Table 5 Overview of publications reporting changes in the composition and phenotype in glyphosate-resistant GE soybeans at different glyphosate dosages
| Study | Parameter | Result | Dosage (if not specified, in kg (a.i.)/ha) |
|---|---|---|---|
| Albrecht et al. [54] | Plant height | Decreased | 1.4/2.8 |
| Number and weight of seeds per plant | Decreased | 1.4/2.8 | |
| Content of protein | Altered 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 seeds | Decreased | 0/0.36/0.72/1.08/1.44 |
| Occurrence of phytopathogens | Increased | 0/0.36/0.72/1.08/1.44 | |
| Yield | Decreased | 0/0.36/0.72/1.08/1.44 | |
| Barbosa et al. [56] | Malondialdehyde, ascorbate peroxidase, glutathione reductase, and catalase | Elevated (seed) | – |
| Actin fragment, cytosolic glutamine synthetase, glycinin subunit G1, and glycine-rich RNA-binding protein | Expressed differently (seed) | – | |
| Barroso and Carvalho [57] | Dry mass (leaves, pod, stem, shoot) | Increased with three doses of phosphate fertilizer | 0.9/1.44 |
| Yield | Increased with three doses of phosphate fertilizer | 0.9/1.44 | |
| Bellaloui et al. [58] | Protein | Increased (seed) | 1.12/3.36 |
| Oil | Decreased (seed) | 1.12/3.36 | |
| Oleic acid | Increased (seed) | 1.12/3.36 | |
| Linolenic acid | Decreased (seed) | 1.12/3.36 | |
| N assimilation, as measured by in vivo nitrate reductase activity (NRA) in leaves, roots, and nodules | Decreased | 1.12/3.36 | |
| Bellaloui et al. [59] | Protein | Increased (seed) | 0.84 |
| Amino acids | Increased (not significant) (seed) | 0.84 | |
| Oil | Decreased (seed) | 0.84 | |
| Oleic acid | Increased (seed) | 0.84 | |
| Linolenic acid | Decreased (seed) | 0.84 | |
| Prolin | Increased (seed) | 0.84 | |
| Nitrate reductase activity (NRA) | Decreased | 0.84 | |
| Bellaloui et al. [60] | Fe | Decreased (seed) | 0.84 |
| Bohm et al. [61] | Number of pods | No effect | 0.96/1.92 |
| Yield | No effect | 0.96/1.92 | |
| N fixation | Decreased | 0.96/1.92 | |
| Isoflavones | Differences among treatments, GE soy is different from conventional soy, but the effect of glyphosate did not become apparent | 0.96/1.92 | |
| Bøhn et al. [53] | Sugar, proteins, Zn, fibre, total saturated fat, omega-6 fatty acids | Decrease 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, Se | Decrease of Ba and Zn, increase of Se | Average ‘glyphosate equivalents’ of 11.9 mg/kg for the GE soybeans (max. 20.1 mg/kg) | |
| Bott et al. [62] | Root biomass and root elongation | Depressions of plant growth in the glyphosate-resistant soybean cultivar Valiosa strongly dependent on the selected culture conditions | 0.9/1.8/1.92 |
| Shoot biomass | In 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 affected | 0.9/1.8/1.92 | |
| N fixation | No effect of glyphosate application on N fixation as measured by acetylene reduction assay, soybean yield, or seed N content | 0.9/1.8/1.92 | |
| Zn in leaves | Decreased | 0.9/1.8/1.92 | |
| Cakmak et al. [63] | Ca, Mn, Mg, and Fe in leaves | Decreased | 0.3 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 cultivars | Roundup 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 cultivars | 0.96 |
| Cesco et al. [65] | Yield | Decreased | 0/0.7/1.4/2.1/2.8/3.6/4.3 |
| Height | Decreased | 0/0.7/1.4/2.1/2.8/3.6/4.3 | |
| Number of pods | Decreased | 0/0.7/1.4/2.1/2.8/3.6/4.3 | |
| Photosynthesis | Decreased | 0/0.7/1.4/2.1/2.8/3.6/4.3 | |
| Correia [66] | N fixation | Decreased | 0.96–6.72 |
| Ding et al. [67] | Chlorophyll | Decreased and recovery at day 28 | 1 |
| Photosynthesis | Decreased and recovery at day 28 | 1 | |
| Stomatal conductance to water vapour and transpiration rates | Decreased | 1 | |
| Root respiration and shoot N content | Decreased and recovery at day 28 | 1 | |
| Duke et al. [68] | Daidzein | Increased (seed) | 1.26/2.1 |
| Duke et al. [69] | Plant mineral nutrition | Rigorous 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 crops | 0.86 |
| Duke et al. [70] | Plant mineral nutrition | No effect | 0.87 |
| Gomes et al. [71] | Plant mineral nutrition | Decreased | – |
| Photosynthesis | Decreased | – | |
| Huber [72] | Uptake and translocation of Fe, Mn and Zn | Decreased | 0.036 (2.5% of recommended rate of glyphosate) |
| Mn uptake and efficiency | Decreased | 1.68 | |
| Root nodulation | Decreased | – | |
| N fixation | Decreased | – | |
| Availability of Fe, Mn, and other essential mineral nutrients for crop uptake | Decreased | – | |
| Krenchinski et al. [73] | Chlorophyll and photosynthesis | Decreased | 0/0.72/2.16 |
| Water use efficiency | No effect | 0/0.72/2.16 | |
| Lappé et al. [74] | Level of phytoestrogens (genistein and daidzein) | Decreased | – |
| Reddy and Zablotowicz. [75] | Chlorophyll content, root and shoot dry weight, or nodule number | No effect | 0.84 |
| Nodule biomass | Decreased by 21 to 28% 14 days after the late post-emergence application (28 days after planting) | 0.84 | |
| Seed protein | Decreased with two applications (seed) | 0.84 | |
| Reddy et al. [76] | AMPA, shikimate, glyphosate levels in plants | Chlorosis, effects measured until 22 days after treatment | 1.12/2.24/3.36/4.48/6.72/and 13.44 |
| Sanogo et al. [77] | Immunity against Fusarium solani f. sp. glycines | Decreased | 0.84 |
| Santos et al. [78] | N, Ca, Mg, Fe, Cu | Decreased | 2 |
| Serra et al. [79] | Mn | No effect V8 (20 days after application) | 0/0.6/1.3/1.9/2.6 |
| Fe, Zn, Mn and Cu | Decreased | 0/0.6/1.3/1.9/2.6 | |
| N, Mn, Cu, Zn and Fe | Decreased | 0/0.6/1.3/1.9/2.6 | |
| Nodes | Decreased | 0/0.6/1.3/1.9/2.6 | |
| Dry mass | Decreased | 0/0.6/1.3/1.9/2.6 | |
| Petter et al. [80] | N, P, K, Ca, Mg, B, Mn, Zn, Fe | Decreased (leaves) | 1.08 and 1.8 |
| Shoot and root dry biomass | Decreased | 1.08/1.8 | |
| Plant height | Decreased | 1.08/1.8 | |
| Root volume | Decreased | 1.08/1.8 | |
| Vivancos et al. [81] | Photosynthesis | Decreased | – |
| Wei et al. [82] | Content of isoflavones | Depending 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 N | Decreased, when high doses of glyphosate were applied (seed) | 0.84/1.68/2.52 + 2.52/0.84 + 0.84 |
| Yield | Decreased | 0.84/1.68/2.52 + 2.52/0.84 + 0.84 | |
| Zobiole et al. [84] | Number and weight of seeds per plant | Decreased 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 parameters | Decreased | 0.6/0.9/1.2/1.8/2.4 |
| Biomass production | Decreased | 0.6/0.9/1.2/1.8/2.4 | |
| Water absorption | Decreased | 0.6/0.9/1.2/1.8/2.4 | |
| Photosynthesis | Decreased | 0.6/0.9/1.2/1.8/2.4 | |
| Water use efficiency | Decreased | 0.6/0.9/1.2/1.8/2.4 | |
| Zobiole et al. [86] | Shoot and root dry biomass | Decreased | 1.2 |
| Photosynthetic parameters | Decreased | 1.2 | |
| Micronutrients (Zn, Mn, Fe, Cu, B) in leaves | Decreased | 1.2 | |
| 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 | 0.6/0.9/1.2/1.8/2.4 |
| Macronutrients (N, P, K, Mg, Ca, S) | Decreased. Effects in the following order: Ca > Mg > N > S > K > P | 0.6/0.9/1.2/1.8/2.4 | |
| 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 | 0.6/0.9/1.2/1.8/2.4 | |
| Shoot, root and total biomass dry weight | Decreased proportional to glyphosate dose | 0.6/0.9/1.2/1.8/2.4 | |
| Zobiole et al. [88] | Photosynthetic rate | Severely decreased RR2 more sensitive than RR1 | 0.8/1.2/2.4 |
| Leaf area and shoot biomass production | Severely decreased RR2 more sensitive than RR1 | 0.8/1.2/2.4 | |
| Zobiole et al. [89] | Photosynthetic rate | At 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 content | Decreased (linear) | 0.45/0.67/0.9/1.35/1.8 | |
| Height and total (shoot and root) dry weight | Decreased (linear) | 0.45/0.67/0.9/1.35/1.8 | |
| Zobiole et al. [90] | Nodule number | Decreased | 1.2 |
| Ni concentration | Decreased | 1.2 | |
| Chlorophyll (SPAD units) | Lower in RR soybean Even lower when treated with glyphosate | 1.2 | |
| Chlorotic symptoms, non-persistent | 1.2 | ||
| Zobiole et al. [91] | Fusarium spp. | Increased in RR1 and RR2 soybean | 0.8/1.2/2.4 |
| Mn reducers ⁄Mn oxidizers ratio | Decreased 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 weight | Decreased 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 | 0.8/1.2/2.4 | |
| Zobiole et al. [92] | Chlorophyll | Decreased | 0.8/1.2/2.4 |
| 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 RR2 | 0.8/1.2/2.4 | |
| Nodule dry weight and number | Reduced tendency for late applications to have less effect than early applications | 0.8/1.2/2.4 | |
| Shoot biomass | Decreased Higher percent reduction associated with late than with early glyphosate applications | 0.8/1.2/2.4 | |
| Chlorosis | The new generation RR2 soybeans also showed undesirable glyphosate effects as ‘‘yellow flashing’’ | 0.8/1.2/2.4 | |
| Zobiole et al. [52] | Photosynthetic rate | Severely decreased | 0.8/1.2/2.4 |
| Macro- and micronutrient accumulations | Proportionally 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 glyphosate | 0.8/1.2/2.4 | |
| Nodule number and dry weight | Significantly decreased In contrast with other results, a tendency was noted for reduced effects at late applications compared with early applications | 0.8/1.2/2.4 | |
| Root dry weight | More severely depressed with glyphosate applied at V2 growth stage compared with V6 growth stage | 0.8/1.2/2.4 | |
| Leaf area and shoot dry weight | More strongly decreased at the late growth stage than at the early stage | 0.8/1.2/2.4 |
