factor B was three application timings at V3 (three trifoliate leaves), V6 (six trifoliate leaves) and R2 (full flowering) growth stages, according to Fehr and Caviness (1977Fehr W.R., Caviness C.E. Stages of soybean development. Ames: Iowa State University, 1977. 12p. (Special Report, 80).). The treatments were always applied in a water carrier with volume of 100 L ha-1 at 25-40 PSI using a CO2 backpack sprayer with a 3.0 m boom using AIXR 110.015 flat-fan nozzles.

Visible leaf chlorosis, epinasty, necrosis, growth inhibition, drooping and overall injury were assessed separately, from 0 (no injury) to 100% (complete plant death), according to the scale of Camper (1986Camper N.D. Research methods in weed science. 3rd ed. Champaign: Southern Weed Science Society, 1986. 486p.). These herbicide symptoms were assessed separately to improve the assessments of the evaluators and detect eventual differential behavior in their magnitude along the evaluations. Visible drooping symptom was assessed at 1 and 7 days after herbicide treatment (DAT), while the other explanatory variables of injury were assessed at 7, 14 and 28 DAT. Also, crop grain yield and grain moisture were assessed at soybean maturity by harvesting the two central rows sprayed and adjusting grain mass to 13% of moisture. Data were subjected to analysis of variance by the F-test for significant effects (p<0.05) and Tukey’s pairwise comparison test for mean separation of the tested treatments. The tested factors and their interaction were considered as fixed effects and locations as a random variable because there was homogeneity of error variances (Zimmermann, 2004Zimmermann F.J.P. Estatística aplicada à pesquisa agrícola. Santo Antônio de Goiás: Embrapa Arroz e Feijão, 2004. 402p.).

RESULTS AND DISCUSSION

The data collected on weather conditions indicate that plants possibly suffered periods of stress during the season, especially high air temperature (>35 oC) at the four experimental sites (Figure 1). Nevertheless, crop injuries were null or low regardless of herbicide treatment and application timing, as well as soybean event and experimental site. In fact, no leaf chlorosis, epinasty, or growth inhibition were observed, while there was slight leaf droop at 1 day after treatment (DAT), but it was null at 7 DAT (Table 3). The 2,4-D choline salt + glyphosate DMA salt at 975 + 1,025 g a.e. ha-1 caused up to 6, 4, and 1% of necrosis or injury, respectively, in the assessments at 7, 14, and 28 DAT. The 2,4-D choline salt + glyphosate DMA salt at 1,950 + 2,050 g a.e. ha-1 caused up to 13, 10, and 2% of necrosis or injury, respectively, at 7, 14, and 28 DAT (Tables 4 and5).

Table 3
Visible leaf drooping (0 to 100%) at 1 and 7 days after treatment (DAT) for the soybean events DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 observed in Indianópolis (MG), Rio Verde (GO), Rondonópolis (MT) and Sorriso (MT) (mean of four trials by soybean event) in the 2015/2016 summer rainy season
Table 4
Visible leaf necrosis (0 to 100%) at 7, 14, and 28 days after treatment (DAT) for the soybean events DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 observed in Indianópolis (MG), Rio Verde (GO), Rondonópolis (MT) and Sorriso (MT) (mean of four trials by soybean event) in the 2015/2016 summer rainy season
Table 5
Visible overall injury (0 to 100%) at 7, 14, and 28 days after treatment (DAT) for the soybean events DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 observed in Indianópolis (MG), Rio Verde (GO), Rondonópolis (MT) and Sorriso (MT) (mean of four trials by soybean event) in the 2015/2016 summer rainy season

The safe use of 2,4-D and glyphosate on different soybean cultivars containing the DAS-444Ø6-6 event was confirmed, even in situations with plant stress, as in the Brazilian Cerrado region. In other studies, conducted in in vitro conditions, the tolerance to 2,4-D of AAD-12 soybean had been very effective and consistent (Wright et al., 2010Wright T.R. et al. Robust crop resistance to broadleaf and grass herbicides provided by aryloxyalkanoate dioxygenase transgenes. Proc Nat Acad Sci USA. 2010;107:20240-5.; Griffin et al., 2013Griffin S.L. et al. Characterization of aryloxyalkanoate dioxygenase-12, a nonheme fe(ii)/α-ketoglutarate-dependent dioxygenase, expressed in transgenic soybean and Pseudomonas fluorescens. J Agric Food Chem. 2013;61:6589-96.). Also, in a field trial, the foliar application of 2,4-D at 1,120 or 2,240 g a.e. ha-1 at V5 and R2 growth stages caused ? 3% injury on all evaluation dates (Robinson et al., 2015Robinson A.P. et al. Response of aryloxyalkanoate dioxygenase-12 transformed soybean yield components to postemergence 2,4-D. Weed Sci. 2015;63:242-7.). The injury was typically small necrotic spots on the treated leaves, as seen in our study - Figure 2, which were gradually covered and reduced by new leaf growth. Leaf necrosis might have been caused by a high concentration of active 2,4-D, or inert ingredients of the formulation might have caused the damage (Robinson et al., 2015).

Figure 2
Examples of DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 soybeans exhibiting 1-2% (A and B), 4-5% (C and D), 7-8% (E and F) and 10-11% (G and H) of leaf necrosis at 7 days after 2,4-D choline salt and glyphosate DMA treatments.

Crop grain yield of both soybean events was not significantly influenced by herbicide treatments, herbicide application timing and their interaction, regardless of the experimental site (Table 6). Thus, there was no yield reduction on the soybean cultivars expressing the DAS-444Ø6-6 event because of post emergence applications of 2,4-D choline salt and glyphosate DMA salt. Also, the cultivars containing this event showed equal level of tolerance to glyphosate, compared to the glyphosate-tolerant cultivars currently available to soybean growers. The spray of 2,4-D at 1,120 or 2,240 g a.e. ha-1 at V5 and R2 greowth stages of soybean with AAD-12 trait did not influence the yield or its components, either (Robinson et al., 2015Robinson A.P. et al. Response of aryloxyalkanoate dioxygenase-12 transformed soybean yield components to postemergence 2,4-D. Weed Sci. 2015;63:242-7.). This research found that minimal soybean injury occurred after 2,4-D treatments were applied and did not reduce the grain yield or yield components of AAD-12 soybean.

Table 6
P-values of the analysis of variance through the F-test for grain yield of soybean events DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 in Indianópolis (MG), Rio Verde (GO), Rondonópolis (MT) and Sorriso (MT) in the 2015/2016 summer rainy season

The triple-herbicide tolerance to 2,4-D, glyphosate and glufosinate provided by DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 soybeans will offer advances over single-herbicide technologies. In fact, several glyphosate-resistant weeds such as Conyzaspp. and Amaranthus palmeri, as well as glyphosate-tolerant weeds such as Commelinaspp., Euphorbiaspp., Ipomoeaspp., Richardiaspp., Spermacocespp., among others, can be well controlled by 2,4-D (Kruger et al., 2010Kruger G.R. et al. Control of horseweed (Conyza canadensis) with growth regulator herbicides. Weed Technol. 2010;24:425 9.; Marchi et al., 2013Marchi S.R. et al. Associações entre glifosato e herbicidas pós-emergentes para o controle de trapoeraba em soja RR®1. Rev Bras Herbic. 2013;12:23-30.; Takano et al., 2013Takano H.K. et al. Efeito da adição do 2,4-D ao glyphosate para o controle de espécies de plantas daninhas de difícil controle. Rev Bras Herbic. 2013;12:1-13.; Trezzi et al., 2016Trezzi M.M. et al. Características biológicas, resistência a herbicidas e manejo de Amaranthus palmeri em agroecossistemas. Rev Bras Herbic. 2016;15:48-57.). In addition to providing more efficient and convenient control of a broad weed spectrum, chemical diversity will deliver lower probability of weed resistance to herbicides. However, DAS-444Ø6-6 soybean will only be sustainable when used as part of an integrated weed management program and by implementing good agricultural practices. The utilization of no-tillage systems, residual herbicides and good agricultural practices is still important to prevent the evolution of weed resistance to herbicides.

In our research, the DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 soybeans showed high tolerance to 2,4-D choline salt and glyphosate DMA in four different sites across the Cerrado region of Brazil. The foliar application of these herbicides caused very low levels of visual necrosis and injury and did not reduce the potential of grain yield of both soybean events evaluated. The DAS-444Ø6-6 and DAS-444Ø6-6 x DAS-81419-2 soybeans will allow the safe use of 2,4-D and glyphosate for postemergence weed control in soybean in the Brazilian Cerrado.

ACKNOWLEDGMENTS

We gratefully acknowledge the efforts and technical assistance of our many colleagues at Dow AgroSciences Ind. Ltda, Coodetec Desenvolvimento, Produção e Comercialização Agrícola Ltda, as well as the support and partnership of Fundação de Apoio à Pesquisa Agropecuária de Mato Grosso, Sementes Don Mário and Tropical Melhoramento e Genética Ltda

REFERENCES

  • Camper N.D. Research methods in weed science. 3rd ed. Champaign: Southern Weed Science Society, 1986. 486p.
  • Empresa Brasileira de Pesquisa Agropecuária - Embrapa. Tecnologias de produção de soja - Região Central do Brasil, 2012 e 2013. Londrina: Embrapa Soja, 2011. 261p. (Sistemas de Produção/Embrapa Soja, 15).
  • Fast B.J. et al. Insect-protected event DAS-81419-2 soybean (Glycine max L.) grown in the United States and Brazil is compositionally equivalent to non-transgenic soybean. J Agric Food Chem. 2015;63:2063-73.
  • Fehr W.R., Caviness C.E. Stages of soybean development. Ames: Iowa State University, 1977. 12p. (Special Report, 80).
  • Griffin S.L. et al. Characterization of aryloxyalkanoate dioxygenase-12, a nonheme fe(ii)/α-ketoglutarate-dependent dioxygenase, expressed in transgenic soybean and Pseudomonas fluorescens J Agric Food Chem. 2013;61:6589-96.
  • Heap I. The international survey of herbicide resistant weeds. [accessed: 02 Mar. 2018]. Available from: Available from: http://www.weedscience.com
    » http://www.weedscience.com
  • King C.A. et al. Plant growth and nitrogenase activity of glyphosate-resistant soybean in response to foliar glyphosate applications. Agron J. 2001;93:179-86.
  • Kruger G.R. et al. Control of horseweed (Conyza canadensis) with growth regulator herbicides. Weed Technol. 2010;24:425 9.
  • Lepping M.D., Herman R.A., Potts B.L. Compositional equivalence of DAS 444Ø6 6 (AAD-12 + 2mEPSPS + PAT) herbicide-tolerant soybean and nontransgenic soybean. J Agric Food Chem. 2013;61:11180-90.
  • Marchi S.R. et al. Associações entre glifosato e herbicidas pós-emergentes para o controle de trapoeraba em soja RR®1. Rev Bras Herbic. 2013;12:23-30.
  • Marques L.H. et al. Efficacy of soybean’s event DAS-81419-2 expressing Cry1F and Cry1Ac to manage key tropical Lepidopteran pests under field conditions in Brazil. J Econ Entomol. 2016;109:1922-8.
  • Robinson A.P. et al. Response of aryloxyalkanoate dioxygenase-12 transformed soybean yield components to postemergence 2,4-D. Weed Sci. 2015;63:242-7.
  • Robinson A.P. et al. Summer annual weed control with 2,4-D and glyphosate. Weed Technol. 2012;26:657-60.
  • Takano H.K. et al. Efeito da adição do 2,4-D ao glyphosate para o controle de espécies de plantas daninhas de difícil controle. Rev Bras Herbic. 2013;12:1-13.
  • Trezzi M.M. et al. Características biológicas, resistência a herbicidas e manejo de Amaranthus palmeri em agroecossistemas. Rev Bras Herbic. 2016;15:48-57.
  • USDA. Department of Agriculture. 2016. World Agricultural Supply and Demand Estimates (WASDE-552) Washington, DC. [accessed: 30 Nov. 2016]. Available at: Available at: http://usda.mannlib.cornell.edu/usda/waob/wasde/2010s/2016/wasde-04-12-2016.pdf
    » http://usda.mannlib.cornell.edu/usda/waob/wasde/2010s/2016/wasde-04-12-2016.pdf
  • Wright T.R. et al. Robust crop resistance to broadleaf and grass herbicides provided by aryloxyalkanoate dioxygenase transgenes. Proc Nat Acad Sci USA. 2010;107:20240-5.
  • Zimmermann F.J.P. Estatística aplicada à pesquisa agrícola. Santo Antônio de Goiás: Embrapa Arroz e Feijão, 2004. 402p.
  • Zobiole L.H.S. et al. Glyphosate effects on photosynthesis, nutrient accumulation, and nodulation in glyphosate-resistant soybean. J Plant Nutr Soil Sci. 2012;175:319-30

Publication Dates

  • Publication in this collection
    2018

History

  • Received
    02 Apr 2017
  • Accepted
    11 May 2017
Sociedade Brasileira da Ciência das Plantas Daninhas Departamento de Fitotecnia - DFT, Universidade Federal de Viçosa - UFV, 36570-000 - Viçosa-MG - Brasil, Tel./Fax::(+55 31) 3899-2611 - Viçosa - MG - Brazil
E-mail: rpdaninha@gmail.com