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Table 5 Overview of publications reporting changes in the composition and phenotype in glyphosate-resistant GE soybeans at different glyphosate dosages

From: Insufficient risk assessment of herbicide-tolerant genetically engineered soybeans intended for import into the EU

StudyParameterResultDosage (if not specified, in kg (a.i.)/ha)
Albrecht et al. [54]Plant heightDecreased1.4/2.8
 Number and weight of seeds per plantDecreased1.4/2.8
 Content of proteinAltered differently; increased when applied at the sixth trifoliate (V6) stage and decreased when applied at full bloom (R2)1.4/2.8
Albrecht et al. [55]Quality of the seedsDecreased0/0.36/0.72/1.08/1.44
 Occurrence of phytopathogensIncreased0/0.36/0.72/1.08/1.44
Barbosa et al. [56]Malondialdehyde, ascorbate peroxidase, glutathione reductase, and catalaseElevated (seed)
 Actin fragment, cytosolic glutamine synthetase, glycinin subunit G1, and glycine-rich RNA-binding proteinExpressed differently (seed)
Barroso and Carvalho [57]Dry mass (leaves, pod, stem, shoot)Increased with three doses of phosphate fertilizer0.9/1.44
 YieldIncreased with three doses of phosphate fertilizer0.9/1.44
Bellaloui et al. [58]ProteinIncreased (seed)1.12/3.36
 OilDecreased (seed)1.12/3.36
 Oleic acidIncreased (seed)1.12/3.36
 Linolenic acidDecreased (seed)1.12/3.36
 N assimilation, as measured by in vivo nitrate reductase activity (NRA) in leaves, roots, and nodulesDecreased1.12/3.36
Bellaloui et al. [59]ProteinIncreased (seed)0.84
 Amino acidsIncreased (not significant) (seed)0.84
 OilDecreased (seed)0.84
 Oleic acidIncreased (seed)0.84
 Linolenic acidDecreased (seed)0.84
 ProlinIncreased (seed)0.84
 Nitrate reductase activity (NRA)Decreased0.84
Bellaloui et al. [60]FeDecreased (seed)0.84
Bohm et al. [61]Number of podsNo effect0.96/1.92
 YieldNo effect0.96/1.92
 N fixationDecreased0.96/1.92
 IsoflavonesDifferences among treatments, GE soy is different from conventional soy, but the effect of glyphosate did not become apparent0.96/1.92
Bøhn et al. [53]Sugar, proteins, Zn, fibre, total saturated fat, omega-6 fatty acidsDecrease of sugars, such as glucose, fructose, sucrose and maltose, decrease of total protein, Zn, increase of fibre, increase of total saturated fat and total omega-6 fatty acids (seed)Average ‘glyphosate equivalents’ of 11.9 mg/kg for the GE soybeans (max. 20.1 mg/kg)
 Ba, Zn, SeDecrease of Ba and Zn, increase of SeAverage ‘glyphosate equivalents’ of 11.9 mg/kg for the GE soybeans (max. 20.1 mg/kg)
Bott et al. [62]Root biomass and root elongationDepressions of plant growth in the glyphosate-resistant soybean cultivar Valiosa strongly dependent on the selected culture conditions0.9/1.8/1.92
 Shoot biomassIn soil culture, shoot biomass production declined by approximately 15–30% in glyphosate treated plants grown on an acidic Arenosol, but not on a calcareous Loess sub-soil, while root biomass was not significantly affected0.9/1.8/1.92
 N fixationNo effect of glyphosate application on N fixation as measured by acetylene reduction assay, soybean yield, or seed N content0.9/1.8/1.92
 Zn in leavesDecreased0.9/1.8/1.92
Cakmak et al. [63]Ca, Mn, Mg, and Fe in leavesDecreased0.3 and 1.2% of field rate
Cavalieri et al. [64]Effect of glyphosate formulations on nutrient accumulation and dry matter production in shoots of two glyphosate-resistant soybean cultivarsRoundup Original®, Roundup Transorb® and Roundup WG® caused the greatest damage to nutrient accumulation and dry matter production. It was concluded that nutrient accumulation and dry matter production in shoots of the soybean plants are affected by glyphosate application, even for glyphosate-resistant cultivars0.96
Cesco et al. [65]YieldDecreased0/0.7/1.4/2.1/2.8/3.6/4.3
 Number of podsDecreased0/0.7/1.4/2.1/2.8/3.6/4.3
Correia [66]N fixationDecreased0.96–6.72
Ding et al. [67]ChlorophyllDecreased and recovery at day 281
 PhotosynthesisDecreased and recovery at day 281
 Stomatal conductance to water vapour and transpiration ratesDecreased1
 Root respiration and shoot N contentDecreased and recovery at day 281
Duke et al. [68]DaidzeinIncreased (seed)1.26/2.1
Duke et al. [69]Plant mineral nutritionRigorous field studies on different soil types (including those highly susceptible to inducing Mn or Fe deficiency in soybeans) are needed to resolve the issue of whether glyphosate might have adverse effects on mineral nutrition of glyphosate-resistant crops0.86
Duke et al. [70]Plant mineral nutritionNo effect0.87
Gomes et al. [71]Plant mineral nutritionDecreased
Huber [72]Uptake and translocation of Fe, Mn and ZnDecreased0.036 (2.5% of recommended rate of glyphosate)
 Mn uptake and efficiencyDecreased1.68
 Root nodulationDecreased
 N fixationDecreased
 Availability of Fe, Mn, and other essential mineral nutrients for crop uptakeDecreased
Krenchinski et al. [73]Chlorophyll and photosynthesisDecreased0/0.72/2.16
 Water use efficiencyNo effect0/0.72/2.16
Lappé et al. [74]Level of phytoestrogens (genistein and daidzein)Decreased
Reddy and Zablotowicz. [75]Chlorophyll content, root and shoot dry weight, or nodule numberNo effect0.84
 Nodule biomassDecreased by 21 to 28% 14 days after the late post-emergence application (28 days after planting)0.84
 Seed proteinDecreased with two applications (seed)0.84
Reddy et al. [76]AMPA, shikimate, glyphosate levels in plantsChlorosis, effects measured until 22 days after treatment1.12/2.24/3.36/4.48/6.72/and 13.44
Sanogo et al. [77]Immunity against Fusarium solani f. sp. glycinesDecreased0.84
Santos et al. [78]N, Ca, Mg, Fe, CuDecreased2
Serra et al. [79]MnNo effect
V8 (20 days after application)
 Fe, Zn, Mn and CuDecreased0/0.6/1.3/1.9/2.6
 N, Mn, Cu, Zn and FeDecreased0/0.6/1.3/1.9/2.6
 Dry massDecreased0/0.6/1.3/1.9/2.6
Petter et al. [80]N, P, K, Ca, Mg, B, Mn, Zn, FeDecreased (leaves)1.08 and 1.8
 Shoot and root dry biomassDecreased1.08/1.8
 Plant heightDecreased1.08/1.8
 Root volumeDecreased1.08/1.8
Vivancos et al. [81]PhotosynthesisDecreased
Wei et al. [82]Content of isoflavonesDepending on duration of soaking and pH of the solution, the results were different. GE soy showed higher and lower isoflavone values
Zablotowicz and Reddy [83]Seed NDecreased, when high doses of glyphosate were applied (seed)0.84/1.68/2.52 + 2.52/0.84 + 0.84
 YieldDecreased0.84/1.68/2.52 + 2.52/0.84 + 0.84
Zobiole et al. [84]Number and weight of seeds per plantDecreased by 25% and 13% (seed)1.2
 17:1n-7 (not essential)Increased (by 30.3%) (seed)1.2
 18:1n-9 (not essential)Increased (by 25%) (seed)1.2
 Linoleic acid (18:2n-6)Decreased (2.3%) (seed)1.2
 Linolenic acid (18:3n-3)Decreased (9.6%) (seed)1.2
Zobiole et al. [85]Photosynthetic parametersDecreased0.6/0.9/1.2/1.8/2.4
 Biomass productionDecreased0.6/0.9/1.2/1.8/2.4
 Water absorptionDecreased0.6/0.9/1.2/1.8/2.4
 Water use efficiencyDecreased0.6/0.9/1.2/1.8/2.4
Zobiole et al. [86]Shoot and root dry biomassDecreased1.2
 Photosynthetic parametersDecreased1.2
 Micronutrients (Zn, Mn, Fe, Cu, B) in leavesDecreased1.2
 Macronutrients (N, P, K, Mg, Ca, S)Decreased (but no effect on N)1.2
Zobiole et al. [87]Photosynthetic parameters (A, SPAD, Fo, Fm)Linear decrease, R1 growth stage
Long-term physiological impacts
 Macronutrients (N, P, K, Mg, Ca, S)Decreased. Effects in the following order: Ca > Mg > N > S > K > P0.6/0.9/1.2/1.8/2.4
 Micronutrients (Fe, Co, Zn, Mn, Cu, Mo, B)Effects of single application in the following order: Fe > Mn > Co > Zn > Cu > B > Mo
Two applications: Fe > Co > Zn > Mn > Cu > Mo > B
 Shoot, root and total biomass dry weightDecreased proportional to glyphosate dose0.6/0.9/1.2/1.8/2.4
Zobiole et al. [88]Photosynthetic rateSeverely decreased
RR2 more sensitive than RR1
 Leaf area and shoot biomass productionSeverely decreased
RR2 more sensitive than RR1
Zobiole et al. [89]Photosynthetic rateAt the 1.8 kg (a.i.) dose: reduction 33 and 31%0.45/0.67/0.9/1.35/1.8
 Lignin and amino acid contentDecreased (linear)0.45/0.67/0.9/1.35/1.8
 Height and total (shoot and root) dry weightDecreased (linear)0.45/0.67/0.9/1.35/1.8
Zobiole et al. [90]Nodule numberDecreased1.2
 Ni concentrationDecreased1.2
 Chlorophyll (SPAD units)Lower in RR soybean
Even lower when treated with glyphosate
  Chlorotic symptoms, non-persistent1.2
Zobiole et al. [91]Fusarium spp.Increased in RR1 and RR2 soybean0.8/1.2/2.4
 Mn reducers ⁄Mn oxidizers ratioDecreased in RR1; The greatest reduction in the ratio of potential Mn reducers ⁄Mn oxidizers occurred when glyphosate was applied at early (V2) compared with later growth stages (V4 and V6)0.8/1.2/2.4
 Root and shoot dry weightDecreased in RR1 and RR2 soybean
Earlier glyphosate applications caused greater decreases in root dry weight. Shoot dry weight of both varieties was most reduced when glyphosate was applied at the V6 growth stage and least at V4 and V2 stages, with the RR2 cultivar affected more than the RR1 cultivar. In general, RR2 produced less biomass (shoot and root) than RR1 when glyphosate was not applied
Zobiole et al. [92]ChlorophyllDecreased0.8/1.2/2.4
 Macro- (N, P, Mg, K, Ca, Mg, S) and micronutrients (Zn, Mn,
Fe, Cu, B) accumulation
All macro- and micronutrients, with exception of N and K, accumulated more in RR1 than RR20.8/1.2/2.4
 Nodule dry weight and numberReduced tendency for late applications to have less effect than early applications0.8/1.2/2.4
 Shoot biomassDecreased
Higher percent reduction associated with late than with early glyphosate applications
 ChlorosisThe new generation RR2 soybeans also showed undesirable glyphosate effects as ‘‘yellow flashing’’0.8/1.2/2.4
Zobiole et al. [52]Photosynthetic rateSeverely decreased0.8/1.2/2.4
 Macro- and micronutrient accumulationsProportionally decreased as glyphosate rates increased and applications were delayed. Macronutrient and all micronutrient concentrations except Cu were within the nutrient-sufficiency ranges for soybean. Concentrations of Ca, Mg, S, and Cu were significantly (p < 5%) lower in glyphosate-treated soybean, yet all values were within the sufficiency ranges to provide acceptable soybean growth. Concentrations of P and Fe appeared to be increased by glyphosate0.8/1.2/2.4
 Nodule number and dry weightSignificantly decreased
In contrast with other results, a tendency was noted for reduced effects at late applications compared with early applications
 Root dry weightMore severely depressed with glyphosate applied at V2 growth stage compared with V6 growth stage0.8/1.2/2.4
 Leaf area and shoot dry weightMore strongly decreased at the late growth stage than at the early stage0.8/1.2/2.4
  1. Most changes relate to compounds, while some relate to phenotypic characteristics. Unless indicated, all results were statistically significant