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Revista de Ciências Agrárias

Print version ISSN 0871-018X

Rev. de Ciências Agrárias vol.42 no.4 Lisboa Dec. 2019 


Techniques for mitigating the symptoms of injury of glyphosate in RR and RR2 soybean

Técnicas de mitigação de sintomas de injúrias de glyphosate em soja RR e RR2

Luisa Carolina Baccin1,*, Fábio Henrique Krenchinski2, Leandro Paiola Albrecht3, Gabriela Gayoso da Cruz3, Alfredo Júnior Paiola Albrecht3, Mateus Daupubel Mattiuzzi4, Carine Cantú5 e Aline Pertuzati6

1 Departamento de Produção Vegetal, ESALQ/USP. Piracicaba, SP, Brazil

2 Departamento de Produção e Melhoramento Vegetal, UNESP. Botucatu, SP, Brazil

3 Departamento de Ciências Agronômicas, UFPR. Palotina, PR, Brazil

4 Departamento de Agronomia, UEM. Maringá, PR, Brazil

5 Centro de Ciências Agrarias, Unioeste.  Marechal Cândido Rondon, PR, Brazil

6 Departamento de Agronomia, Unicentro.  Guarapuava, PR, Brazil



The use of high rates of glyphosate, even if tolerant (RR) technology, can cause leaf insults, such as the yellow flashing effect, which is characterized by a yellowing of the leaves, which can lead to loss of yield. The present study aimed to increase doses of glyphosate in tolerant soybean. Tests were conducted in greenhouse 2015/2016 and 2016/2017, in Palotina, western region of Paraná in a completely randomized arrangement. The first assay was conducted in a 3x8 factorial set (products x cultivars) with four replicates mixed with glyphosate with growth regulator, one compound of amino acids and one source of manganese, and in the second a factorial scheme 6x3 (products x cultivars) using glyphosate, a growth regulator, a source of manganese and the glyphosate associated to the other products, besides a control without application. A phytotoxicity, chlorophyll index, shoot dry mass and root mass were evaluated visually. A variation of response to cultivar was observed due to characteristics of each genotype. The differences between the products were not observed. A cultivar ‘M6210' presented greater symptom of crop injury while cultivating ‘BMX Ponta', presenting greater tolerance. No phytotoxic effect was observed for the test.

Keywords: Glycine max L. Merr., herbicides; yellow flashing, transgenic crops.


A utilização de altas doses de glyphosate, mesmo na tecnologia tolerante (RR) pode causar injúrias nas plantas, conhecido como efeito “Yellow flashing”, que é caracterizado por um amarelecimento das folhas apicais, podendo levar à perda de produtividade. O presente estudo objetivou avaliar técnicas visando a atenuação do efeito de doses de glyphosate em cultivares tolerantes de soja (RR e RR2). Os ensaios foram conduzidos em estufa nos anos 2015/2016 e 2016/2017, em Palotina, região oeste do Paraná em um arranjo inteiramente casualizado. O primeiro ensaio foi conduzido em arranjo fatorial 3x8 (produtos x cultivares) com quatro repetições utilizando misturas de glyphosate com regulador de crescimento, um composto de aminoácidos e uma fonte de manganês, e no segundo um esquema fatorial 6x3 (produtos x cultivares) utilizando glyphosate, um regulador de crescimento, uma fonte de manganês isolados e o glyphosate associado aos demais produtos, além de um tratamento controle sem aplicação. Foram avaliados visualmente a fitotoxicidade, índice de clorofila, massa seca de parte aérea e de raiz. Observou-se uma diferença de resposta para as cultivares devido a características de cada genótipo. Não foram observadas diferenças entre os produtos. A cultivar ‘M6210' apresentou-se maior sintoma de fitointoxicação enquanto a cultivar ‘BMX Ponta' apresentou maior tolerância. Para o segundo ensaio não foi observado efeito fitotóxico.

Palavras-chave:Glycine maxL.,herbicidas, yellow flashing,transgénicos.


The Roundup Ready® (RR) technology introduced genes (cp4epsps) from Agrobacterium sp. to soybean plants, which codes enzyme EPSP synthase with a high catalytic activity in the presence of glyphosate and maintains aromatic amino acid levels in tolerant plants (Reddy, 2001).

Previous studies have shown that the effects of glyphosate application to RR soybean causes a reduction of chlorophyll content and increased phytotoxicity, possibly because of AMPA (aminomethylphosphonic acid) accumulation, which is the first phytotoxic metabolite of glyphosate. Some cultivars of RR soybean exhibit small visible injuries while other cultivars present more pronounced symptoms.

Lower volume of plant biomass, less nodulation and, consequently, reduced biological nitrogen fixation, as well as reduced uptake levels of macro- and micro-nutrients, in addition to low yields and low seeds quality are common effects (Zobiole et al., 2009a,b; Albrecht et al., 2011, 2014a,b; Krenchinski et al., 2017).

With the increasing utilization of glyphosate-resistant technology, farmers have noticed that some RR cultivars show visible injuries after post-emergence application of the herbicide. A typical symptom that can be seen in the field is called “yellow flashing”, which consists of yellowing of the upper leaves of the plant (Zobiole et al., 2011).

Glyphosate application is performed at various crop stages, depending on the level of weed infestation, but Albrecht et al. (2014a) demonstrated that glyphosate application at the R1 stage causes a reduction of plants height and an increase of phytotoxicity. Reddy and Zablotowicz (2003) observed that application of glyphosate reduced nodule mass.

Studies conducted with herbicides indicate that an exogenous application of amino acids may be a tool to reduce inhibition of plants growth. In the case of glyphosate, which inhibits enzyme 5-enol–pyruvyl-3-shikimate-phosphate (EPSP) synthase, some studies indicate that exogenous applications of amino acid mixtures succeeded in preventing growth inhibition (Zobiole et al., 2010, 2011).

The use of bioregulators may assist the plant in the recovery from these undesirable effects, as a form to increase crop growth and yields. Substances analogous to plant hormones, called plant regulators or bioregulators, have been largely applied in several crops, and studies have reported its effectiveness in soybean crops by improving the plants agronomic performance and seeds production components (Albrecht et al., 2011; Zobiole et al., 2011).

The use of manganese has also been studied to prevent damages caused by the herbicide due to the reduced chlorophyll content in the plants. This occurs in response to a manganese-induced deficiency after application of glyphosate caused by a low efficiency of nutrient accumulation due to the action of the herbicide in the same metabolic pathway. It was observed that even with the application of low doses of glyphosate the absorption and the translocation of manganese in the plants was reduced (Rosolem et al., 2010; Zobiole et al., 2010).

Regarding the mitigation of glyphosate application symptoms in RR soybean, supplementation provided to the plant, with application of products associated with the herbicide is a technically viable option for the producer, so the aim of this study was to assess the efficiency of products used for reversal of phytotoxicity caused by glyphosate herbicides in Roundup Ready® soybean cultivars.


Plant material and growing conditions

Two experiments were carried out from November 2015 to January 2016 (experiment I) and March to May 2017 (experiment II). The experiments were conducted in a greenhouse under controlled ambient conditions, temperature between 20-25ºC, 60% of mean relative humidity, 5 mm/day of mean precipitation, and a photoperiod of nearly 12 hours, in the municipality of Palotina, in the western of state of Paraná, Brazil. Both experiments were carried out in a controlled ambient condition free of pests and diseases.

From the literature review, the phytotoxic effect of the application of high doses of glyphosate on RR and RR2 soybean was observed, causing productivity reduction. An initial screening was carried out to identify cultivars that presented greater and lesser injuries.

For the experiment I, eight RR soybean cultivars were used: ‘TMG 7062', ‘MONSOY 6210', ‘BMX Ponta', ‘CD 2720' and RR2: ‘TMG 7262', ‘BRS 359', ‘BRS 388' and ‘CD 2737'. The cultivars ‘TMG 7062' and ‘TMG 7262' have a semi-determined growth habit, while the other cultivars used in the experiment have an undetermined growth habit.

For the second experiment, the cultivars ‘MONSOY 6210', ‘TMG 7262' and ‘BMX Ponta' were utilized. These cultivars present an undetermined growth habit and the effects of manganese and bioregulator on the reversal of glyphosate phytotoxicity were evaluated.

In both experiments, 5 L plastic pots filled with eutrophic Red Latosol were used and two plants were sown per pot.

Experimental design

Experiment 1 was conducted on a 3x8 factorial arrangement (products x cultivars) with four replicates, each pot containing two plants which were considered one replicate, totalizing 96 pots. 

The second experiment was conducted on a 3x6 factorial arrangement and six treatments, containing four replicates, and each pot with two plants was considered a replicate, totalizing 72 pots, both in a completely randomized design (CRD) with factorial arrangement.


In the first experiment the treatments consisted of combinations of Roundup Ready® glyphosate (2880 g a.e. ha-1) with plant growth regulator (Stimulate®) (250 mL ha-1), with chelated manganese (125g ha-1) and with amino acids compound (Protemax®) (1 L ha-1). The products and doses are described in Table 1.

The treatments of the second experiment consisted of one untreated control, Roundup Ready glyphosate (2880 g a.e. ha-1), Stimulatebioregulator (250 mL ha-1), and manganese (184.8 g ha-1) alone and combined with the Stimulateherbicide and with manganese. The treatments and doses used are described in Table 2.

Herbicide sprayed conditions

In both experiments, application was conducted at the V4 growth stage using a CO2pressurized backpack sprayer, at constant pressure, providing 150 L ha-1 of fluid volume.

Phytotoxicity rates

A score for visible phytotoxicity was given at 7, 14, 21, 28 and 35 days after application (DAA), ranging from 0 to 100%, where score zero is attributed to asymptomatic plants and 100% represents plant death from herbicide effect. The scores for visible damage were assessed according to the scoring proposed by the Brazilian Society of Weed Science (SBCPD, 1995) and chlorophyll content was also measured with the aid of a chlorophyll meter at 7, 14, 21, 28 and 35 DAA.

At 35 DAA, the plants were removed from the pots and the roots were separated from the shoots. Measurements of shoot dry matter were performed. The roots were washed and the nodules were carefully removed. The number and weight of nodules were also assessed as well as the root dry matter.

For the second experiment, visible phytotoxicity damages were assessed with scores at 3, 7, 14 DAA, also following the scores scale proposed by the Brazilian Society of Weed Science (SBCPD, 1995) ranging from 0 to 100%, where score zero is attributed to asymptomatic plants and 100% represents plant death from herbicide effect.

The chlorophyll content was measured at 3, 7, and 14 DAA, and at 14 DAA one plant was removed from each pot for measurement of shoot fresh matter and shoot dry matter.

Statistical analysis

The data were submitted to analysis of variance (ANOVA), the necessary splits were performed in the factorial interaction, and the means tested by Tukey at 5% probability (p≤0.05) and, when necessary, the data transformations were performed (Ferreira, 2011).


It was observed in two experiments that there was a significant interaction and the factors were dependent. There was a difference among the products due to the characteristics of each cultivar.

Experiment I

Visible phytotoxicity symptoms were more pronounced at 7 and 14 days after application (DAA) (Table 3). At 7 DAA, both the growth regulator and amino acid showed varying effects on the studied cultivars. For the ‘BRS 359' cultivar, the amino acid had a higher effect between both products, presenting a lower score of visible phytotoxicity. At 21 and 28 DAA, there was no difference between the products for each cultivar studied, but there was a distinct response for the cultivars (Table 4).

At 35 DAA (Table 5) the visible injuries caused by application of the herbicide decreased considerably, and only cultivar ‘Monsoy 6210' exhibited a slight mild toxicity symptom when treated with bioregulator and amino acid, showing in this case the manganese efficiency.

With respect to shoot dry matter, the association with manganese was more effective for cultivars ‘BMX Ponta' and ‘BRS 388', where the amino acid was more effective for cultivars ‘BRS 388' and ‘CD 2737', in which a positive effect of Stimulate® was observed (Table 6).

Considering the number of nodules (Table 7), ‘BMX Ponta' and ‘Monsoy 6210' showed a greater number of nodules when treated with manganese. Regarding the nodules weight, no difference was found for the different product combinations with glyphosate.

At 7 DAA, a decrease in chlorophyll content was observed, but there was a recovery by 35 DAA. Cultivar ‘M6210' showed a better response to the association of glyphosate with amino acid, but cultivar ‘BMX Ponta' exhibited a different behavior: at 28 DAA, this cultivar was more responsive to the application of glyphosate associated with manganese (Figure 1).

Cultivars ‘TMG 7262', ‘BRS 359' and ‘CD 2737' did not show differences with application of the products. For ‘BRS 388' (Figure 2), it was found, at 21 DAA, that glyphosate application combined with amino acid provided a higher chlorophyll content, demonstrating the product efficiency.

Experiment II

In the second experiment, cultivar ‘BMX Ponta' exhibited more tolerance to the application of the herbicide and ‘Monsoy 6210' was more susceptible to phytotoxicity. For ‘TMG 7262' (Figure 3), the application of reversing products resulted in higher phytotoxicity scores compared to the application of the herbicide alone.



Regarding shoot dry weight (g), there were no differences between the products for each cultivar (Table 8), as well as for chlorophyll content (Table 9). It was found that the phytotoxicity level observed in the second experiment in general was less pronounced compared to the first experiment, making it more difficult to reach a conclusion about the technologies.




The visible symptoms may be caused by the immobilization of divalent cations such as iron and manganese, since glyphosate is a phosphonic acid that chelates cations, according to Merotto et al. (2015). Glyphosate is mobile by phloem and is rapidly translocated to younger tissues of root and tissue growth, accumulating at millimolar concentrations after foliar application, which may lead to a slight reduction in dry root mass but the accumulation can be overcome without causing effects on productivity (Feng et al., 1999; Hetherington et al., 1999).

Duration of the effect is also related to the plant ability to absorb the elements immobilized by glyphosate. In the first experiment, the visible injury diminished considerably at 28 DAA, when application was conducted during the vegetative stage, corroborating data of Krenchinski et al. (2017) and Albrecht et al. (2014a).

The visible phytotoxicity symptom has a linear relation with the herbicide dosage. Krenchinski et al. (2017) mention that the phytotoxic effects found in their study were higher with the highest dose of glyphosate applied. As in the present study, the authors observed that the phytotoxicity symptoms had diminished significantly at 35 DAA due the plant recovery.

The chlorophyll content was affected in both experiments. The association of glyphosate with manganese provided a satisfactory result, with an increase in the chlorophyll content. Glyphosate has a negative linear effect on the chlorophyll content because this herbicide can cause damages to chloroplasts. Other hypothesis is that the herbicide chelates the cationic ions such as iron and manganese, and the enzymes required for chlorophyll biosynthesis (catalase and peroxidase) are extremely sensitive to a deficiency of these micronutrients (Malavolta et al., 1989; Reddy et al., 2004). 

The association of bioregulators with glyphosate provides modifications for having a direct physiological action on the plants, especially when the herbicide is applied on the leaves during the vegetative stage. Plants that are in hormonal balance exhibit an adequate growth of shoots and roots, with a good development of vegetative and reproductive structures (Albrecht et al., 2010, 2012), as observed in the present study.

Foliar application of manganese increased the production of plants dry matter, as pointed out in studies by Oliveira Junior et al. (2000). Such association also provided a greater number of nodules per plant. Glyphosate applications may inhibit soybean-fixing bacterium (rhysobium) symbiosis. Manganese plays a co-factor role in the activation of various enzymes, and this micronutrient is responsible for the biosynthesis of amino acids and secondary products, such as flavonoids. Flavonoids, in turn, act in the root system stimulating nodulation, and, therefore, the manganese deficiency and the stress undergone by the plant signals to the symbiotic bacteria to discontinue the biological nitrogen fixation (Albrecht et al., 2010).

In a study containing manganese mixture with glyphosate, Freitas et al. (2018) observed the increase in productivity after treatment with manganese-containing the fertilizer in its formulation. This exogenous supply of the nutrient can overcome the temporary deficiency caused by the herbicide without any alteration in the agronomic performance of the crop.

Santos et al. (2015) conducted research with manganese application and was successful in increasing productivity assessment for this treatment. Bertolin et al. (2010) when evaluating the efficiency of plant regulators also observed increased productivity. This efficiency can be attributed due to the hormonal balance that is affected in the plant, promoting its growth.

However, when the phytotoxic effect of glyphosate is increased with the mixture with bioregulator it can be attributed to the low response of the cultivar to the technologies used. The application of the growth regulator may have caused a hormonal imbalance, promoting glyphosate phytotoxicity.

Zobiole et al. (2010) mentions that the response of each cultivar may be related to its maturity group. Early-cycle cultivars are more affected by phytotoxicity than long-cycle cultivars due to the longer detoxification period by glyphosate or AMPA, which is formed as a product of glyphosate degradation. Thus, it can be seen in the present study that the early-cycle M6210 cultivar presented more injuries after application of the herbicide.

The results of this study contribute to the understanding of these technologies, but more studies are necessary on these and other products and formulations due to the large number of products (fertilizers and growth regulators) available in the market. Studies with different formulations and with other cultivars and under field conditions may offer more results for the basis of the technical recommendations, since for the conditions of this experiment, in pots placed in a greenhouse, there was no difference, but under field conditions the answer may be different.


Differences were observed among cultivars due to genotype characteristics. For the products used in mixture no differences were observed and in the second experiment no phytotoxicity symptom was observed. Based on the results obtained in the present experiment the products did not demonstrate significant effect on the reversion of phytotoxicity caused by glyphosate.



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The authors would like to thank CNPQ – Conselho nacional de Desenvolvimento Científico e Tecnológico, Universidade Federal do Paraná and SUPRA Pesquisa.


Received/recebido: 2019.03.25

Accepted/aceite: 2019.10.23

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