Mutation in Amaranthus hybridus reduces growth without glyphosate

The TAP-IVS triple mutation, identified in the EPSPS gene of Amaranthus hybridus, confers high resistance to the herbicide glyphosate. This discovery represents a breakthrough in understanding the rapid adaptation of weeds in agricultural environments. However, the study points to a significant adaptive cost: in herbicide-free environments, plants with the mutation lose competitiveness compared to susceptible ones.

The study evaluated the performance of glyphosate-resistant and -susceptible genotypes under conditions with and without resource competition. The results indicate that, while resistance ensures survival in herbicide-treated environments, it compromises plant growth and reproduction in herbicide-free environments.

Rare and potent mutation

The TAP-IVS mutation combines three alterations in the EPSPS gene: T102I, A103V, and P106S. This combination has never been reported in plants. It renders the EPSPS enzyme virtually insensitive to glyphosate.

In biochemical tests, the mutated variant showed a 0,3-fold decrease in catalytic efficiency compared to the wild-type enzyme. This loss of efficiency compromises the plant's metabolism and helps explain the performance penalty observed in a competitive environment.

Glyphosate resistance based on mutations in the enzyme's target site is common, but multiple mutations like TAP-IVS are rare. This rarity suggests an evolutionary barrier: the high biological cost may hinder the spread of these mutations in natural populations without constant selective pressure.

Impact under competition

In an environment without competition, resistant plants showed no obvious growth impairment. In some cases, they even outperformed susceptible plants in terms of vegetative biomass. However, the situation changes dramatically when competition arises.

Resistant plants lost height, reduced stem biomass by up to 93%, and decreased lateral branch production by 99% when competing with susceptible plants.

Inflorescence production also decreased by between 66% and 92% under these conditions. These data indicate that the mutation confers significant disadvantages in environments where the plant must compete for light and nutrients.

The proportion of biomass allocated to reproduction remained similar across genotypes. However, the absolute value of resources allocated by resistant plants fell sharply, reflecting the limitation in vegetative growth.

The minimum biomass required to initiate reproduction was lower in resistant species, suggesting an attempt to compensate for limited resources.

Biochemical confirmation

Four variants of the EPSPS enzyme A. hybridus were expressed in E. coli to measure their efficiency and sensitivity to glyphosate. The versions with the P106S, TIPS, and TAP-IVS mutations showed increasing resistance to the herbicide. Conversely, all showed a significant decrease in catalytic activity.

The TAP-IVS variant showed the greatest reduction in the maximum enzymatic reaction rate (Vmax), confirming a metabolic limitation imposed by the mutation. The study concludes that this enzyme deficiency partly explains the reduced performance of resistant plants under natural competitive conditions.

Implications for agriculture

Despite the adaptive cost, the TAP-IVS mutation has sparked interest in genetic engineering. It has already been successfully introduced into rice and corn using precision gene editing techniques, such as "prime editing." In these crops, the impact of the biological cost can be offset by gene overexpression, a common practice in commercial GMOs.

The study indicates that simply assessing the effectiveness of resistance is not enough. It is necessary to consider the ecological and agronomic consequences of introducing these mutations into commercial crops.

In weeds, the high cost may limit the natural spread of the mutation. In crops, its viability will depend on technical adjustments that offset the loss of metabolic efficiency.

Further information at doi.org/10.1016/j.plantsci.2025.112731