Molecular mechanisms of adaptive evolution revealed by global selection for glyphosate resistance

Gaines, Todd A.; Patterson, Eric; Neve, Paul

doi:10.1111/nph.15858

Cited by 86 publications

(91 citation statements)

References 44 publications

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“…Multiple copies of EPSPS were first discovered in Amaranthus palmeri, and have now been reported for a number of other GR species such as Kochia scoparia and Lolium multiflorum. 31 Gene amplification can confer high levels of resistance (more than ten-fold), but we found no evidence supporting higher number of EPSPS copies in B. subalternans. The two B. subalternans biotypes had the same number of EPSPS gene copies as well as similar EPSPS Figure 5.…”

Section: Epsps Gene Amplificationcontrasting

confidence: 68%

A novel TIPT double mutation in EPSPS conferring glyphosate resistance in tetraploid Bidens subalternans

Takano

Fernandes

Adegas

et al. 2019

Pest Management Science

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BACKGROUND Bidens subalternans (greater beggarticks) is a tetraploid and troublesome weed infesting annual crops in most tropical regions of the world. A glyphosate‐resistant (GR) B. subalternans biotype was detected in a soybean field from Paraguay. A series of physiological and molecular analyses were conducted to elucidate its resistance mechanisms. RESULTS The GR biotype had a high level of resistance (> 15‐fold LD50), relative to a glyphosate‐susceptible (GS) biotype. Shikimate accumulation was up to ten‐fold greater for GS compared with GR. We found no differences in sensitivity when plants were treated and kept under lower (10/4 °C) or higher temperatures (25/20 °C). GS and GR had the same relative EPSPS gene copy number, and similar glyphosate absorption and translocation rates. Neither biotype metabolized glyphosate. A double amino acid substitution (TIPT – Thr102Ile and Pro106Thr) was found in only one EPSPS allele from one of the two EPSPS homoeologs present in tetraploid GR B. subalternans. CONCLUSION This is the first report of a TIPT double mutation conferring high levels of glyphosate resistance in a weed species. The presence of both wild‐type and TIPT mutant EPSPS on the polyploid genome of GR B. subalternans may offset a potential fitness cost, requiring additional research to confirm the absence of deleterious effects. © 2019 Society of Chemical Industry

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Section: Epsps Gene Amplificationcontrasting

confidence: 68%

A novel TIPT double mutation in EPSPS conferring glyphosate resistance in tetraploid Bidens subalternans

Takano

Fernandes

Adegas

et al. 2019

Pest Management Science

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“…Pooled means of GS and GR plants were 0.46 (±0.02) and 0.44 (±0.11) of EPSPS relative expression, respectively. EPSPS overexpression often results from gene duplication in GR plants, requiring greater amounts of glyphosate to inhibit the pool of EPSPS proteins and lead to plant death [12]. While EPSPS gene duplication as a GR mechanism has been reported in eight weed species worldwide [12], it does not contribute to GR in wild poinsettia.…”

Section: Epsps Expressionmentioning

confidence: 99%

“…The most frequent amino acid substitution resulting in GR occurs at Pro106 on EPSPS sequence [6]. At this position, amino acid changes to Ser, Leu, Thr and Ala have been reported [12]. A single mutation at Thr102 has evolved in only one species (Tridax procumbens) [5].…”

Section: Plos Onementioning

confidence: 99%

“…More recently, a GR smooth pigweed (Amaranthus hybridus) population evolved a triple amino acid mutation in EPSPS (Pro102Ser, Ala103Val and Pro106Ser) [10]. Another important TSR mechanism is associated with the overexpression of EPSPS and was first discovered in Palmer amaranth (Amaranthus palmeri) [11] and has now been reported in eight species [12]. In this case, GR plants increase the number of EPSPS copies and, therefore, EPSPS protein, requiring more glyphosate to inhibit the enzyme and lead to plant death.…”

Section: Introductionmentioning

confidence: 99%

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Evolution of EPSPS double mutation imparting glyphosate resistance in wild poinsettia (Euphorbia heterophylla L.)

et al. 2020

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The evolution of glyphosate resistance (GR) in weeds is an increasing problem. Glyphosate has been used intensively on wild poinsettia (Euphorbia heterophylla L.) populations for at least 20 years in GR crops within South America. We investigated the GR mechanisms in a wild poinsettia population from a soybean field in southern Brazil. The GR population required higher glyphosate doses to achieve 50% control (LD 50) and 50% dry mass reduction (MR 50) compared to a glyphosate susceptible (GS) population. The ratio between the LD 50 and MR 50 of GR and GS resulted in resistance factors (RF) of 6.9-fold and 6.1-fold, respectively. Shikimate accumulated 6.7 times more in GS than in GR when leaf-discs were incubated with increasing glyphosate concentrations. No differences were found between GR and GS regarding non-target-site mechanisms. Neither population metabolized glyphosate to significant levels following treatment with 850 g ha-1 glyphosate. Similar levels of 14 C-glyphosate uptake and translocation were observed between the two populations. No differences in EPSPS expression were found between GS and GR. Two target site mutations were found in all EPSPS alleles of homozygous resistant plants: Thr102Ile + Pro106Thr (TIPT-mutation). Heterozygous individuals harbored both alleles, wild-type and TIPT. Half of GR individuals were heterozygous, suggesting that resistance is still evolving in the population. A genotyping assay was developed based on the Pro106Thr mutation, demonstrating high efficiency to identify homozygous, heterozygous or wild-type EPSPS sequences across different plants. This is the first report of glyphosate-resistant wild-poinsettia harboring an EPSPS double mutation (TIPT) in the same plant.

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“…Due to the strong selection pressure of continuous, heavy use of this herbicide in glyphosateresistant crops, many weeds have developed resistance to glyphosate and multiple resistance mechanisms are known (Heap and Duke 2018). These include target site mutations in the EPSPS enzyme itself, as well as other mechanisms including gene amplification of EPSPS (Gaines et al 2010) (Gaines et al 2019) and mutations that increase vacuolar sequestration of glyphosate (Ge et al 2014). In some cases, weed species exhibit combinations of multiple resistance mechanisms (Gherekhloo et al 2017) (Sammons and Gaines 2014).…”

Section: Introductionmentioning

confidence: 99%

Development of non-transgenic glyphosate tolerant wheat by TILLING

Moehs

Austill

Facciotti

et al. 2020

Preprint

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Glyphosate (N-phosphonomethyl-glycine) is the world’s most widely used broad spectrum, post-emergence herbicide. It inhibits the chloroplast-targeted enzyme 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS; EC 2.5.1.19), a component of the plant and microorganism-specific shikimate pathway and a key catalyst in the production of aromatic amino acids. Variants of EPSPS that are not inhibited by glyphosate due to particular amino acid alterations in the active site of the enzyme are known. Some of these variants have been identified in weed species that have developed resistance to glyphosate because of the strong selective pressure of continuous, heavy glyphosate use. We have used TILLING (Targeting Induced Local Lesions in Genomes), a non-transgenic, target-selected, reverse genetics mutation breeding technique, and conventional genetic crosses, to identify and combine, through two rounds of mutagenesis, wheat lines having both T102I and P106S (so-called TIPS enzyme) mutations in both the A and the D sub-genome homoeologous copies of the wheat EPSPS gene. The combined effects of the T102I and P106S mutations are known from previous work in multiple species to minimize the binding of the herbicide while maintaining the affinity of the catalytic site for its native substrates. These novel wheat lines exhibit substantial tolerance to commercially relevant levels of glyphosate.

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Molecular mechanisms of adaptive evolution revealed by global selection for glyphosate resistance

Cited by 86 publications

References 44 publications

A novel TIPT double mutation in EPSPS conferring glyphosate resistance in tetraploid Bidens subalternans

A novel TIPT double mutation in EPSPS conferring glyphosate resistance in tetraploid Bidens subalternans

Evolution of EPSPS double mutation imparting glyphosate resistance in wild poinsettia (Euphorbia heterophylla L.)

Development of non-transgenic glyphosate tolerant wheat by TILLING

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